available online at www.studiesinmycology.org
doi:10.3114/sim.2011.70.02
StudieS in Mycology 70: 53–138. 2011.
Taxonomy of Penicillium section Citrina
J. Houbraken1,3, J.C. Frisvad2 and R.A. Samson1
1
CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands; 2Department of Systems Biology, Building 221, Technical University of Denmark,
DK-2800 Kgs. Lyngby, Denmark; 3Microbiology, Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands.
*Correspondence: Jos Houbraken, j.houbraken@cbs.knaw.nl
Abstract: Species of Penicillium section Citrina have a worldwide distribution and occur commonly in soils. The section is here delimited using a combination of phenotypic
characters and sequences of the nuclear ribosomal RNA gene operon, including the internal transcribed spacer regions ITS1 and ITS2, the 5.8S nrDNA (ITS) and partial RPB2
sequences. Species assigned to section Citrina share the production of symmetrically biverticillate conidiophores, lask shaped phialides (7.0–9.0 µm long) and relatively
small conidia (2.0–3.0 µm diam). Some species can produce greyish-brown coloured cleistothecia containing langed ascospores. In the present study, more than 250 isolates
presumably belonging to section Citrina were examined using a combined analysis of phenotypic and physiological characters, extrolite proiles and ITS, β-tubulin and/or
calmodulin sequences. Section Citrina includes 39 species, and 17 of those are described here as new. The most important phenotypic characters for distinguishing species
are growth rates and colony reverse colours on the agar media CYA, MEA and YES; shape, size and ornamentation of conidia and the production of sclerotia or cleistothecia.
Temperature-growth proiles were made for all examined species and are a valuable character characters for species identiication. Species centered around P. citrinum
generally have a higher maximum growth temperature (33–36 °C) than species related to P. westlingii (27–33 °C). Extrolite patterns and partial calmodulin and β-tubulin
sequences can be used for sequence based identiication and resolved all species. In contrast, ITS sequences were less variable and only 55 % of the species could be
unambiguously identiied with this locus.
Key words: citreoviridin, citrinin, soil fungi, taxonomy, phylogeny.
Taxonomic novelties: Penicillium argentinense Houbraken, Frisvad & Samson, P. atrofulvum Houbraken, Frisvad & Samson, P. aurantiacobrunneum Houbraken, Frisvad
& Samson, P. cairnsense Houbraken, Frisvad & Samson, P. christenseniae Houbraken, Frisvad & Samson, P. copticola Houbraken, Frisvad & Samson, P. cosmopolitanum
Houbraken, Frisvad & Samson, P. neomiczynskii Cole, Houbraken, Frisvad & Samson, P. nothofagi Houbraken, Frisvad & Samson, P. pancosmium Houbraken, Frisvad &
Samson, P. pasqualense Houbraken, Frisvad & Samson, P. quebecense Seifert, Houbraken, Frisvad & Samson, P. raphiae Houbraken, Frisvad & Samson, P. terrigenum Seifert,
Houbraken, Frisvad & Samson, P. ubiquetum Houbraken, Frisvad & Samson, P. vancouverense Houbraken, Frisvad & Samson, P. wellingtonense Cole, Houbraken, Frisvad
& Samson.
INTroducTIoN
Raper & Thom (1949) introduced the “Penicillium citrinum series”
for Penicillium species with restricted growth on Czapek’s agar
and producing terminal verticils of metulae in combination with
relatively small conidia (2.5–3.2 µm). Penicillium citrinum, P.
corylophilum and P. steckii were classiied in this series. Ramírez
(1982) followed Raper & Thom’s concept, and added P. matritii. Pitt
(1980) formalised series Citrina, and using similar criteria as Raper
& Thom, he accepted seven species: P. citrinum, P. corylophilum,
P. miczynskii, P. humuli, P. herquei, P. paxilli and P. inlatum. In his
description of series Citrina, Pitt (1980) noted that it encompasses
a rather diverse collection of species, which in some cases show
relatively little afinity with each other. This observation was
supported by the taxonomic and phylogenetic study of Houbraken
et al. (2010). Seven species were recognised in series Citrina,
and of all the species mentioned above, only P. citrinum and P.
steckii were maintained. Peterson (2000) was among the irst to
study the phylogeny of Penicillium with sequence data. Using ITS
sequences, he constructed a phylogeny of Penicillium and showed
that P. citrinum is related to P. westlingii, P. sumatrense, P. paxilli, P.
waksmanii, P. miczynskii, Eupenicillium anatolicum and E. shearii.
Recently, a new sectional classiication for Penicillium was proposed
and section Citrina was introduced (Houbraken & Samson 2011).
This classiication was based on a combined analysis of sequence
data of four loci and the species belonging to section Citrina are
the same as those belonging to Peterson’s group 1. Peterson et al.
(2004) and Houbraken et al. (2010) studied certain species of this
section in more detail, however, a modern overview of species and
their synonyms is lacking.
Members of section Citrina are very abundant and have a
worldwide distribution. It is even claimed that P. citrinum may well
be one of the most commonly occurring eukaryotic life forms on
earth (Pitt 1980). Species of this section are very common in soil,
but are also isolated from indoor environments and foodstuffs (Pitt
& Hocking 2009, Samson et al. 2010). The distribution of species
appears to be climate-related. Penicillium citrinum is more common
in (sub)tropical soils, and present only in low numbers in soils from
temperate regions (the Netherlands, Poland, Canada), where P.
westlingii and related species predominate.
Members of section Citrina are also known for their ability to
produce the mycotoxins citrinin and citreoviridin. The nephrotoxic
compound citrinin is consistently produced by P. citrinum, but also by
other related species including P. gorlenkoanum, P. hetheringtonii,
P. miczynskii, P. chrzaszczii, P. manginii and P. westlingii, and
citreoviridin is produced by P. miczynskii and P. manginii (Pollock
1947, Frisvad 1989, Frisvad & Filtenborg 1990, Frisvad et al. 2006,
Houbraken et al. 2010). Many other extrolites are reported to be
produced by members of section Citrina; however, some of these
extrolites are erroneously linked to certain species (Frisvad 1989,
Frisvad & Filtenborg 1990, Houbraken et al. 2010).
Copyright 2011 CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
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53
Houbraken et al.
Table 1. Isolates in Penicillium section Citrina examined in this study.
Species
cBS no.
other numbers
DTO 23A1 = IBT 30775
Contaminant of CBS 316.67
CBS 308.89
CBS H-20648 = DTO 23E6 = IBT 30768
Soil, Keewadin Island, Florida, USA
CBS 467.67
CBS H-20647 = DTO 23A2 = CSIR 1095 = IBT
30763
Sandy soil, Kosi Bay, Natal, South Africa
CBS 478.66T
DTO 22I5 = DTO 22I6 = ATCC 18621 = CSIR 940
= IFO 31729 = IMI 136242 = IBT 30765
Soil, Turkey
CBS 479.66
DTO 22I6 = IBT 16177 = IBT 30764
Soil, Turkey
CBS 130371T
CBS H-20641 = DTO 16B7 = IBT 30761
Soil, Valdes Peninsula peninsula, prov. Chubet, Argentinia
CBS 130373
DTO 18B1 = IBT 30760
Soil, Spaanderswoud, Bussum, the Netherlands
CBS 130374
DTO 18B6 = IBT 30761
Soil, Spaanderswoud, Bussum, the Netherlands
CBS 130381
DTO 132D5
Phaenocoma leaf bracts, South Africa
CBS 109.66
CBS H-20650 = DTO 31B2 = FRR 799 = IBT
30032 = IBT 29667
Soil, Katanga, Zaire
CBS 126331
DTO 120G7
Soil of oak forest; Ras Rajel, Tunesia
CBS 126332
DTO 118D4
Soil of oak forest; Fey el Rih, Tunesia
CBS 261.64
DTO 22H4 = IBT 16171
Unrecorded source, the Netherlands
CBS 126228T
CBS H-20662 = DTO 78G2 = IBT 18753
Air sample, Cake factory, Give, Denmark
CBS 126229
DTO 82C3 = IBT 23001
Soil, Nothofagus sp., Chile
CBS 126230
DTO 82C9 = IBT 29145
Wood litter, Eves Bush, Marlborough, New Zealand
CBS 126277
DTO 76D1 = IBT 29115
Soil, New Zealand
CBS 117962
DTO 55A5 = KAS 2100 = IBT 29675
Decaying basidioma of Lactarius sp.; Algonquin Park, Ontario, Canada,
45.593086° -78.519914°
CBS 117982
DTO 5A7 = KAS 2122 = IBT 29857
Nut of Carya cordiformis (bitternut); Fireman’s Park, Niagara Falls,
Ontario, Canada, 43.142051° -79.115903°
CBS 118028
CBS H-20653 = DTO 55B2 = KAS 2178
Ants (Camponotus spp.), New Brunswick, Canada
CBS 124324
DTO 30B9 = IBT 29068
Soil, near lake Barrine, Australia
CBS 124325T
DTO 30E6 = IBT 29042
Soil, Atherton Tableland, Australia
CBS 124326
DTO 30E8 = IBT 29069
Soil, Atherton Tableland, Australia
CBS 126225
DTO 82B6 = IBT 18352 = CCRC 33163
Soil, Sun-Moon Lake, Nantou County, Taiwan
CBS 126226
DTO 85A4 = IBT 30006
Soil, 2 mtr. from road, Ranomafana, Madagascar
CBS 126236T
CBS H-20656 = DTO 76C3 = IBT 23355
Soil in native forest near base of aerial tram. “Lowland forest” east /
north east side of Costa Rica about 30 km inland from Limon and the
Caribbean
CBS 126237
DTO 78A5 = RMF 9554 = IBT 18183
Litter of Manilkara bidenta or Guarea guidonia, rainforest, El verde in the
Luquillo Experimental Forest, Caribbean National Forest, Puerto Rico
CBS 124320
DTO 42A8 = IBT 30635
Soil, Poland
CBS 126430
DTO 42G9 = IBT 30634
Soil, Poland
CBS 176.81
DTO 23D7 = ATCC 42242 = IJFM 7097 = VKM
F-2198 = IBT 16265
Type of P. turolense; leaves litter of Fagus silvatica, near Nancy, France
CBS 217.28T
22E4 = FRR 903 = MUCL 29167 = NRRL 903
= NRRL 1741 = IBT 18226 = IBT 11222 = IBT
16409
Woodland soil, Puszcza Bialowieska Forest, Poland
CBS 101275
DTO 23G2 = IBT 29060
Leaf, Panama
CBS 115992
DTO 23G6
Compost, the Netherlands
P. anatolicum
P. argentinense
P. atrofulvum
P. aurantiacobrunneum
P. cairnsense
P. christenseniae
P. chrzaszczii
P. citrinum
54
T
Substrate and locality
CBS 117.64
DTO 22H3 = IBT 30003
Epoxy softener, the Netherlands
CBS 122394
DTO 7B8
Soil, Malaysia
CBS 122395
DTO 20A3
Coconut milk; produced in Indonesia, imported into the Netherlands
CBS 122397
DTO 6D6
Soil, Treasure Island, Florida, USA
CBS 122398
DTO 31F9
Peanut, Indonesia
CBS 122451
DTO 48C2 = NRRL 2145 = IBT 16140
Color mutant; unrecorded source
CBS 122452
DTO 32B6 = IBT 30061
Color mutant, coffee beans, Thailand
CBS 122726
DTO 58A4 = NRRL 783 = IBT 16149
Representative of P. sartoryi, unrecorded source
taxonoMy of Penicillium Section citrina
Table 1. (Continued).
Species
cBS no.
other numbers
Substrate and locality
P. citrinum
CBS 139.45
DTO 22F3 = ATCC 1109 = ATCC 36382 = CECT
2269 = FRR 1841 = IMI 091961 = IMI 092196 =
MUCL 29781 = NRRL 1841 = IBT 16200 = NRRL
1842 = IBT 16207
Type of P. citrinum and P. auriluum, unrecorded source
CBS 232.38
DTO 37B7 = Thom 4733.73 = IBT 21675
Type of P. implicatum; unrecorded source
CBS 241.85
IMI 092267 = MUCL 29788 = IBT 21934
Type of P. phaeojanthinellum; unrecorded source
CBS 252.55
DTO 22G4 = ATCC 12068 = FRR 3463 = NRRL
3463 = QM 6946 = IBT 19474
Isotype of P. botryosum; herbarium specimen, Recife, Brazil
DTO 23F8
Patient with acute myeloid leukemia, autopsy of lung and pericardium
T
CBS 865.97
P. copticola
CBS 127355
CBS H-20643 = DTO 19H7 = IBT 30771
Tortilla, USA
CBS 127356
DTO 104E8 = IBT 30772
Dried lower of Cannabis, the Netherlands
CBS 130382
DTO 162G5
Air of a toilet in a kindergarten, Trier, Germany
DTO 82C8 = IBT 29104
Forest soil, Hokitika, New Zealand
T
P. cosmopolitanum
P. decaturense
P. euglaucum
DTO 42G4 = IBT 29692
Soil, Poland
CBS 122406
DTO 17E3
Soil under oak, Spaanderswoud, Bussum, the Netherlands
CBS 122435
DTO 38D6 = IBT 29040
Organic soil of mixed forest, Rijnsweerd, Utrecht
CBS 124315
DTO 42F6 = IBT 30684
Soil, Poland
CBS 124316
DTO 42D3 = IBT 29677
Soil, Poland
CBS 126990
DTO 42F4 = IBT 30691
Soil, Poland
CBS 126991
DTO 42G6 = IBT 30693
Soil, Poland
CBS 126992
DTO 41B1 = IBT 30719
Soil, Poland
CBS 126993
DTO 40E9 = IBT 30690
Soil, Poland
CBS 126994
DTO 40I4 = IBT 30697
Soil, Poland
CBS 126995T
CBS H-20665 = DTO 92E8 = IBT 30681
Soil heathland, Cartier heide, Eersel, the Netherlands
CBS 126996
DTO 42G1 = IBT 30683
Soil, Poland
CBS 126997
DTO 42A1 = IBT 29690
Soil, Poland
CBS 126998
DTO 41A4 = IBT 30757
Soil, Poland
CBS 126999
DTO 39D5 = IBT 30687
Soil, Poland
CBS 127000
DTO 92G6 = IBT 30678
Soil heathland, Cartier heide, Eersel, the Netherlands
CBS 127001
DTO 92E9 = IBT 30682
Soil heathland, Cartier heide, Eersel, the Netherlands
CBS 127002
DTO 42E1 = IBT 30680
Soil, Poland
CBS 127038
DTO 76B6 = IBT 21692
Soil, near Lyngby Lake, Denmark
CBS 200.86
DTO 23E4 = IBT 16144 = IBT 29697
Root of Pseudotsuga menziesii, the Netherlands
CBS 251.70
DTO 23B1 = IBT 29071
Root of gymnosperm, Denmark
CBS 552.86
DTO 23E5 = IBT 29681 = IBT 30689
Root of Pseudotsuga menziesii, the Netherlands
CBS 586.70
DTO 23B5 = IBT 30686
Root of gymnosperm, Denmark
CBS 637.70
DTO 23B6
Root of gymnosperm, Denmark
CBS 117504
DTO 3A9 = IBT 27057 = NRRL 29675
Trichaptum biformis, on dead hardwood branch, Chehaw Park, Albany,
Georgia, USA
CBS 117505
DTO 3B1 = IBT 27058 = NRRL 29708
Basidiomycete on dead hardwood, Reed Bingham State park (hardwood
swamp area), Adel, Georgia, USA
CBS 117506
DTO 3B2 = IBT 27059 = NRRL 29828
Trichaptum biformis, on dead hardwood branch, Wakulla Springs State
Park, Crawfordsville, Florida, USA
CBS 117507
DTO 3F5 = IBT 27111 = NRRL 28160
Ischnoderma, old basidiomata, found on dead hardwood log, North
Picture Ridge Road, Peoria, Illinois, USA
CBS 117508
DTO 3F6 = IBT 27114 = NRRL 29840
Polypore found on a dead pine branch, Blountstown, Torreya State Park,
Illinois, USA
CBS 117509T
DTO 3F7 = IBT 27117 = NRRL 28152
Old resupinate fungus, Ramsey Lake State Park, Decatur, Illinois, USA
CBS 117510
DTO 3F8 = IBT 27120 = NRRL 28119
Wood decaying fungus
CBS 119390
DTO 9F2 = IBT 27868 = NRRL 29807
Pyrenomycete stroma on dead hardwood; sabal palm swamp, Hickory
Mounds, Florida, USA
CBS 130372
DTO 16G1 = IBT 30776
Soil, Azul, prov. Buenos Aires, Argentina
CBS 323.71NT
DTO 23B9 = IBT 30767
Soil, Argentina
www.studiesinmycology.org
55
Houbraken et al.
Table 1. (Continued).
Species
cBS no.
other numbers
Substrate and locality
P. gallaicum
CBS 164.81
DTO 34G2 = IJFM 7026 = IMI 253797 = VKM
F-2193 = IBT 22014
Type of P. alicantinum; air, Madrid, Spain
CBS 167.81T
DT 34G3 = IJFM 5597 = DTO 34G3 = ATCC
42232 = IMI 253794 = VKM F-2190 = IBT 22016
Air, Madrid, Spain
CBS 418.69
DTO 23A9 = NRRL 3759 = IBT 30046 = IMI
140303 = FRR 519
Type of P. syriacum nomen dubium; soil, Berza, Damascus, Syria
CBS 117273
DTO 2H8 = IBT 29661
Butter, the Netherlands
CBS 124319
DTO 39C7 = IBT 29678
Soil, Bialowieska, Poland
CBS 126419
DTO 40E3 = IBT 30692
Soil, Bialowieska, Poland
CBS 126420
DTO 39C4 = IBT 30637
Soil, Bialowieska, Poland
CBS 126421
DTO 42G2 = IBT 30636
Soil, Bialowieska, Poland
CBS 126422
DTO 76B5 = IBT 21219
Sand under pine, summit of Eagle Rock, Medicine Bow National Forest
near Laramie, Wyoming, USA
CBS 126423
DTO 42E7 = IBT 30638
Soil, Bialowieska, Poland
CBS 126424
DTO 58C6 = IBT 30640
Unknown substrate, Germany
CBS 215.28T
DTO 22E2 = ATCC 10449 = ATCC 48714 = FRR
2111 = I FO 7724 = IMI 040591 = MUCL 29243 =
NRRL 2111 = QM 7566 = VKM F-1826
Soil under pine, Bialowieska, Poland
CBS 218.28
ATCC 10457 = FRR 2147 = IFO 30869 = IFO
7674 = IMI 040567 = MUCL 29245 = NRRL 2147
= QM 7588 = IBT 4998 = IBT 5045
Type strain of P. kapuscinskii, ex sandy soil, Baltic, Poland
CBS 408.69IsoT
DTO 34E3 = FRR 511 = IMI 140339 = VKM
F-1079 = IBT 19235
Soil, Syria
CBS 411.69
DTO 23A6 = IMI 140337 = VKM F-1070 = IBT
16117
Type strain of P. damascenum; soil, Ima, Damascus region, Syria
DTO 30H7
Soil, Lookout Kuranda, Australia
CBS 122392T
DTO 5H9 = IBT 29057
Soil, Treasure Island, Florida, USA
CBS 124286
DTO 30H5 = IBT 29061
Soil, Lookout Kuranda, Australia
CBS 124287
DTO 32E3
Soil, Lake Easchem, Australia
P. godlewskii
P. gorlenkoanum
P. hetheringtonii
CBS 108.66
DTO 22I3 = IBT 16132 = IBT 30406
Soil, Latosol, near Kipushi, Katanga, Congo
CBS 122403
DTO 21B2
Indoor air of house, Eindhoven
CBS 126232
DTO 87E5
Soil of rainforest, Ranoma fana, Madagascar
CBS 126233
CBS H-20654 = DTO 76B7 = IBT 22405
Soil under Cyathea tree ferns, on Rio Jaba Trail near Quebrada Culebra,
Wilson Botanical Garden/ La Cruces Biological Station, Costa Rica
CBS 253.31NT
DTO 22E9 = NRRL 2134 = IMI 191732 = FRR
2134 = IBT 18224
Soil, unknown locality
CBS 265.65
DTO 22H6 = ATCC 18334 = IMI 143926 = NRRL
3379 = IBT 18186
Type of P. pedemontanum, mycorrhizae of Fagus silvatica, Italy
CBS 327.79
DTO 23D5 = IJFM 3782 = IBT 29651
Air, Madrid, Spain
CBS 343.52
DTO 22G2 = BRL 111A = IBT 16157
Soil, Norway
CBS 378.65
DTO 22H8 = NRRL 3555 = IBT 18223 = IBT
30412 = IBT 29064
Soil, near Baya, Katanga, Congo
CBS 407.65
DTO 22H9 = IMI 096225
Hay, Haslemere, Surrey, UK
CBS 408.65
DTO 22I1 = FRR 1836 = IMI 099085 = IBT 3998
Soil, Cambridge, England, UK
CBS 409.65
DTO 22I2 = IMI 096290
Rhizosphere of Triticum aestivum, Rothamsted, UK
CBS 124323
DTO 42F2 = IBT 30584
Soil, Bialowieza National Park, Poland
CBS 126222
DTO 16A2 = IBT 29054
Soil, Los Alerces National Park, Chubut, Argentina
CBS 126223
DTO 76B2 = IBT 18227 = RMF 7771
A1 horizon soil in conifer forest (lodgepole pine), Cinnabar Park,
Wyoming, USA
CBS 126224
DTO 82C7 = IBT 26903
Soil, Spread Creek, Wyoming, USA
CBS 220.28
DTO 22E5 = ATCC 10470 = DSM 2437 = FRR
1077 = IFO 7730 = IMI 040030 = MUCL 29228 =
NRRL 1077 = IBT 5491
Soil under conifer, Tatry mountains, Poland
P. neomiczynskii
CBS 126231T
CBS H-20661 = DTO 78C2 = IBT 23560
Soil, New Zealand
P. nothofagi
CBS 127004
DTO 80D2 = IBT 17235
Soil, Brazil
CBS 130383
CBS H-20655 = DTO 76C2 = IBT 23018
Soil under Nothofagus, Chile
P. manginii
P. miczynskii
T
56
taxonoMy of Penicillium Section citrina
Table 1. (Continued).
Species
cBS no.
other numbers
DTO 82D1 = IBT 29160
Unknown source, New Zealand
CBS 118007
DTO 55A9 = KAS 2150 = IBT 29670
Porcupine dung, Dufferin, Dufferin County Forest, 1 km N. of Mansield,
Ontario, Canada
CBS 118018
DTO 55B1 = KAS 2163 = IBT 29871
Nut of Juglans cinerea (butternut); Fireman’s Park, Niagara Falls,
Ontario, Canada, 43.142051° -79.115903°
CBS 124293
DTO 84H4 = IBT 22166
Growth on Piptosphaeria (on Betula sp), Lambs Lane, New Jersey, USA
CBS 126431
DTO 118I8 = IBT 30707
Soil of oak forest; Fey el Rih, Tunesia
CBS 126432
DTO 100A1
Soil, Portugal
CBS 126433
DTO 82C2 = IBT 22969
Soil under Nothofagus, Chile
CBS 126434
DTO 120A1 = IBT 30648
Soil; Ras Rajel, Tunesia
CBS 126435
DTO 119A4 = IBT 30643
Soil of oak forest, Fey el Rih, Tunesia
CBS 276.75T
CBS H-20651 = DTO 31B4 = DAOM 147467 =
IBT 29991
Old Armillaria mellea, on hardwood log; Meach Lake, Gatineau Park,
Gatineau County, Quebec, Canada
P. pancosmium
P. pasqualense
Substrate and locality
CBS 122402
DTO 28C2 = IBT 29047
Air in bakery, Averhorn, the Netherlands
CBS 124327
DTO 57D3
Soil, Katandra Nature Reserve, NSW, Australia
CBS 126329
DTO 78B3 = IBT 17865
Soil and debris under Juniperus sp., Wind River canyon, 10 km south of
Thermopolis, Wyoming, USA
CBS 126330T
CBS H-20663 = DTO 80D5 = IBT 14235
Soil, Easter Island, Chile
CBS 101273
DTO 23F9 = IBT 30832
Leaf, Panama
CBS 117190
DTO 31A8 = IBT 16459
Soil, Galapagos Islands, Ecuador
CBS 117191
DTO 31A9 = IBT 20977 = IBT 21034 = IBT 21005
Mangrove, Venezuela
CBS 118002
KAS 2144
Coustania superba, Panama
CBS 118052
KAS 2206 = IBT 29839
Nut of Carya cordiformis (bitternut); Fireman’s Park, Niagara Falls,
Ontario, Canada, 43.142051° -79.115903°
CBS 127360
DTO 52F9 = IBT 30839
Melon imported in the Netherlands, Brazil
CBS 127361
DTO 30A6 = IBT 29070
Soil, near lake Cratez, Barrine, Queensland, Australia
CBS 162.96
DTO 23F3 = IBT 30847
Wood in tropical rainforest, Madang Province, Finisterre Range, PapuaNew Guinea
CBS 360.48T
DTO 31A6 = ATCC 10480 = FRR 2008 = IMI
040226 = NRRL 2008 = QM 725 = IBT 16202
Optical instrument, Barro Colorado Island, Panama
CBS 547.77
DTO 31A7 = ATCC 26601 = FRR 1900 = IBT
3128 = IBT 3329 = IBT 5531
Carya illinoensis, Juglandaceae, Georgia, USA
P. quebecense
CBS 101623T
CBS H-20666 = DTO 9B8 = IBT 29050
Air in sawmill, Quebec, Canada
P. raphiae
CBS 126234T
CBS H-20660 = DTO 78B8 = IBT 22407
Soil under Raphia (?) palm in primary forest, Las Alturas, elev. 1530 m,
Costa Rica
CBS 126235
CBS H-20664 = DTO 84I9 = IBT 30001
Soil under baobab tree; Montagne d’Ambre National Park, Madagascar
P. paxilli
P. roseopurpureum
CBS 127025
DTO 28F5 = IBT 30782
Indoor air of house, Eindhoven, the Netherlands
CBS 127026
DTO 28F6 = IBT 30781
Indoor air of house, Eindhoven, the Netherlands
CBS 127027
DTO 76C9 = IBT 27944
Soil under Pinus lexilis, Bear Mountain, Wyoming, USA
CBS 127028
DTO 76D3 = IBT 27930
Soil under Artemisia cana, Bear Mountain, Wyoming, USA
CBS 266.29
DTO 9E3 = ATCC 10492 = ATHUM 2895 = FRR
2064 = IMI 040573 = MUCL 28654 = MUCL
29237 = NRRL 2064 = NRRL 2064A
Unrecorded source
CBS 281.39
DTO 9E7 = FRR 2066 = MUCL 28670 = MUCL
29240 = NRRL 2066 = IBT 30783
Type of P. carminoviolaceum; plant material in ethanol, unknown location
NT
P. sanguiluum
CBS 110.64
DTO 9E6 = IBT 29045
Soil, Erzurum, Turkey
CBS 118020
DTO 128C8 = KAS 2165
Ants (Camponotus spp.), New Brunswick, Canada
CBS 118024
DTO 128C9 = KAS 2171
Ants (Camponotus spp.), New Brunswick, Canada
CBS 127029
DTO 15H6 = IBT 30793
Soil, Parque Nacional Los Alerces, Argentina
CBS 127030
DTO 6D7 = IBT 30759
Chestnut, Corsica, France
CBS 127031
CBS H-20642 = DTO 17G5 = IBT 29051
Soil, Calahonda, Costa del Sol, Spain
CBS 127032NT
CBS H-20645 = DTO 20B7 = IBT 29041
Soil, Calahonda, Costa del Sol, Spain
CBS 127033
DTO 99I9 = IBT 30786
Unknown, Catia Rodriguez
CBS 127034
DTO 119I1 = IBT 30785
Soil, Ras Rajel, Tunesia
www.studiesinmycology.org
57
Houbraken et al.
Table 1. (Continued).
Species
cBS no.
other numbers
P. sanguiluum
CBS 127035
DTO 120G9 = IBT 30784
Soil, Ras Rajel, Tunesia
CBS 127036
DTO 121D8
Soil, Ras Rajel, Tunesia
CBS 148.83
DTO 9E2 = CECT 2753
Type of P. vaccaeorum; sandy soil under pine tree, Valladolid, Spain
CBS 300.67
DTO 9E5 = IBT 30787
Sandy greenhouse soil, the Netherlands
CBS 643.73
DTO 9E4 = IBT 30789
Soil, sandy beach ridge, Manitoba, Canada
CBS 685.85
DTO 36B9 = IJFM 19078 = IBT 4904 = IBT 10578
= IBT 10579
Type of P. lacussarmientei, sandy soil, National Park of Torres del Paine,
near Lake Sarmiento, Tierra del Fuego, Chile
DTO 78C5 = IBT 28734
Unknown source, Brazil
P. shearii
P. sizovae
CBS 118059
DTO 23H7 = KAS 2214 = IBT 30164
Soil eaten by chimpanzees, Mahale Mountains National Park, Tanzania
CBS 127358
DTO 54B8 = IBT 30837
Soil, Langkawi, Malaysia
CBS 127359
DTO 99H1 = IBT 30821
Soil, Portugal
CBS 290.48T
DTO 22F6 = IMI 39739 = ATCC 10410 = NRRL
715 = IFO 6088 = IBT 24588
Soil, Tela, Honduras
CBS 342.68
DTO 23A3 = IBT 14785 = IBT 14786
Soil, Congo
CBS 343.54
DTO 22G3 = NRRL 3325 = IBT 14695
Soil, Congo
CBS 502.78
DTO 23D4 = IBT 24589
Cassava ield soil, Colombia
CBS 513.73
NHL 6444 = IBT 14698
Soil, Cape Hoskins, Waississi, New Britain Island, Papua-New Guinea
CBS 578.70
DTO 23B4 = IBT 30815
Soil, San Blas, Nayarit State, Mexico
CBS 115968
DTO 23G5
Cropped soil, Italy
CBS 117183
DTO 23H2
Papaver somniferum, the Netherlands
CBS 117184
DTO 23H3 = IBT 22812
Salty water in saltern, Slovenia
CBS 122386
DTO 5C5
Glue, the Netherlands
CBS 122387
DTO 19H1
Margarine, the Netherlands
CBS 139.65
DTO 22H5
Sea salt, Portugal
CBS 413.69NT
DTO 23A7 = FRR 518 = IMI 140344 = VKM
F-1073
Soil, Syria
DTO 49G1 = IBT 14692 = NRRL 2142
Exposed fabric, Panama
CBS 122388
DTO 49F9 = IBT 14691 = NRRL 6336
Baled coastal grass hay, Bermuda
CBS 122389
DTO 49F8 = IBT 19353 = IFO 6024
Unrecorded source
CBS 122390
DTO 48D3 = IBT 21096
Caranx crysos (blue runner, ish), sand bottoms with corals, surface
water 23°C, dept 2–3 m at Cabruta, Mochima Bay, Venezuela
CBS 122391
DTO 7D2
Potting soil, the Netherlands
CBS 122417
DTO 48D2 = IBT 20952
Ascidie (tunicate, urochordata), sand bottoms with corals, surface water
23 °C, dept 2–3 m at Cabruta, Mochima Bay, Venezuela
P. steckii
P. sumatrense
58
Substrate and locality
CBS 122418
DTO 48D1 = IBT 6452
Cynara scolymus (Artichoke), Egypt
CBS 260.55NT
DTO 22G5 = ATCC 10499 = CECT 2268 = DSM
1252 = IMI 040583 = NRRL 2140 = QM 6413
Cotton fabric treated with copper naphthenate; Panama
CBS 325.59
DTO 22G7 = ATCC 20203 = ATCC 18307 =
CECT 2273 = FRR 636 = IFO 6227 = IMI 068229
= QM 7291
Type of P. corylophiloides; soil, Japan
CBS 789.70
DTO 23B7 = IBT 3145
Unrecorded source
CBS 115708
DTO 23G4 = IBT 29691
Soil, Presicce, Apulia, Italy
CBS 117185
DTO 23H4 = IBT 24845 = IBT 29668
Bromeliad leaf tissue, Orthophyton burle-marxii, Selby Botanical Garden,
Sarasota, Florida, USA
CBS 127362
DTO 5I2 = IBT 29048
Soil, Land’s end Garden, Treasure Island, Florida, USA
CBS 127363
DTO 15E6 = IBT 30841
Packaging material, imported into the Netherlands
CBS 127364
DTO 30H8 = IBT 29059
Soil, Lookout Kuranda, Queensland, Australia
CBS 127365
DTO 99B6 = IBT 30840
Soil, Portugal
CBS 127366
DTO 120H3 = IBT 30831
Soil, Ras Rajel, Tunisia
CBS 130377
DTO 78A8 = IBT 27264
Bromeliad leaf, Aechmia magdalenae, Panama
CBS 130378
DTO 78B2 = IBT 28809
Forest fruit, Uganda
CBS 130380
DTO 80D6 = IBT 13201
Utility Pole, USA (no. JP 923, as P. steckii)
taxonoMy of Penicillium Section citrina
Table 1. (Continued).
Species
cBS no.
P. sumatrense
CBS 281.36
P. terrigenum
other numbers
Substrate and locality
DTO 22F1 = NRRL 779 = FRR 779 = ATCC
48669 = IBT 29658 = IBT 4978
Soil, Toba Heath, Sumatra, Indonesia
CBS 335.59
DTO 31B8 = ATCC 18378 = FAT 803 = FRR
639 = IFO 6232 = IMI 068232 = QM 7313 = IBT
14696
Type of P. meleagrinum var. viridilavum; soil, Japan
CBS 416.69
DTO 23A8 = FRR 508 = IMI 140336 = VKM
F-1069 = IBT 29648
Isotype of P. baradicum; soil under cornel, Damascus, Syria
CBS 117967
KAS 2104 = IBT 29807
Mushroom fairy ring, Oshawa, Ontario, Canada
CBS 117993
KAS 2133 = IBT 29908
Leaf surface, Puerto Rico
T
CBS 127354
T
CBS H-20667 = DTO 9D4 = IBT 30769
Soil, Hawaii, USA
CBS H-20644 = DTO 19H8 = IBT 30770
Tortilla, USA
P. cf. terrigenum
CBS 127357
P. tropicoides
CBS 122410T
DTO 10C4 = IBT 29043
Type; soil rainforest, near Hua-Hin, Thailand
CBS 122436
DTO 10C8
Soil rainforest, near Hua-Hin, Thailand
DTO 78C4 = IBT 27056
Leaf, Florida, USA
CBS 112584
DTO 31B1 = IBT 24580
Soil under Coffea arabica, Mertha Subbagudigy, Karnataka, India
P. tropicum
T
P. ubiquetum
P. vancouverense
CBS 130379
DTO 80D3 = IBT 16462 = DMG 1004
Soil, Galapagos Islands, Ecuador
CBS 124317
DTO 30A8 = IBT 30705
Soil near lake Cratez, Barrine, Queensland, Australia
CBS 124318
DTO 32D7 = IBT 30704
Soil, Lake Easchem, Queensland, Australia
CBS 124450
DTO 84G8 = IBT 13179 = WSF 2210
A1 horizon soil, maple-elm-ash forest, Wisconsin, USA
CBS 126436
DTO 30E2 = IBT 30397
Soil, wet forest, Atherton Tableland, Queensland, Australia
CBS 126437T
CBS H-20659 = DTO 78B5 = IBT 22226
Soil, Wilson Botanical Garden, Costa Rica
CBS 126438
DTO 87B4 = IBT 30011
Soil under tree; Montagne d’Ambre, Madagascar
CBS 126439
DTO 85B6 = IBT 30644
Soil, Ranoma fana, Madagascar
CBS 117962
DTO 55A4 = KAS 2098 = IBT 29801
Nut of Juglans cinerea (butternut); Fireman’s Park, Niagara Falls,
Ontario, Canada, 43.142051° -79.115903°
CBS 122400
DTO 38F5
Organic soil, mixed forest Rijnsweerd, Utrecht, the Netherlands
CBS 122401
DTO 21B1 = IBT 29063
Indoor air of house, Eindhoven
CBS 124328
DTO 30D3 = IBT 29736
Soil, wet forest, Atherton Tableland, QLD, Australia
CBS 124329
DTO 38D2 = IBT 30044
Organic soil, mixed forest Rijnsweerd, Utrecht, the Netherlands; dilution
plate
CBS 126321
DTO 78B6 = IBT 22265
Soil, Paciic slope of Volcan Barva at ca. 2000 m, just above Porrosati, in
Heredia Province, under Ticodendron in wet montane forest, Costa Rica,
November 2000
CBS 126322
DTO 76B4 = IBT 20820
Soil under Maple tree, Vancouver, BC, Canada
CBS 126323
CBS H-20646 = DTO 82B8 = IBT 20700
Soil under Maple tree, Vancouver, BC, Canada
CBS 126324
DTO 76B9 = IBT 22472
Type; soil under Nothofagus glauca, Costa Azul School Forest of
Universidad Catolica del Maule (35 37c / 72 c45w), Chile
CBS 126325
DTO 30D1 = IBT 29058
Soil, wet forest, Atherton Tableland, QLD, Australia
CBS 126326
DTO 76D2 = IBT 29309
Soil under Cypress, Pebble beach, Asilomar, California, USA
CBS 126327
DTO 82C4 = IBT 20692
Soil under Maple tree, Vancouver, BC, Canada
CBS 126328
DTO 85B2 = IBT 30004
Soil rainforest, Ranoma Fana, Madagascar
CBS 130376
DTO 78A4 = IBT 16486
Soil under fern on slope on the way to the beach, “path 3”, University of
Vancouver, Vancouver, BC, Canada
DTO 78C1 = IBT 23508
Soil, New Zealand
DTO 3A8 = IBT 27053 = ATCC 48699 = FRR 906
= NRRL 906
Type of P. rivolii; forest soil, Poland
T
P. waksmanii
CBS 117502
CBS 117525
DTO 3A7 = IBT 27052 = NRRL 28095
Dead polypore, New Mexico, USA
CBS 124295
DTO 84H6 = IBT 24654
Soil under conifer, Selatræd, Osterøy, Faroe Islands
CBS 124321
DTO 42F8 = IBT 29680
Soil, Poland
CBS 124322
CBS H-20652 = DTO 42G7 = IBT 29993
Soil, Poland
CBS 126425
DTO 76A7 = IBT 13531
Tilia swamp, Denmark
CBS 126426
CBS H-20658 = DTO 78A3 = IBT 15841 = DAOM
174586
Washed organic soil particle, Alberta, Canada
CBS 126427
DTO 42A6 = IBT 29674
Soil, Poland
www.studiesinmycology.org
59
Houbraken et al.
Table 1. (Continued).
Species
cBS no.
other numbers
Substrate and locality
P. waksmanii
CBS 126428
DTO 82C6 = IBT 24649
Soil under tax tree, Selatræd, Osterøy, Faroe Islands
CBS 126429
DTO 76C7 = IBT 23558x
Culture contaminant of IBT 23558
CBS 230.28
DTO 22E6 = ATCC 10516 = FRR 777 = IFO 7737
= IMI 039746 = IMI 039746i = MUCL 29120 =
NRRL 777 = QM 7681 = IBT 5003 = IBT 6994
Woodland soil, Purczcza Bialowieska Forest, Poland
T
P. wellingtonense
CBS 130375
CBS H-20657 = DTO 76C6 = IBT 23557
Soil, New Zealand
P. westlingii
CBS 118037
KAS 2189 = IBT 29822
Moose dung, Haliburton, Algonquin Park, Wildlife Research Station,
Ontario, Canada
CBS 118051
KAS 2205 = IBT 29838
Nut of Juglans nigra (black walnut); Fireman’s Park, Niagara Falls,
Ontario, Canada, 43.142051° -79.115903°
CBS 118166
KAS 2117 = IBT 29853
Acorns of Quercus, Simcoe, Cawaja Beach, Ontario, Canada
CBS 122407
DTO 28F9 = IBT 30688
Indoor air of house, Eindhoven, the Netherlands
CBS 122408
DTO 18D7 = IBT 30677
Soil under oak, Spaanderswoud, Bussum, the Netherlands
CBS 122409
DTO 17H7 = IBT 29062
Soil under oak, Spaanderswoud, Bussum, the Netherlands
CBS 124311
DTO 39D4 = IBT 30774
Soil, Poland
CBS 124312
DTO 30D6 = IBT 29067
Soil of rainforest, Atherton Tableland, Queensland, Australia
CBS 124313
CBS H-20649 = DTO 30E3 = IBT 29992
Soil, Atherton Tableland, Queensland, Australia
CBS 127003
DTO 32E1 = IBT 29659
Soil, Lake Easchem, Queensland, Australia
CBS 127005
DTO 39D8 = IBT 30758
Soil, Poland
CBS 127006
DTO 92G3
Soil heathland, Cartier heide, Eersel, the Netherlands
CBS 127007
DTO 42H1 = IBT 30756
Soil, Poland
CBS 127008
DTO 80I4 = IBT 30685
Indoor environment, Germany
CBS 127037
DTO 78B7 = IBT 22399
Soil under Cyathea fern tree, on Rio Jaba trail, near Quebrada, Culebra,
Wilson Botanical garden, Las Cruces Biological state park, Costa Rica
CBS 127039
DTO 78B4 = IBT 22164
On Ganoderma lucidum, Turkey Swamp, New Jersey, USA
CBS 127040
DTO 78G4 = DTO 78G3 = IBT 22985
Soil, St. Teresa Forest reserve, Brazil
CBS 231.28T
DTO 22E7 = IMI 092272 = IBT 15088
Soil under conifer, Denga Goolina, Poznan, Poland
CBS 688.77
DTO 23D2 = IJFM 3046 = IBT 19471
Type of P. citrinum var. pseudopaxilli; andosol soil, Navarra, Spain
In this study, we delimited Penicillium section Citrina using a
combination of ITS (internal spacer region and 5.8S rDNA gene)
and partial RPB2 gene sequences. After delimitation, the taxonomy
of this section was studied in-depth using a polyphasic approach.
Over 250 strains belonging to section Citrina, including type and
freshly isolated strains, were included. Sequences of a part of the
β-tubulin and calmodulin gene in combination with extrolite proiles,
physiological and macro- and micromorphological characters were
used for species delimitation.
dNA extraction, Pcr ampliication and sequencing
MATerIAl ANd MeThodS
data analysis
Strains
The sequence data was optimised using the software package
Seqman from DNAStar Inc. Sequences were aligned using the
software Muscle in the MEGA5 programme (Tamura et al. 2011).
The RAxML (randomised axelerated maximum likelihood) software
(Stamatakis et al. 2008) was used in order to perform the Maximum
Likelihood (ML) analysis on the combined data sets. Combined data
sets were analysed as two distinct data partitions and individual
branch length optimisation was applied per partition. Maximum
Likelihood analysis on the individual data sets was performed
with the MEGA5 software. Trees were redrawn from tree iles
using TREEVIEW (Page 1996). Section Citrina was delimitated
Data on the strains used in this study are listed in Table 1. More
detailed information can be found in the on-line database of the
CBS. These fungi are permanently preserved in the culture
collection of the CBS-KNAW Fungal Biodiversity Centre, Utrecht,
the Netherlands and placed in the working collection of the
department of Applied and Industrial Mycology (DTO), housed at
CBS.
60
Strains were grown for 7 to 14 d on MEA prior to DNA extraction.
DNA extraction was performed using the UltracleanTM Microbial
DNA isolation Kit (MoBio, Solana Beach, U.S.A.) according to
the manufacturer’s instructions. The extracted DNA was stored
at -20 °C until used. The ITS regions and parts of the β-tubulin,
calmodulin and RPB2 genes were ampliied and sequenced
according the method described previously (Houbraken et al. 2007,
2011a, 2011b, Houbraken & Samson 2011).
taxonoMy of Penicillium Section citrina
using a combination of ITS and RPB2 sequences. Coccidioides
immitis (strain RS) was used as an outgroup for this analysis. The
phylogeny of different lineages within section Citrina was studied
using a combination of partial β-tubulin and calmodulin sequences.
These phylograms were rooted with P. corylophilum CBS 330.79,
a member of section Exilicaulis (Houbraken & Samson 2011).
Also the ITS region was sequenced for the majority of strains, and
this locus was used to determine the effectiveness for species
recognition. Unique, newly generated sequences were deposited
in GenBank with accession numbers JN606358–JN606858.
Morphological analysis
Macroscopical characters were studied on the agar media Czapek
yeast extract agar (CYA), CYA supplemented with 5 % NaCl
(CYAS), yeast extract sucrose agar (YES), creatine sucrose agar
(CREA), dichloran 18 % glycerol agar (DG18), oatmeal agar (OA)
and malt extract agar (Oxoid) (MEA). The strains were inoculated
at three points on 90-mm Petri dishes and incubated for 7 d at
25 °C in darkness. In addition, CYA plates were inoculated and
incubated for 7 d at 15, 30 and 37 °C (CYA15°C, CYA30°C and
CYA37°C, respectively). All media were prepared as described
by Samson et al. (2010). The temperature-growth response of the
strains was studied on CYA. Strains were inoculated at 3 points
and incubated at 18, 21, 24, 27, 30, 33, 36 and 40 °C for 7 d in
darkness. After incubation, the colony diameter on the various agar
media was measured. Also the degree of sporulation, obverse and
reverse colony colours and the production of soluble pigments
was determined. Colony colours were not described using colour
standards as good colour charts are rarely available and frequently
used colour plates differ between the various copies of the same
book. Instead, we choose to take pictures of the colonies with a
Nikon Coolpix 990. The isolates were also examined for production
of alkaloids reacting with Ehrlich reagent using a ilter paper method
(Lund 1995). The appearance of a violet ring within 10 min was
regarded as a positive reaction, all other colours were considered
negative.
Fungal material was examined using light microscopy (Olympus
BH2 or Zeiss Axioskop 2 Plus). Microscopic mounts were prepared
in 85 % lactic acid from MEA or OA and a drop of alcohol was added
to remove air bubbles and excess conidia. Detailed examination of
the ornamentation of the ascospores was performed by scanning
electron microscopy (SEM). A quick sample preparation method
was developed (J. Dijksterhuis unpubl. data), and this method is
explained here in brief. Fungal cultures with ripe ascomata were
looded with 10 mM ACES buffer (pH 6.8, N-[2-acetamido]-2aminoethane-sulfonic acid) supplemented with 0.05 % Tween 80.
The ascomata were disconnected by vortexing with glass beads
(1 mm) and iltered through sterile glass wool. Ascospores were
spun down at 1,100×g (10 min) and washed twice in ACES buffer.
In the last washing step, sterile demineralised water was used and
the suspension was sonicated for 30 s prior to centrifugation. Filter
disks with 1 µm pore size were placed on a Whatman ilter paper
(grade no. 1). Small aliquots of the ascospore-suspension were
transferred on the ilter disk, resulting in a quick removal of the
water. The ilter disks with the ascospores were ixed on aluminium
stubs with carbon conductive double-sided tape and air-dried.
Samples were examined in a JEOL 5600LV scanning electron
microscope (JEOL, Tokyo, Japan).
www.studiesinmycology.org
extrolite analysis
Strains listed in Table 1 were grown for 7 d at 25 °C on YES and
CYA prior to extrolite extraction. Five agar plugs were taken along
a diameter of the fungal colony and pooled together into the same
vial. The extraction solvent ethyl acetate / dichloromethane /
methanol (3:2:1, v/v/v) with 1 % (v/v) formic acid was added to the
vial and subsequently ultrasonicated for 50 min. The extracts were
transferred to 1.5 ml autosampler screw-cap vials, evaporated to
dryness and re-dissolved in 400 μl methanol by ultrasonication for
10 min. Subsequently, the extracts were iltered through 0.45 μm
ilter (Minisart RC4, Sartorius, Germany) and kept at -18° C prior
to analysis. The extracts were analysed by ultra high performance
liquid chromatography (U-HPLC) using alkylphenone retention
indices and diode array UV-VIS detection as described by Frisvad
& Thrane (1987) and Nielsen et al. (2011). Identiication of extrolites
was performed by comparison of the UV-Visible spectra and
retention times of the extrolites with those present in the collection
at Department of Systems Biology, Kgs. Lyngby, Denmark. During
our investigations many compounds were found, which could not
be chemically identiied. However, these extrolites proved to be
important components for the species extrolite proile and they are
listed between quotation marks.
reSulTS
delimitation of section Citrina
In order to determine the species belonging to section Citrina, a
phylogenetic study using combined sequence data of two loci (ITS
and RPB2) was performed. 52 taxa were included in the analysis
and the total length of the alignment was 1491 characters. The ITS
partition was 575 characters long and had 174 variable sites, while
the RPB2 partition included 915 base pairs and 424 of them were
variable. Figure 1 shows the results of this analysis. Members of
section Citrina form a well-supported lineage on the phylogram (100
%). The majority of the branches in the backbone of this section
are poorly supported. Two species-rich lineages are present in
this section: one lineage is centered on P. citrinum and the other
on P. westlingii. Three other well-supported lineages are present
and these are centered on P. sanguiluum/P. roseopurpureum, P.
copticola/P. terrigenum and P. anatolicum/P. euglaucum. These
lineages appear to be less species-rich than those centered on P.
citrinum and P. westlingii. Penicillium shearii and P. paxilli occurred
on single branches and the relationship with other members of
section Citrina remains unsolved. An overview of species classiied
by other authors in the P. citrinum series (Raper & Thom 1949,
Ramírez 1982) or series Citrina (Pitt 1980) is presented in Table 2.
Several of these species do not phylogenetically belong to section
Citrina (Fig. 1), including P. corylophilum (synonyms: P. obscurum,
P. chloroleucon, P. citreovirens, P. humuli), P. soppii (synonym: P.
matris-meae), P. herquei (synonym: P. luteocoeruleum nom. inval.),
P. coralligerum, P. atrosanguineum, P. matriti and Aspergillus
inlatus (basionym: P. inlatum, R.A. Samson, unpublished data).
Species belonging to section Citrina share several characters.
The majority of species produce symmetrically biverticillate
conidiophores, lask shaped phialides (7.0–9.0 µm long) and
relatively small-sized conidia (2.0–3.0 µm diam). The conidiophores
of some species have an additional branch, which itself can also
be biverticillate branched. Six of the 39 species produced greyish
61
Houbraken et al.
CBS 232.38 P. implicatum
CBS 139.45T P. citrinum
CBS 122392T P. hetheringtonii
CBS 413.69NT P. sizovae
CBS 125.84T P. tropicum
P. citrinum‐clade
CBS 122410T P. tropicoides
100
100
76
70
84
97
100
97
100
CBS 260.55NT P. steckii
CBS 408.69NT P. gorlenkoanum
CBS 416.69T P. sumatrense
detailed analysis: Fig. 2
NRRL 779 P. sumatrense
NRRL 6181 P. sumatrense
CBS 148
148.83
83 P.
P sanguifluum
CBS 685.85 P. sanguifluum
CBS 266.29T P. roseopurpureum
CBS 290.48T P. shaerii
NRRL 35755 P. alicantinum
100
NRRL 3759 P. syriacum
CBS 167.81T P. galliacum
CBS 360.48NT P. paxilli
CBS 220.28NT P. miczynskii
95
CBS 101623T P.
P quebecense
b
CBS 126236T P. christenseniae
CBS 253.31NT P. manginii
CBS 231.28NT P. westlingii
CBS 217.28NT P. chrzaszczii
P. westlingii‐clade
CBS 230.28NT P. waksmanii
detailed analysis: Fig.
CBS 215.28NT P. godlewskii
CBS 117509T P. decaturense
CBS 126234T P. raphiae
DTO 76C6T P. wellingtonense
CBS 122402 P. pasqualense
100
Section Citrina
70
76
100
100
3
CBS 109.66T P. atrofulvum
100
CBS 127355T P. copticola
100
CBS 127354T P. terrigenum
100
CBS 479.66T P. anatolicum
CBS 323.71NT P. euglaucum
CBS 336.48 P. herquei
CBS 347
347.51
51 P.
P luteocoeruleum
CBS 330.79 P. corylophilum
CBS 231.38 P. humuli
CBS 380.75 P. atrosanguineum
CBS 226.28 P. soppii
100
CBS 225.28 P. matris-meae
100
100
Penicillium
93
100
CBS 263.29 P. sulphureus
CBS 261.33 P. raistrickii
CBS 347.61 P. matriti
100
CBS 216
216.28
28 P.
P jjenseniiii
100
CBS 137.41 P. novae-zeelandiae
CBS 123.65 P. coralligerum
CBS 368.48 P. rolfsii
CBS 682.70 P. inflatum (= Asp. inflatus)
Strain RS Coccidioides immitis
96
100
0.1
Fig. 1. Best-scoring Maximum Likelihood tree using RAxML based on a combination of partial RPB2 and ITS sequences. Members of section Citrina are in a well-supported
lineage (100 % bs) and some species previously belonging to series Citrina are placed in other lineages. Bootstrap percentages of the Maximum Likelihood (ML) analysis are
presented at the nodes. Values less than 70 % supported in the ML are not shown and branches with more than 95 % bootstrap support are thickened. The bar indicates the
number of substitutions per site. The phylogram is rooted with Coccidioides immitis (Strain RS).
brown cleistothecia and these cleistothecia contain langed
ascospores. The extrolite citrinin was produced by 16 of the 39
species and was most commonly produced by species belonging to
section Citrina. The majority of the species grows poorly on CREA
and do not have a violet reaction with Ehrlich reagent.
62
Phylogeny of section Citrina
Section Citrina was studied in detail with partial β-tubulin and
calmodulin sequences. Three separated analyses were performed:
one with species related to P. citrinum (= P. citrinum-clade) (Fig. 2),
one with species related to P. westlingii (P. westlingii-clade) (Fig.
taxonoMy of Penicillium Section citrina
Table 2. Overview of species classiied by Raper & Thom (1949), Pitt (1980) and Ramírez (1982) in the series P. citrinum or related P.
miczynskii (Christensen et al. 1999). The names in bold are excluded from section Citrina in the current study.
raper & Thom (1949)
Pitt (1980)
ramírez (1982)
christensen et al. (1999)
P. citrinum
P. citrinum
P. citrinum
P. miczynskii
P. corylophilum
P. corylophilum
P. corylophilum
P. manginii
P. steckii
P. miczynskii
P. steckii
P. atrosanguineum
P. inlatum
P. matriti
P. soppii
P. paxilli
P. syriacum nomen ambiguum
P. herquei
P. chrzaszcii nomen ambiguum
P. humuli
P. sulphureum nomen dubium
(P. rolfsii)*
(P. raistrickii)*
* P. raistrickii and P. rolfsii were included in this study for comparison purposes and were not claimed to be related to P. miczynskii.
3) and one with all the other members of section Citrina (Fig. 4).
Details on the partitions and variable sites are given in Table 3.
Individual gene trees can be found in supplementary Figs 1–6.
Fifty-three strains were included in the analysis of the members
belonging to the P. citrinum-clade and the total length of the
alignment was 938 characters. This clade includes eight accepted
species: P. citrinum, P. hetheringtonii, P. sizovae, P. tropicoides,
P. tropicum, P. steckii, P. gorlenkoanum and P. sumatrense. The
former seven species are accommodated in a well-supported
lineage (100 %), and statistical support for the relationship of the
latter species is lacking. However, this species was included in this
analysis based on the results presented in Fig. 1, which conidently
included this species in this clade (97 %).
One hundred and sixty-six isolates were included in the analysis
of the P. westlingii-clade, and the total length of the alignment was
921 characters. Twenty-one species are present in this clade, and
14 of those are newly described here. The P. westlingii-clade can be
subdivided into different subclades. Penicillium cosmopolitanum,
P. westlingii, P. nothofagi, P. pancosmium, P. decaturense, P.
ubiquetum, P. waksmanii, P. godlewskii and P. chrzaszczii are
on a well-supported lineage (99 %). Another subclade only
includes the newly described species P. vancouverense, P.
wellingtonense, P. pasqualense, P. atrofulvum (96 %); P. raphiae
and P. christenseniae are basal to this clade (82 %). Penicillium
cairnsense, P. quebecense, P. miczynskii, P. aurantiacobrunneum
and P. neomiczynskii are on another well-supported branch (98 %)
and P. manginii is on a separate well-supported branch (100 %).
The phylogenetic relationships of the species not belonging
to the P. citrinum or P. westlingii-clades are shown in Fig. 4. Sixty
strains were included and the total length of the alignment was 1208
characters long. Six different lineages are present and comprise
10 species. Penicillium paxilli formed one clade, and this clade is
related to a lineage containing the new species P. copticola and
P. terrigenum (97 %). Penicillium shearii and P. gallaicum formed
single lineages, while P. sanguiluum and P. roseopurpureum
were together on a well-supported branch (100 %). Penicillium
euglaucum, P. anatolicum and P. argentinense were also together
on a well-supported branch (100 %).
Fig. 2. Best-scoring Maximum Likelihood tree using RAxML based on a combination
of partial β-tubulin and calmodulin sequences, showing the relationship among
members of the P. citrinum-clade. Bootstrap percentages of the maximum likelihood
(ML) analysis are presented at the nodes. Values less than 70 % supported in
the ML are not shown and branches with more than 95 % bootstrap support are
thickened. The bar indicates the number of substitutions per site. The phylogram is
rooted with P. corylophilum (CBS 330.79).
www.studiesinmycology.org
DTO 78C3 P. citrinum
83
CBS 122452 P. citrinum
CBS 117.64 P. citrinum
CBS 122451 P. citrinum
CBS 122397 P. citrinum
CBS 122419 P. citrinum
CBS 252.55 P. citrinum
CBS 232.38 P. citrinum
CBS 122726 P. citrinum
CBS 122394 P. citrinum
CBS 241. 85 P. citrinum
CBS 139.45T P. citrinum
CBS 122396 P. citrinum
CBS 122395 P. citrinum
CBS 115992 P. citrinum
90
CBS 865.97 P. citrinum
100
CBS 122392T P. hetheringtonii
100
CBS124287 P. hetheringtonii
CBS 115968 P.
P sizovae
98
70
100
96
CBS 117184 P. sizovae
CBS 413.69NT P. sizovae
CBS 139.65 P. sizovae
CBS 122387 P. sizovae
CBS 122436 P. tropicoides
100
95
DTO 78B9 P. citrinum
CBS 101275 P. citrinum
DTO 30H7 P. hetheringtonii
100
CBS 122410T P. tropicoides
87
CBS 112584T P. tropicum
CBS 122389 P. steckii
71
100
100
99
CBS 260.55NT P. steckii
CBS 122388 P. steckii
CBS 122390 P. steckii
DTO 49G1 P. steckii
CBS 122391 P. steckii
NRRL 35625 P. steckii
CBS 325.59 P. steckii
CBS 789.70 P. steckii
100
CBS 408.69NT P. gorlenkoanum
CBS 411.69 P. gorlenkoanum
CBS 127363 P.
P sumatrense
DTO 80D6 P. sumatrense
CBS 335.59 P. sumatrense
89
98
CBS 117185 P. sumatrense
DTO 78B2 P. sumatrense
DTO 78A8 P. sumatrense
70
CBS 127362 P. sumatrense
CBS 127365 P. sumatrense
86
83
100
CBS 416.69 P. sumatrense
100
CBS 127366 P. sumatrense
CBS 115708 P. sumatrense
CBS 127364 P. sumatrense
CBS 281.36T P. sumatrense
0.01
CBS 330.79 P. corylophilum
63
Houbraken et al.
88
98
93
99
CBS 122406 P. cosmopolitanum
CBS 126992 P. cosmopolitanum
CBS 126990 P. cosmopolitanum
CBS 122435 P. cosmopolitanum
Clade 1
CBS 126991 P. cosmopolitanum
CBS 251.70 P. cosmopolitanum
CBS 124315 P. cosmopolitanum
CBS 637.70 P. cosmopolitanum
74
CBS 200.86 P. cosmopolitanum
CBS 124316 P. cosmopolitanum
92 CBS 126995 P. cosmopolitanum
Clade 2
CBS 126993 P. cosmopolitanum
CBS 126994 P. cosmopolitanum
CBS 126999 P. cosmopolitanum
CBS 552.86 P. cosmopolitanum
DTO 82C8 P. cosmopolitanum
CBS 126995T P. cosmopolitanum
Clade 3
CBS 127002 P. cosmopolitanum
99
CBS 127000 P. cosmopolitanum
DTO 42G4 P. cosmopolitanum
CBS 586.70
586 70 P.
P cosmopolitanum
CBS 126998 P. cosmopolitanum
Clade 4
100
CBS 126996 P. cosmopolitanum
CBS 127038 P. cosmopolitanum
CBS 126997 P. cosmopolitanum
CBS 127005 P. westlingii
CBS 122409 P. westlingii
CBS 231.28T P. westlingii
CBS 127008 P. westlingii
CBS 127007 P. westlingii
98
CBS 122407 P. westlingii
CBS 127006 P. westlingiii
CBS 688.77 P. westlingii
CBS 124311 P. westlingii
CBS 122408 P. westlingii
CBS 127037 P. westlingii
CBS 127039 P. westlingii
CBS 118051 P. westlingii
CBS 118166 P. westlingii
95
CBS 118037 P. westlingii
89 DTO 78G3 P. westlingii
CBS 127040 P. westlingii
CBS 127003 P. westlingii
95 CBS 124312 P.
P westlingii
CBS 124313 P. westlingii
98 CBS 130383T P. nothofagi
CBS 127004 P. nothofagi
CBS 126435 P. pancosmium
KAS 2126 P. pancosmium
DTO 82D1 P. pancosmium
KAS 2138 P. pancosmium
91
CBS 276.75T P. pancosmium
CBS 118018 P. pancosmium
CBS 126433 P. pancosmium
CBS 124293 P. pancosmium
100
CBS 126432 P. pancosmium
98
CBS 126434 P. pancosmium
100 CBS 126431 P. pancosmium
CBS 118007 P. pancosmium
CBS 117506 P. decaturense
CBS 119390 P. decaturense
80
CBS 117510 P. decaturense
CBS 117509T P. decaturense
80 CBS 117504 P. decaturense
CBS 117508 P. decaturense
100
CBS 117505 P. decaturense
CBS 117507 P.
P decaturense
CBS 124450 P. ubiquetum
84
CBS 126437T P. ubiquetum
CBS 117212 P. ubiquetum
CBS 124318 P. ubiquetum
89
CBS 124317 P. ubiquetum
97
CBS 126439 P. ubiquetum
CBS 126438 P. ubiquetum
98
CBS 126436 P. ubiquetum
NRRL 35636 P. ubiquetum
0.01
Fig. 3. Best-scoring Maximum Likelihood tree using RAxML based on a combination of partial β-tubulin and calmodulin sequences, showing the phylogenetic relationship among
members of the P. westlingii-clade. Newly described species belonging to this section are presented in dark blue. Bootstrap percentages of the maximum likelihood (ML) analysis
are presented at the nodes. Values less than 70 % supported in the ML are not shown and branches with more than 95 % bootstrap support are thickened. The bar indicates
the number of substitutions per site. The phylogram is rooted with P. corylophilum (CBS 330.79).
64
taxonoMy of Penicillium Section citrina
98
CBS 124321 P. waksmanii
CBS 124322 P. waksmanii
CBS 124295 P. waksmanii
97 CBS 126427 P. waksmanii
CBS 126425 P. waksmanii
CBS 126428 P. waksmanii
CBS 126426 P. waksmanii
99
CBS 117502 P. waksmanii
CBS 230.28T P. waksmanii
92 CBS 117525 P. waksmanii
DTO 78C1 P. waksmanii
CBS 126429 P. waksmanii
CBS 126419 P. godlewskii
CBS 218.28 P. godlewskii
76
99
CBS 117273 P. godlewskii
DTO 42E9 P. godlewskii
CBS 126421 P. godlewskii
CBS 126420 P. godlewskii
CBS 215.28T P. godlewskii
CBS 124319 P.
P godlewskii
90
CBS 126424 P. godlewskii
CBS 126423 P. godlewskii
73
CBS 126422 P. godlewskii
74 CBS 126430 P. chrzaszczii
CBS 176.81 P. chrzaszczii
99
CBS 217.28T P. chrzaszczii
CBS 124320 P. chrzaszczii
96
82
98
76
72
KAS 2098 P. vancouverense
CBS 126327 P. vancouverense
CBS 122400 P. vancouverense
100 CBS 124329 P. vancouverense
CBS 126326 P. vancouverense
CBS 122401 P. vancouverense
P vancouverense
78 87 CBS 126325 P.
CBS 124328 P. vancouverense
CBS 126321 P. vancouverense
84
CBS 126328 P. vancouverense
CBS 130376P. vancouverense
100
CBS 126322 P. vancouverense
96 CBS 126323T P. vancouverense
98
CBS 126324 P. vancouverense
CBS 130375T P. wellingtonense
99
96
CBS 122402 P. pasqualense
100
CBS 126330T P. pasqualense
CBS 124327 P. pasqualense
CBS 126329 P. pasqualense
CBS 261.64 P. atrofulvum
100
CBS 126331P.
126331P atrofulvum
100
CBS 126332 P. atrofulvum
CBS 109.66T P. atrofulvum
100
CBS 126234T P. raphiae
CBS 126235 P. raphiae
100
CBS 126237 P. christenseniae
CBS 126236T P. christenseniae
CBS 126226 P. cairnsense
CBS 118028 P. cairnsense
KAS 2102 P. cairnsense
79 KAS 2103 P. cairnsense
CBS 117982 P. cairnsense
CBS 117962 P. cairnsense
70
CBS 124326 P. cairnsense
DTO 87B9 P. cairnsense
CBS 124325T P. cairnsense
100
CBS 124324 P. cairnsense
100 CBS 126225 P. cairnsense
100
DTO 82B7 P. cairnsense
CBS 101623T P. quebecense
CBS 126224 P. miczynskii
CBS 124323 P. miczynskii
CBS 126223 P. miczynskii
99
CBS 220.28T P. miczynskii
CBS 126222 P. miczynskii
CBS 126277 P. aurantiacobrunneum
CBS 126229 P. aurantiacobrunneum
100
CBS 126230 P. aurantiacobrunneum
CBS 126228T P. aurantiacobrunneum
CBS 126231T P.
P neomiczynskii
CBS 122403 P. manginii
CBS 407.65 P. manginii
78 CBS 253.31NT P. manginii
CBS 408.65 P. manginii
CBS 343.52 P. manginii
70
CBS 126232 P. manginii
98
CBS 409.65 P. manginii
CBS 265.65 P. manginii
CBS 327.79 P. manginii
96
CBS 378.65 P. manginii
100
CBS 108.66 P. manginii
CBS 126233 P. manginii
CBS 330.79 P. corylophilum
0.01
Fig. 3. (Continued).
www.studiesinmycology.org
65
Houbraken et al.
CBS 360.48NT P. paxilli
CBS 127360 P. paxilli
75
CBS 162.96 P. paxilli
96
CBS 117190 P. paxilli
CBS 547.77
547 77 P.
P paxilli
100 CBS 101274 P. paxilli
88
CBS 101273 P. paxilli
100
CBS 117191 P. paxilli
CBS 127361 P. paxilli
KAS 2144 P. paxilli
97
97 CBS 130382 P. copticola
100
CBS 127356 P. copticola
CBS 127355T P. copticola
CBS 137357 P. cf. terrigenum
100
CBS 127354T P. terrigenum
99
KAS 2104 P. terrigenum
KAS 2133 P. terrigenum
CBS 290.48T P. shearii
CBS 502.78 P. shearii
80
CBS 343.54 P. shearii
CBS 118059 P. shearii
100
CBS 513.73 P. shearii
CBS 578.70 P. shearii
100 CBS 479.66T P. anatolicum
76 CBS 478.66 P. anatolicum
CBS 467.67 P. anatolicum
CBS 308.89 P. anatolicum
CBS 130371T P. argentinense
100
CBS 130373 P. argentinense
100
CBS 130381 P.
P argentinense
DTO 130372 P. euglaucum
100
CBS 323.71NT P. euglaucum
86 CBS 300.67 P. sanguifluum
CBS 118024 P. sanguifluum
98
CBS 441.88 P. sanguifluum
CBS 127029 P. sanguifluum
90
CBS 643.73 P. sanguifluum
100
99
CBS 644.73
644 73 P.
P sanguifluum
80
CBS 118020 P. sanguifluum
99
CBS 685.85 P. sanguifluum
CBS 148.83 P. sanguifluum
CBS 110.64 P. sanguifluum
100
CBS
127036 P. sanguifluum
94
CBS 127035 P. sanguifluum
CBS 127032NT P. sanguifluum
98
CBS 127033 P. sanguifluum
100
CBS 127030 P. sanguifluum
CBS
127034 P. sanguifluum
100
100 CBS 127031 P. sanguifluum
DTO 28F5 P. roseopurpureum
73 DTO 28F6 P. roseopurpureum
96
CBS 281.39 P. roseopurpureum
100
CBS 266.29T P. roseopurpureum
CBS 127028 P. roseopurpureum
99
CBS 127027 P. roseopurpureum
CBS 164.81 P. gallaicum
100
CBS 167.81T P. gallaicum
CBS 418.69 P. gallaicum
CBS 330.79 P. corylophilum
Clade 1
Clade 2
0.1
Fig. 4. Best-scoring Maximum Likelihood tree using RAxML based on a combination of partial β-tubulin and calmodulin sequences, showing the phylogenetic relationship among
selected members of section Citrina. Newly described species belonging to this section are presented in dark blue. Bootstrap percentages of the maximum likelihood (ML)
analysis are presented at the nodes. Values less than 70 % supported in the ML are not shown and branches with more than 95 % bootstrap support are thickened. The bar
indicates the number of substitutions per site. The phylogram is rooted with P. corylophilum (CBS 330.79).
66
taxonoMy of Penicillium Section citrina
Table 3. Parameters of matrices used to generate phylogenies.
Figure
No. species
calmodulin
β-tubulin
length
Variable sites
length
Variable sites
Fig. 2, P. citrinum-clade
8
474
149
464
178
Fig. 3, P. westlingii-clade
21
452
148
469
225
Fig. 4, other sect. Citrina species
10
475
212
733
349
Morphology and physiology
Macro-morphology
Various phenotypic differences were observed among the
investigated species. Growth rates on CYA, MEA, YES and DG18
are useful diagnostic features for species recognition. Some
species, e.g. P. wellingtonense, P. nothofagi grow very restricted
on CYA (5–15 mm), while others grow rapidly (P. sumatrense, P.
decaturense, P. quebecense, 30–45 mm). Reverse colours on CYA
and YES and the production of soluble pigments were also useful
characters for differentiating species belonging to section Citrina.
The colour of the mycelium was white and inconspicuous in most
species, but certain species had (light) yellow coloured mycelium
(e.g. P. vancouverense, P. miczynskii, P. cairnsense). Creatine agar,
which is used for identiication of species belonging to subgenus
Penicillium (Frisvad 1985, Frisvad & Samson 2004) was also
tested, but had little discriminatory power. Most species showed
weak growth with no or weak acid production. Exceptions are P.
christenseniae, P. steckii and P. copticola and certain strains of P.
pasqualense, P. tropicoides, P. tropicum and P. atrofulvum. Another
important feature was the production of sclerotia or cleistothecia.
Six species formed cleistothecia on OA: P. shearii, P. euglaucum, P.
anatolicum, P. argentinense, P. tropicum and P. tropicoides. These
cleistothecia were coloured in greyish-brown shades and often
took more than 6 wk to ripen. The ascospores of these species
were ellipsoidal, with two narrow, closely appressed equatorial
ridges. The ornamentation of the valves varied among the species,
from inely roughened (P. anatolicum, P. tropicum) to warted (P.
tropicoides) or reticulate (P. argentinense, P. euglaucum). Eight
species produced sclerotia and these structures remained sterile
after prolonged incubation up to 6 mo on OA, MEA and CYA. The
production of sclerotia was species speciic and most prominently
present in freshly isolated strains. With exception of P. gallaicum,
all sclerotium producing species belong to the P. westlingii-clade (P.
atrofulvum, P. aurantiacobrunneum, P. cairnsense, P. manginii, P.
miczynskii, P. pasqualense, P. quebecense). Some of the sclerotia
of the latter six species were lecked, caused by short segments of
pigmented external hyphae (Christensen et al. 1999). Penicillium
atrofulvum produces black sclerotia, and all others were in shades
of orange-brown. The Ehrlich reaction was of poor added value for
differentiating among species of section Citrina. With exception of
P. aurantiacobrunneum, all strains were negative in their Ehrlich
reaction.
Micro-morphology
The micro-morphology was similar for most species and the
majority has symmetrically branched biverticillate condiophores.
Some species have additional branches and in some species
these branches have the same branching pattern as the main
axis (“double symmetrically biverticillate”, e.g. in P. pasqualense).
Penicillium roseopurpureum, P. sanguiluum and P. galliacum are
exceptions in section Citrina and these species do not produce
www.studiesinmycology.org
symmetrically branched conidiophores. They are predominantly
monoverticillate, however, examination of older parts of the culture
showed presence of divergent lower branch-like metulae or
symmetrically biverticillate structures. The majority of the members
of section Citrina have smooth walled stipes; however, there are
exceptions, e.g. P. paxilli and certain isolates of P. manginii and P.
atrofulvum. Conidia generally measure 2.0–3.0 µm and vary from
smooth to rough-walled and from globose to ellipsoidal.
Temperature-growth curves
One of the main characters for identiication of species in section
Citrina is the optimum and maximum growth temperature on CYA.
Temperature-growth curves were made, if possible, for at least four
strains of each species. An overview of typical growth proiles is
shown in Figs 5–9 and Table 4. The result of this analysis shows
that optimum and maximum growth temperature is a species-speciic
character and an important feature for identiication of members of
section Citrina. Often phylogenetically related species also have
similar optimum and maximum growth temperatures. Members of
the P. westlingii-clade generally have maximum growth temperatures
at or below 30 °C and an optimum between 21 and 24 °C. The
exceptions in this clade are P. pasqualense, P. quebecense and P.
decaturense. These species grow well at 30 °C (5–15 mm), and some
strains can even grow at 33 °C. Members of the P. citrinum-clade, in
contrast, have higher optimum and maximum growth temperatures.
With exception of P. tropicoides, all species were able to grow at 33
°C. Furthermore, all examined P. citrinum strains consistently grew at
37 °C. Some strains of P. sizovae (ive of seven) and P. hetheringtonii
(one of four) were able to grow at this temperature, though more
restrictedly than P. citrinum. Not only members of the P. citrinumclade were able to grow at 37 °C. This feature is shared by P. shearii,
P. gallaicum and P. euglaucum and related species.
extrolites
Extrolite analysis showed that all species have a unique proile of
metabolites. An overview of extrolites produced by all section Citrina
species is given in Table 5. The extrolite proiles of each species
are included in the species descriptions (see Taxonomy). Citrinin
was most frequently detected and 41 % of the Citrina species were
able to produce this extrolite. These citrinin producing strains were
not present in a certain clade within section Citrina. In contrast,
the tentatively named extrolite “MIF” (26 %) was only produced by
species belonging to the P. westlingii-clade, and citreoviridin (23 %)
and terrein (26 %) were almost exclusively produced by this clade.
These extrolites could have been present in a common ancestor
for all the species in the P. westlingii-clade. In general, the extrolite
proiles were congruent with phenotype and phylogeny. Exceptions
are in e.g. P. manginii, P. vancouverense, P. waksmanii, where
strains could be divided in different subgroups based on extrolite
proiles. More detailed chemical investigations are needed and
these species might actually represent species complexes.
67
Penicillium sp.
colony diameter
(mm)
cleistothecia / Maximum growth
Shape, ornamentation and size
sclerotia
temperature (colony conidia
diameter, mm)*
Typical feature(s)
Similar species
Globose to subglobose, inely roughened,
2.0–2.5 µm
Yellow soluble pigments
P. argentinense, P. euglaucum, P. gallaicum
Soluble pigment absent
P. anatolicum, P. euglaucum, P. gallaicum
cYA
MeA
P. anatolicum
21–30
15–21
Cleistothecia
P. argentinense
21–27
20–25
Cleistothecia
36 °C (mc–10)
Globose, smooth, 2.0-2.5 µm
P. atrofulvum
30–40
28–38
Sclerotia
27 °C (13–21)
Ellipsoidal, smooth, 2.0–3.0 × 2.0–2.5 µm
Dark sclerotia
None
P. aurantiacobrunneum
24–30
22–28
Sclerotia
27 °C (15–20; 2/4)
(Sub)globose, smooth, 2.0–3.0 µm
Ehrlich reaction positive
P. miczynskii, P. neomiczynskii
P. cairnsense
29–39
28–38
Sclerotia
30 °C (5–10; 1/4)
(Sub)globose to broadly ellipsoidal, smooth,
2.0–3.0 × 1.8–2.5 µm
Red or blackish reverse on YES and/or
DG18
P. quebecense
33 °C (15–25; 1/4)
36 °C (0–15; 3/4)
30 °C (0–mc; 2/4)
33 °C (0–5; 3/4)
P. christenseniae
31–37
21–28
Absent
27 °C (15–22)
Globose to subglobose, inely roughened,
2.0–3.0 µm
Short stipes, moderate growth on CREA
P. cosmopolitanum, P. pancosmium, P. ubiquetum,
P. westlingii
P. chrzaszczii
25–33
21–28
Absent
27 °C (15–25)
(Sub)globose, inely roughened, 2.0–3.0 µm
No sporulation of CYA, yellow soluble
pigments on CYA, reverse on DG18 in
shades of yellow
P. cosmopolitanum, P. waksmanii, P. westlingii
P. citrinum
27–33
18–25
Absent
36 °C (8–17)
(Sub)globose, smooth, 1.8–2.5 µm
Growth at 37 °C, yellow reverse on CYA,
soluble pigment on CYA and YES
P. gorlenkoanum, P. hetheringtonii
P. copticola
31–37
25–34
Absent
33 °C (5–10)
Broadly ellipsoidal, smooth, 2.5–3.0 × 2.0–2.5
µm
Good growth on CREA
P. christenseniae, P. steckii, P. terrigenum,
P. cosmopolitanum
25–32
20–29
Absent
27 °C ((8–) 18–28)
Globose, roughened, 2.5–3.0 µm
No or weak sporulation on CYA and YES;
reverse CYA beige-brown with orange
coloured sulcations
P. chrzaszczii, P. pancosmium, P. ubiquetum, P.
westlingii
P. decaturense
32–40
27–34
Absent
30 °C (5–15; 3/5)
(Sub)globose, inely roughened, 2.0–2.5 µm
Colony diameters on CYA30°C 5–15 mm
P. cosmopolitanum, P. pancosmium, P. ubiquetum,
P. westlingii
Globose, inely roughened, 2.0–2.5 µm
Ascospores 3.0–4.0 × 2.5–3.0 µm
P. anatolicum, P. argentinense, P. gallaicum
33 °C (0–10; 2/5)
P. euglaucum
23–29
22–26
Cleistothecia
36 °C (5–15)
P. gallaicum
19–25
24–30
Sclerotia
36 °C (3–10)
(Sub)globose, smooth, 2.0–2.5 µm
Monoverticillate conidiophores
P. anatolicum, P. argentinense, P. euglaucum
P. godlewskii
15–25
12–20
Absent
27 °C (mc–10)
(Sub)globose, inely roughened, 2.0–2.5 µm
No growth at 30 °C and small colonies at
27 °C
None
P. gorlenkoanum
26–31
20–27
Absent
33 °C (6–12; 1/3)
(Sub)globose, inely roughened, 2.0–2.5
(–3.0) µm
Crème-brown reverse on CYA
P. citrinum, P. hetheringtonii
P. hetheringtonii
26–32
17–23
Absent
36 °C (7–14)
(Sub)globose, smooth to inely roughened,
2.0–2.5 µm
Growth at 36 °C
P. citrinum, P. gorlenkoanum
P. manginii
28–40
25–37
Sclerotia
27 °C (20–35; 5/8)
(Broadly) ellipsoidal, smooth, 2.5–3.0 ×
2.0–2.5 µm
Yellow mycelium on CYA15°C, fast growth
rate on YES with red soluble pigments
P. miczynskii
36 °C (0–mc; 2/3)
30 °C (0–10; 3/8)
Houbraken et al.
68
Table 4. Overview of main characters for identiication of species belonging to section Citrina.
Table 4. (Continued)..
www.studiesinmycology.org
Penicillium sp.
colony diameter
(mm)
cleistothecia / Maximum growth
Shape, ornamentation and size
sclerotia
temperature (colony conidia
diameter, mm)*
Typical feature(s)
Similar species
cYA
MeA
P. miczynskii
21–27
17–25
Sclerotia
27 °C (12–25)
Subglobose to broadly ellipsoidal, smooth,
2.0–3.0 × 2.0–2.5 µm
Soluble pigments, if produced, yellow
P. aurantiacobrunneum, P. manginii, P.
neomiczynskii
P. neomiczynskii
21–27
12–18
Absent
27 °C (8–15)
Subglobose-broadly ellipsoidal, smooth,
2.0–3.0 × 2.0–2.5 µm
Reverse on CYA yellowish brown, soluble
pigments yellow-brown
P. aurantiacobrunneum, P. miczynskii
P. nothofagi
5–10
4–8
Absent
24 °C (10-15)
Globose to subglobose, inely roughened,
2.5–3.5 µm
Restricted growth on CYA, MEA and YES
P. wellingtonense
P. pancosmium
(23–)
28–35
(20–)
25–31
Absent
27 °C (15–25; 3/5)
Globose to subglobose, inely roughened,
2.0–3.0 µm
Reverse on YES yellow-orange or orange,
dull-green or grey-green conidia on CYA
P. ubiquetum
P. pasqualense
25–35
(15–)25–30
Sclerotia
30 °C (6–15; 2/4)
(Sub)globose, spinose, 2.5–3.5 µm
Dark brown reverse on CYA, conidia (dark)
blue green, spinose
None
P. paxilli
30–37
28–35
Absent
33 °C (mc–15)
Subglobose-broadly ellipsoidal, smooth or
nearly so, 2.0–3.0 µm
Rough walled stipes, predominantly
biverticillate with appressed terminal whorl of
4-8 metulae
P. raphiae
30 °C (0–mc; 2/5)
33 °C (0–mc, 2/4)
38–42
30–35
Sclerotia
33 °C (3–10)
Subglobose, smooth, 2.0–3.0 µm
Dark red reverse on YES
P. cairnsense
32–36
21–25
Absent
27 °C (15–22)
Broadly ellipsoidal,smooth or inely
roughened, 2.0–2.5 × 1.8–2.5 µm
Symmetrically biverticillate conidiophores,
broadly ellipsoidal conidia
P. paxilli
P. roseopurpureum
7–16
9–19
Absent
30 °C (mc–15)
(Sub)globose, smooth to inely roughened,
1.8–2.5 µm
Monoverticillate conidiophores, reverse
on CYA in shades of red with red-brown
diffusible pigments
P. sanguiluum
P. sanguiluum
(15–)
18–26
17–26
Absent
33 °C (mc–10)
Globose to subglobose, smooth to inely
roughened, 2.0–2.5 µm
Monoverticillate conidiophores, reverse
on CYA in shades of red with red-brown
diffusible pigments
P. roseopurpureum
P. shearii
28–40
26–37
Cleistothecia
36 °C (8–20)
Subglobose-broadly ellipsoidal, smooth,
2.5–3.0 × 1.8–2.5 µm
Abundant production of dark grey coloured
cleistothecia, growth at 37 °C
P. tropicum, P. tropicoides
P. sizovae
28–39
27–35
Absent
36 °C (4–8)
(Sub)globose, inely roughened, 2.0–2.5 µm
Fast growth rate on MEA and YES, pale
reverse on CYA, growth at 36 °C
P. steckii
P. steckii
24–32
21–30
Absent
33 °C (mc–12 (–24); 5/6)
Broadly ellipsoidal towards fusiform, smooth,
2.3–3.0 × 2.0–2.5 µm.
Weak to moderate growth on CREA
P. christenseniae, P. copticola, P. sizovae, P.
sumatrense, P. terrigenum
Subglobose-broadly ellipsoidal, inely
roughened, 2.0–2.5 µm
Good growth on YES with yellow reverse
P. steckii
36°C (0–12; 1/6)
P. sumatrense
33–42
27–36
Absent
30 °C (10–30; 2/9)
P. terrigenum
28–36
25–32
Absent
33 °C (10–15)
Broadly ellipsoidal, smooth, 2.0–3.0 × 2.0–2.5 µm
Poor growth on CREA
P. copticola, P. steckii
P. tropicoides
24–30
18–23
Cleistothecia
30 °C (10–16)
Broadly ellipsoidal, smooth, 2.0–3.0 × 1.8–2.5
µm
Abundant production of drab-grey
cleitothecia, no growth at 33 °C
P. shearii, P. tropicum
P. tropicum
24–31
23–27
Cleistothecia
33 °C (8–18)
Broadly ellipsoidal, smooth, 2.0–3.0 × 2.0–2.5
µm
Abundant production of brownish-grey
cleitothecia, growth at 33 °C
P. shearii, P. tropicoides
33°C ((0–) 5–20; 7/9)
69
taxonoMy of Penicillium Section citrina
P. quebecense
P. raphiae
70
30 °C (0–mc; 3/14)
mc = micro colonies, 1–2 mm in diam.
Absent
25–34
(25–)
30–36
P. westlingii
*The maximum growth temperature is determined at intervals of 3 °C (see material & methods). The highest temperature with visible growth is listed and the colony diameter is mentioned between brackets. If the maximum growth varied within a
species, then both temperatures are listed together with the number of isolates showing growth at that temperature.
dIScuSSIoN
P. chrzaszczii, P. cosmopolitanum, P. pancosmium,
P. ubiquetum
No or weak sporulation on CYA and YES;
reverse CYA pale, pale-beige or pinkishbeige
Globose, roughened, 1.8–2.5 µm
27 °C ((8–) 15–27; 11/14)
P. nothofagi
Slow growth on MEA and CYA, reverse on
CYA in shade of orange
Subglobose to broadly ellipsoidal, smooth to
inely roughened 2.5–3.5 µm
8–13
P. wellingtonense
10–15
Absent
24 °C (15–20)
P. chrzaszczii, P. godlewskii
Beige-brown reverse on CYA
18–24
(–30)
P. waksmanii
(20–)
25–32
Absent
27 °C (10–25)
(Sub)globose, inely roughened, 2.0–3.0 µm
P. manginii P. miczynskii
Light yellow mycelium (most pronouncedly
on YES), colonies restricted
Subglobose, inely roughened, 2.0–3.0 µm
16–23
P. vancouverense
20–30
Absent
27 °C (mc–15)
Reverse on YES orange to pinkish-red,
conidia dull green or dark green on CYA
(Sub)globose, inely roughened, 1.8–2.5 µm
27 °C (15–25)
18–26
24–34
Absent
MeA
cYA
P. ubiquetum
colony diameter
(mm)
Penicillium sp.
Table 4. (Continued)..
cleistothecia / Maximum growth
Shape, ornamentation and size
sclerotia
temperature (colony conidia
diameter, mm)*
Typical feature(s)
P. pancosmium
Similar species
Houbraken et al.
The species in section Citrina are very common in soil, but are also
found in foods, indoor air and many other substrates. The description of
17 new species may help determining more accurately the mycobiota
of soils, which may be important for biodiversity, ecological and climate
change studies. Even though the species treated here are both
phylogenetically and ecologically related, section Citrina was treated
very differently in previous taxonomic studies (Raper & Thom 1949,
Pitt 1980, Ramírez 1982). The inclusion of physiological, chemical
and nucleotide sequence based data has changed the perception
of series and sections in ilamentous fungi and these taxonomic
groupings are now both phylogenetically and ecologically consistent.
Disregarding the many different species concepts proposed, a
polyphasic approach to taxonomy has proven to give clear results that
are predictive (e.g. Frisvad & Samson 2004). The species in section
Citrina grow optimally at 23–26 °C, can grow at low water activities,
in substrates containing NaCl, and often produce citrinin, citreoviridin,
anthraquinones, indol-alkaloids, paxillin, and/or isochromantoxins.
On the other hand, no species in section Citrina produce asperentins,
atpenins, austins, brevianamides, chaetoglobosins, chrysogines,
communesins, compactins, curvulic acids, cycloaspeptides,
expansolides, fumitremorgins, fumagillins, gliotoxins, griseofulvins,
kojic acids, mycophenolic acids, ochratoxins, paraherquamides,
patulins, penicillic acids, penicillins, penigequinolones, penitrems,
psychrophilins, pyripyropens, terrestric acids, tryptoquialanins,
tryptoquivalins, viridicatumtoxins, verruculones, viridicatins,
xanthocillins, xanthoepocins, xanthomegnins, and several other
extrolites, often found in Penicillium subgenus Penicillium or section
Lanata-divaricata (as series Simplicissima) (Frisvad & Filtenborg
1990, Frisvad & Samson 2004). Despite this, a large number of
extrolites could not be identiied (Table 5) and may prove to be new
interesting drug leads.
TAxoNoMY
Species delimitation
In this study, we applied a polyphasic approach for species
recognition. Phenotypic and physiological characters combined
with extrolite proiles and DNA sequences were used for species
delimitation. New species were introduced when the results of these
approaches were congruent. In some cases, these approaches
were incongruent. In general, the phylogenetic analysis based
on partial β-tubulin and calmodulin sequences generated more
taxonomic units (clades) than the analyses based on phenotypic
and physiological characters. If no distinct differences in phenotype
and/or extrolite patterns were detected between those closely
related clades, then we decided to keep them as one species, until
more evidence becomes available to warrant describing them as
species. More details on these decisions are given in the “taxonomy
and phylogeny” part in the species descriptions.
Identiication
As mentioned above, current species delimitation is based on
a combination of characters. An overview of useful phenotypic
and physiological characters for identiication is given in Table
4. Although there are differences in phenotype and physiology
among these species, identiication based on these features
taxonoMy of Penicillium Section citrina
Fig. 5. Overview of growth rates on CYA (reverse) after 7 d at various temperatures. Row, left to right: 21, 24, 27, 30, 33, 36 °C; columns, top to bottom: P. nothofagi, P.
wellingtonense, P. godlewskii, P. vancouverense, P. neomiczynskii, P. atrofulvum, P. christenseniae, P. miczynskii, P. waksmanii.
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71
Houbraken et al.
Fig. 6. Overview of growth rates on CYA (reverse) after 7 d at various temperatures. Row, left to right: 21, 24, 27, 30, 33, 36 °C; columns, top to bottom: P. raphiae, P. chrzaszczii,
P. ubiquetum, P. aurantiacobrunneum, P. pancosmium, P. cosmopolitanum, P. westlingii, P. manginii, P. manginii.
72
taxonoMy of Penicillium Section citrina
Fig. 7. Overview of growth rates on CYA (reverse) after 7 d at various temperatures. Row, left to right: 21, 24, 27, 30, 33, 36 °C; columns, top to bottom: P. roseopurpureum, P.
tropicoides, P. cairnsense, P. pasqualense, P. decaturense, P. sanguiluum, P. quebecense, P. terrigenum, P. copticola.
www.studiesinmycology.org
73
Houbraken et al.
Fig. 8. Overview of growth rates on CYA (reverse) after 7 d at various temperatures. Row, left to right: 21, 24, 27, 30, 33, 36 °C; columns, top to bottom: P. paxilli, P. tropicum,
P. sumatrense, P. gorlenkoanum, P. steckii, P. sizovae, P. argentinense, P. euglaucum, P. anatolicum.
74
taxonoMy of Penicillium Section citrina
Fig. 9. Overview of growth rates on CYA (reverse) after 7 d at various temperatures. Row, left to right: 21, 24, 27, 30, 33, 36 °C; columns, top to bottom: P. gallaicum, P.
hetheringtonii, P. citrinum, P. shearii.
remains dificult for non-specialists. Molecular based identiication
(sequencing) is nowadays common practice. Currently, ITS is the
accepted barcode (C. Schoch et al., unpubl. data); however, this
locus is inadequate for species recognition in section Citrina. 55
% of the species could be unambiguously identiied using ITS
sequences. Especially in the P. westlingii-clade, many species
share the same ITS sequence. Partial calmodulin and β-tubulin
sequences had suficient discriminatory power to differentiate all
species of section Citrina. It is therefore recommended to sequence
either gene for correct species identiication.
Sporulation on CYA moderate, conidia grey green, cleistothecia
abundantly produced in freshly isolated strains and covered under
a felt of conidiophores, mycelium inconspicuous, clear exudate
produced in small droplets, soluble pigment strong yellow, margin
entire, reverse yellow-brown. Sporulation on YES moderate,
conidia blue-green, mycelium pale-yellow, soluble pigments yellow,
reverse (vivid) yellow. Sporulation on DG18 weak to moderate,
conidia blue-green, mycelium white, reverse vivid yellow. Moderate
sporulation on MEA, conidia dull-green with a blue element, colony
texture slightly loccose, mycelium white. Ehrlich reaction negative.
list of accepted species and their synonyms
Cleistothecia produced on most agar media, yellow-brown when
young, becoming brown at age; globose or subglobose, up to 200
µm diam, occasionally larger, consisting of sclerotioid masses
of polygonal cells, ripening after 4–5 wk or more. Ascospores
ellipsoidal, with 2 distinct, appressed equatorial ridges, smooth
to slightly roughened valves under light microscope, but showing
warts and small ridges when viewed with SEM, 2.5–3.5 × 2.0–3.0
µm. Conidiophores predominantly biverticillate, stipes variable in
length 20–200 µm, smooth walled, 2.0–3.0 µm wide. Metulae in
verticils of 2–3 (–4), unequal in length, divaricate, slightly inlated
at the apex, 10–20 × 2.0–4.0 µm. Phialides ampulliform, 6.0–8.0
× 2–3 µm. Conidia globose, inely roughened, 2.3–2.8 µm diam.
Our polyphasic taxonomic approach revealed that Penicillium
section Citrina includes 39 species including 17 new species. An
overview of species belonging to section Citrina is presented in
Table 4. Species belonging section Citrina and their synonyms
are listed in Table 6 and the current classiication is compared with
those of Pitt (1980), Ramírez (1982) and Pitt et al. (2000).
Species descriptions
Penicillium anatolicum Stolk, Ant. van Leeuwenhoek 34:
46. 1968. Fig. 10.
= Eupenicillium anatolicum Stolk, Ant. van Leeuwenhoek 34: 46. 1968.
Extrolites: Anthraquinones, bisanthrons, curvularin, dehydrocurvularin, sorbicillins, “POTO”, “3-T”.
Typus: ex soil, Turkey (CBS 479.66, holotype; cultures ex-type
CBS H-20647 = DTO 16B7 = IBT 16177 = IBT 30764).
Diagnostic characters: Yellow soluble pigments (sorbicillins),
metulae of unequal length, with inlated apex.
Description: Colony diam, 7 d, in mm: CYA 18–30; CYA15°C 4–8;
CYA30°C 23–32; CYA37°C 0–5; MEA 15–21; YES 23–30; DG18
20–28; ratio CYAS:CYA 0.85–1.0; creatine agar 11–18, weak
growth, weak or no acid, and no base production.
Similar species: Penicillium anatolicum is phylogenetically
related to P. euglaucum and P. argentinense. The ascospores
of P. euglaucum are larger than those of P. anatolicum and P.
argentinense. In addition, P. argentinense does not produce
www.studiesinmycology.org
75
Houbraken et al.
Table 5. Extrolites produced by species assigned to Penicillium section Citrina.
Species
extrolites produced
P. anatolicum
Anthraquinones, bisanthrons, curvularin, dehydrocurvularin, sorbicillins, “POTO”, “3-T”
P. argentinense
Curvularin, dehydrocurvularin, “AURANMUF”, “OXIM”
P. atrofulvum
“ALK”, “GULLA”, “SOLIS”, “3T”
P. aurantiacobrunneum
Benzomalvins, citreoviridin, terrein, “OTOT”
P. cairnsense
CBS 126226, CBS 117982, CBS 118028 and CBS 117962: benzomalvins, citreoviridin, phoenicin, decaturin; CBS 124325, CBS 126225 and
DTO 87B9: citreoviridin, terrein and/or quinolactacin; other extrolites: “KUM”, “MIF”, “MIM”, “RAI”, “SENGA”
P. christenseniae
Citrinin, quinolactacin, “FON”, “KUM”, “MIF”, “RYLA”
P. chrzaszczii
Citrinin, terrein, “MIF”, “MIM”, “RAI”, “3T”, “VERN”
P. citrinum
Citrinin, quinolactacins, citrinadins, perinadine, several anthraquinones, “CITY”, “met k”, “shamix”
P. copticola
“GULLA”, “HAEN”, “PRS”, “VERSI”
P. cosmopolitanum
Citrinin, okaramin, perinadine, territrems, “CURVO”, “HAEN”, “PHOE”, “ROTO”, “SENGA”, “TRIP”, “VERSI”, “XANTHOC”
P. decaturense
Daldinin D, decaturin A, deoxyoxalicine B, terrein, “SENGA”, “SNIL”, “SVOL”, “VERSI”, “XANTHOC”
P. euglaucum
Terrein, “ALK”, “FRIL”, “GLAD”, “RAI”, “SPOKO”, “3-T”
P. gallaicum
Citreoviridin, “KOKSO”, “3-S”, “TIDL”, “VYL”
P. godlewskii
Citrinin, citreoviridin, decaturin, okaramin, perinadine, “TRIP”
P. gorlenkoanum
Citrinin, costaclavin, chanoclavine-I, “KUSK”, “PHOE”, “WK”, “WS”, “WT” and “WØ”
P. hetheringtonii
Citrinadine, citrinin, quinolactacin, anthraquinones, “SHAMIX”, “FON”, “CITY”, “PR1-x”
P. manginii
Citrinin, citreomontanin, citreoviridin A, citreoviridinol A1 and A2, epicitreoviridinol, phoenicin, “MIF”, ”MIM”
P. miczynskii
Citreoviridin, cyclopiazonic acid, quinolactacin, terrein, “met OE”, “MIF”, “TERRIT”, “XANTHOC”
P. neomiczynskii
Citreoviridin, terrein, “MIF”, “OFSO”
P. nothofagi
Citrinin, “CURVU”, “SENTRIP”, “SKAEM”
P. pancosmium
Citrinin, daldinin D, decaturin, terrein, “MELI”, “ORAN”, “SENGA”, “XANTHOC”
P. pasqualense
Pyrenocines, indol alkaloids, “PAS”
P. paxilli
Paxillin, dehydroxypaxillin, 1’-O-acetylpaxillin, meleagrin, “PU”, “PUX”, “TOTO”
P. quebecense
Citreoviridin, phoenicin, terrein, “SENOE” (verrucofortine-type molecule), “MIF”, “MIM”, “SENGA”, “alk-770”
P. raphiae
CBS 126234T: citrinin, “FON”, “MIF”,”KUM”, “LOST”,“PHOE”, and “TRIP”; CBS 126235: citrinin, quinolactacin,”FON”, “MIF”, “KUM”, “MIM”,
“REJS”, “SENGA”, and “XANTHOC”
P. roseopurpureum
Bisanthrons, roseopurpurin, sorbicillins, “AQ”, “SEL”
P. sanguiluum
Bisanthrons, roseopurpurin, β-hydroxycurvularin, dehydrocurvularin, curvularin, “FOSI”, “FYKS”, “SNIT”, “TIDL”, “VERN”
P. shearii
Paxillin, paspalinine, shearinin A & B, “XX” and several indole alkaloids
P. sizovae
Quinolactacin, tanzawaic acid E, verrucolone, “AFSI”, “CHAE and “PNUF”
P. steckii
Isochromantoxins, quinolactacin, tanzawaic acid E, “ALTI”, “EXPO”, “FON”, “FOS”, “GLOO”, “GYF”, “PHOE”, “RAI”, “STOK”, “SVUL”, “VERN”
P. sumatrense
Curvularin, dehydrocurvularin, “POTO”, “SAAT”, “TERRIT”, “TIDL”, “VOX”
P. terrigenum
“HAEN”, “ISOC”, “PRS”, “VERSI”
P. tropicoides
Isochromantoxins, several apolar indol-alkaloids, “CITY”, “HOLOX”, “PR1-x”, “RAIMO”
P. tropicum
Several apolar indol-alkaloids, “CITY”,”EMON”, ”HOLOX” and “RAIMO
P. ubiquetum
Citrinin, terrein, “ALK”, “GLYF”, “RAI”, “TRIP”, “XANTHOC”; CBS 126438, CBS 126436: anthraquinone bisanthorns, citrinin, okaramins, and
“SENGA”
P. vancouverense
Citrinin, citreoviridin, “MIF”, “PAS”, “met OE”
P. waksmanii
Citrinin, cyclopiamin, meleagrin (only produced by one isolate), “GLYF”, “PAS”, “SENGA”.
P. wellingtonense
Citrinin, decaturin, “MIF”, “met Q”, “POF”, “RAI”, “TRIP”, “XANTHOC”
P. westlingii
Citrinin, curvularin, dehydrocurvularin,”PHOE”, “TRIP”, “XANTHOC”
yellow soluble pigments. Penicillium gallaicum also yellow soluble
pigments (citreoviridins), but forms predominantly monoverticillate
conidiophores and produces sclerotia instead of ascomata.
Distribution and ecology: Soil seems to be the primary habitat;
isolated in Turkey, Florida, USA and South-Africa.
Barcode & molecular based ID: GenBank no. GU944598. This
species can be identiied with ITS, β-tubulin and calmodulin
sequences.
76
Taxonomy and phylogeny: Stolk & Samson (1983) reduced E.
anatolicum to synonymy with E. euglaucum, and P. citreonigrum
was considered to be the anamorph. Peterson (2000) found that E.
anatolicum is phylogenetically distinct from E. euglaucum and not
closely related to P. citreonigrum. In contrast, our data show that P.
anatolicum and P. euglaucum are closely related and both species
are phylogenetically distinct from P. citreonigrum (Houbraken &
Samson 2011). CBS 308.89 warrants further attention. This strain
is phylogenetically related to P. anatolicum (Fig. 4), though without
statistical support. This strain resembles P. anatolicum in many
aspects, but differs in having a more restricted growth rate on DG18.
taxonoMy of Penicillium Section citrina
Fig. 10. Penicillium anatolicum. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–C. Ascomata. D–E. Ascospores. F–H. Conidiophores. I. Conidia. Scale bars = 10 µm.
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Houbraken et al.
Table 6. Taxonomic disposition of members of section Citrina in different studies of Penicillium.
original species name
Pitt (1980)
ramírez (1982)
Pitt et al. (2000)
current study
Citromyces cesiae
P. roseopurpureum
P. cyaneum, p.655
P. roseopurpureum
P. roseopurpureum
Citromyces sanguiluus
P. roseopurpureum
P. roseopurpureum
P. roseopurpureum
P. sanguiluum
Citromyces subtilis
P. citrinum
P. sartoryi
P. citrinum
P. citrinum
E. anatolicum
E. anatolicum
Not treated
E. anatolicum
P. anatolicum
E. euglaucum
Not treated
Not treated
Not treated
P. euglaucum
E. shearii
E. shearii
Not treated
E. shearii
P. shearii
E. tropicum
Not treated
Not treated
Not treated
P. tropicum
P. alicantinum
Not treated
P. alicantinum
P. citreonigrum
P. gallaicum
P. auriluum
P. citrinum
P. citrinum
P. citrinum
P. citrinum
P. baradicum
P. citrinum
P. baradicum
P. citrinum
P. sumatrense
P. botryosum
P. citrinum
P. botryosum
P. citrinum
P. citrinum
P. carminoviolaceum
P. roseopurpureum
P. roseopurpureum
P. roseopurpureum
P. roseopurpureum
P. chrzaszczii
P. miczynskii
P. jensenii
P. miczynskii
P. chrzaszczii
P. citrinum
P. citrinum
P. citrinum
P. citrinum
P. citrinum
P. corylophiloides nom. inval.
P. jensenii
P. corylophilum
P. jensenii
P. steckii
P. damascenum
P. melinii
P. damascenum
P. melinii
P. gorlenkoanum
P. decaturense
Not treated
Not treated
Not treated
P. decaturense
P. gallaicum
Not treated
P. gallaicum
P. citreonigrum
P. gallaicum
P. godlewskii
P. jensenii
P. godlewskii
P. jensenii
P. godlewskii
P. gorlenkoanum
P. citrinum
P. gorlenkoanum
P. citrinum
P. gorlenkoanum
P. hetheringtonii
Not treated
Not treated
Not treated
P. hetheringtonii
P. implicatum
P. implicatum
P. implicatum
P. implicatum
P. citrinum
P. kapuscinskii
P. canescens
P. kapuscinskii
P. canescens
P. godlewskii
P. lacussarmientei
Not treated
Not treated
P. roseopurpureum
P. sanguiluum
P. manginii
P. miczynskii
P. miczynskii
P. manginii
P. manginii
P. meleagrinum var. viridilavum
P. janthinellum
P. janthinellum
P. janthinellum
P. sumatrense
P. miczynskii
P. miczynskii
P. miczynskii
P. miczynskii
P. miczynskii
P. paxilli
P. paxilli
P. paxilli
P. paxilli
P. paxilli
P. pedemontanum
P. miczynskii
P. pedemontanum
P. pedemontanum
P. manginii
P. phaeojanthinellum
P. fellutanum
P. fellutanum
P. fellutanum
P. citrinum
P. rivolii
P. jensenii
P. janthinellum
P. jensenii
P. waksmanii
P. roseopurpureum
P. roseopurpureum
P. roseopurpureum
P. roseopurpureum
P. roseopurpureum
P. sartoryi
P. citrinum
P. sartoryi
P. citrinum
P. citrinum
P. sizovae
P. fellutanum
P. sizovae
P. sizovae
P. sizovae
P. steckii
P. citrinum
P. steckii
P. steckii
P. steckii
P. sumatrense
P. corylophilum
P. corylophilum
P. corylophilum
P. sumatrense
P. tropicoides
Not treated
Not treated
Not treated
P. tropicoides
P. turolense
Not treated
P. turolense
P. westlingii
P. chrzaszczii
P. vaccaeorum
Not treated
Not treated
P. roseopurpureum
P. sanguiluum
P. waksmanii
P. waksmanii
P. waksmanii
P. waksmanii
P. waksmanii
P. westlingii
P. waksmanii
P. waksmanii
P. westlingii
P. westlingii
Penicillium argentinense Houbraken, Frisvad & Samson,
sp. nov. MycoBank MB563185. Fig. 11.
Etymology: Named after Argentina, the location of the type culture.
Differt ab omnibus speciebus afinibus coloniis ad 37 °C haud crescentibus,
reverso pallido vel psammocolorato coloniae in agaro CYA et YES, sine pigmentis
solubilibus.
78
Typus: ex soil, Valdes Peninsula, Chubet, Argentinia, M.B. Pildain.
(CBS H-20641 – holotypus, cultures ex-type CBS 130371 = DTO
16B7 = IBT 30761).
Description: Colony diam, 7 d, in mm: CYA 21–27; CYA15°C 3–7;
CYA30°C 22–30; no growth on CYA37°C; MEA 20–25; YES 22–29;
DG18 14–20; ratio CYAS:CYA 1.0–1.1; creatine agar 8–14, weak
growth, weak acid and no base production.
taxonoMy of Penicillium Section citrina
Fig. 11. Penicillium argentinense. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B. Ascomata. C–D. Ascospores. E–G. Conidiophores. H. Conidia. Scale bars = 10 µm.
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Houbraken et al.
Sporulation on CYA absent after 7 d and sporulation sparsely
after prolonged incubation, cleistothecia sparsely produced and
inconspicuous when young and becoming brownish grey in age,
mycelium white, exudate clear, produced in small droplets, soluble
pigments absent, margin entire, reverse pale or beige. Sporulation
on YES absent, mycelium white, soluble pigments absent, reverse
in shades of pale-beige, becoming brown in the centre after
prolonged incubation. Sporulation on DG18 absent, mycelium
white, reverse pale to pale-cream. Sporulation on MEA absent,
remaining sterile after prolong incubation, mycelium white. Ehrlich
reaction negative.
Cleistothecia only produced on CYA and oatmeal agar, globose
or subglobose, up to 100–200 µm diam, consisting of sclerotioid
masses of polygonal cells, slowly ripening in more than 6 wk.
Ascospores ellipsoidal, with 2 inconspicuous equatorial ridges,
roughened valves under light microscope, reticulate when viewed
with SEM, 2.5–3.0 × 2.0–2.5 µm. Conidiophores monoverticillate or
biverticillate, stipes variable in length 30–200 µm, smooth walled,
thin, measuring 1.5–2.5 µm, ending with a slightly inlated apex,
2.0–4.0 µm. Metulae, when present, as additional branch, 10–20
× 1.5–3.0 µm wide. Phialides ampulliform, occasionally positioned
subapically, 7.0–9.0 × 2–3 µm. Conidia globose, smooth, 2.0–2.5
µm diam.
Extrolites: Curvularin, dehydrocurvularin, “AURANMUF”, “OXIM”.
Diagnostic characters: No growth at 37 °C, pale or beige reverse
on CYA and YES, soluble pigments absent.
Similar species: See P. anatolicum.
Distribution and ecology: This species has a worldwide distribution.
It has been isolated from soil in Argentina and the Netherlands and
Phaenocoma leaf bracts from South Africa.
Barcode & molecular based ID: JN831359. This species can be
identiied with ITS, β-tubulin and calmodulin sequences.
Taxonomy and phylogeny: None.
Penicillium atrofulvum Houbraken, Frisvad & Samson, sp.
nov. MycoBank MB563183. Fig. 12.
Etymology: Named after the black coloured sclerotia produced by
this species.
Differt ab omnibus speciebus afinibus formatione sclerotiorum atratorum, reverso
atrocolorato coloniae in agaro diverso et conidiophoris symmetricis biverticillatis.
Typus: ex soil, Katanga near Kipushi, Zaire; No. 153, C. Lanneau
(CBS H-20650 – holotypus, cultures ex-type CBS 109.66 = DTO
31B2 = FRR 799 = IBT 30032).
Description: Colony diam, 7 d, in mm: CYA 30–40; CYA15°C 15–
25; CYA30°C and CYA37°C: no growth; MEA 28–38; YES 40–47;
DG18 28–35; ratio CYAS:CYA 1.0–1.2; creatine agar 13–22, weak
to moderate growth and no acid production.
Moderate to good sporulation on CYA, velvety, conidia darkgreen or dull green, mycelium inconspicuous, exudate absent or
sparsely produced as small clear droplets, soluble pigment absent,
80
margin entire, reverse dark brown to dark green and almost black
underneath the sclerotia. Good sporulation on YES, conidia dull
green, mycelium inconspicuous, soluble pigments absent, reverse
black with beige margins. Good sporulation on on DG18, conidia
grey green, reverse pale with a black centre. Colonies on MEA grey
or dull-grey green, colony texture loccose, mycelium white. Ehrlich
reaction negative.
Sclerotia black, partly embedded in the agar, irregular in shape,
up to 50–800 µm diam, often produced under a thick felt of
conidiophores, rather soft, conluent and forming coriaceous
masses, sometimes concentrated along radial lines, consisting of
dark pigmented, polygonal, thick walled cells. Asci and ascospores
are not observed. Conidiophores predominantly symmetrically
biverticillate, stipes 300–500 µm long, smooth or inely rough
walled, 2.5–3.5 µm wide; metulae in a compact terminal whorls of
3–5, equal in length, 10–14 × 2.5–3.5 µm; phialides ampulliform,
7–9 × 2.0–3.0 µm. Conidia ellipsoidal, smooth walled, variable in
size, but not in shape, 2.0–3.0 × 2.0–2.5 µm.
Extrolites: “ALK”, “GULLA”, “SOLIS”, “3T”.
Diagnostic characters: The formation of dark sclerotia, black
coloured reverse on various agar media, symmetrical biverticillate
conidiophores.
Similar species: None; this species is unique because of the
formation of dark coloured sclerotia.
Distribution and ecology: This species has a worldwide occurrence
and is isolated from soil in the Netherlands, Zaire and Tunisia.
Barcode & molecular based ID: GenBank no. JN617663. This
species has unique ITS, β-tubulin and calmodulin sequences.
Taxonomy and phylogeny: Penicillium atrofulvum phenotypically
resembles P. novae-zeelandiae by the production of black coloured
sclerotia and symmetrical biverticillate conidiophores. The lectotype
of P. novae-zeelandiae (CBS 137.41T = NRRL 2128T) is related to P.
canescens, P. jensenii and P. coralligerum in section Canescentia
(Peterson & Horn 2009, Houbraken & Samson 2011). According
to the original description of van Beyma (1940), this ex-type strain
of P. novae-zeelandiae (CBS 137.41) produces black coloured
sclerotia. However, this strain no longer shows this diagnostic
feature. Phenotypically, P. novae-zeelandiae can be differentiated
from P. atrofulvum by the formation of warted stipes and globose
conidia. Furthermore, P. novae-zeelandiae produces patulin, an
extrolite not formed by P. atrofulvum (Frisvad & Filtenborg 1990).
Penicillium aurantiacobrunneum Houbraken, Frisvad &
Samson, sp. nov. MycoBank MB563206. Fig. 13.
Etymology: Named after the orange-brown coloured sclerotia,
produced by this species.
Differt ab omnibus speciebus afinibus divisione elementorum “Ehrlich”
roseoviolacea, ratione CYAS:CYA 1.0–1.2, sclerotiis pallide aurantiacis.
Typus: ex air sample of cake factory, Give, Denmark, A. Svendsen
(CBS H-20662 – holotype, cultures ex-type CBS 126228 = DTO
78G2 = IBT 18753).
taxonoMy of Penicillium Section citrina
Fig. 12. Penicillium atrofulvum. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–C. Sclerotia. D–G. Conidiophores. H. Conidia. Scale bars = 10 µm.
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Houbraken et al.
Fig. 13. Penicillium aurantiacobrunneum. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18
reverse, CREA obverse. B. Sclerotia. C–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
82
taxonoMy of Penicillium Section citrina
Description: Colony diam, 7 d, in mm: CYA 24–30; CYA30°C
germination–3; CYA37°C: no growth; MEA 22–28 mm; YES 31–35
mm; DG18 21–29; ratio CYAS:CYA 1.0–1.2; creatine agar 12–18
mm, weak growth and no acid production.
Description: Colony diam, 7 d, in mm: CYA 29–39; CYA30°C 5–12;
CYA37°C: no growth; MEA 28–38 mm; YES 40–50 mm; DG18
25–34; ratio CYAS:CYA 1.0–1.2; creatine agar 17–26 mm, weak
growth and no acid production.
Good sporulation on CYA with velvety to loccose surface, conidia
dull blue green, mycelium inconspicuous or pale-yellow, exudate
absent or sparsely produced as small clear droplets, soluble
pigments yellow, margin entire or slightly polygonal, reverse yelloworange. Moderate to good sporulation on YES, conidia light green,
soluble pigments yellow, reverse yellow-orange or yellow brown.
Good sporulation on DG18, conidia dull-grey green, reverse pale or
pale yellow. Good sporulation on MEA, conidia grey green or bluish
grey green, colony texture velvety to loccose. Ehrlich reaction
positive (pinkish-violet).
Good sporulation on CYA, velvety to slightly loccose, conidia dull
green, mycelium light yellow, exudate produced in many minute
droplets and clear to light yellow coloured, soluble pigments yellow,
margin polygonal, reverse yellow-orange or orange, but also in
shades of yellow brown, light brown or brown. Good sporulation on
YES, conidia dull green, soluble pigments produced in most isolates
and red, reverse brownish red or blackish red. Good sporulation on
DG18, conidia dull-grey green, mycelium white, reverse (dark) red
with red soluble pigments diffusing into the agar or pale yellow.
Good sporulation on MEA, conidia dull-grey green, colony texture
velvety. Ehrlich reaction negative.
Sclerotia white when young, becoming pale orange to orangebrown, 150–250 µm, sparsely produced on oatmeal agar under a
layer of conidiophores and large exudates droplets; hard, consisting
of polygonal cells; no asci or ascospores observed. Conidiophores
200–400 µm long, predominant biverticillate, occasionally
terverticillate, stipes smooth, 2.5–3.5 µm wide. Metulae in terminal
whorls of 3–6 and mostly equal in length, 10–14 × 2.5–3.5 µm.
Phialides ampulliform with short neck, 7–9 × 2.5–3.5 µm. Conidia
subglobose, smooth, rather large variation in size within an isolate,
2.0–3.0 µm diam.
Extrolites: Benzomalvins, citreoviridin, terrein, “OTOT”.
Diagnostic characters: Ehrlich reaction pinkish-violet, ratio
CYAS:CYA 1.0–1.2, pale orange sclerotia.
Similar species: See P. miczynskii. Penicillium aurantiacobrunneum
morphologically resembles P. miczynskii and P. neomiczynskii, but
can be differentiated by the pinkish-violet Ehrlich reaction of the
former species.
Distribution and ecology: Worldwide distribution; from soil (New
Zealand, Chile) and air (Denmark).
Barcode & molecular based ID: GenBank no. JN617670.
Penicillium aurantiacobrunneum and P. miczynskii share the same
ITS sequence. Partial β-tubulin and/or calmodulin sequences can
be used to identify these species.
Taxonomy and phylogeny: None.
Sclerotia white when young, becoming pale orange to orange-brown
in age, 125–250 (–300) µm, produced on oatmeal agar in a velvety
layer with small exudate droplets; consisting of polygonal cells and
red-brown pigmented spots are present on the surface of the sclerotia;
asci and ascospores not observed. Conidiophores predominantly
biverticillate, but also a large portion terverticillate, additional branch
both direct under terminal whorl and further down the stipe, 200–400
µm long, stipes smooth or occasionally inely roughened, 2.0–3.5
µm wide. Metulae in terminal whorls of 3–6 (–8) and often unequal
in length, 9–13 (–15) × 2.5–3.5 µm. Phialides ampulliform, with short
neck, 7–9 × 2–3 µm. Conidia smooth walled, subglobose to broadly
ellipsoidal, 2.0–3.0 × 2.0–2.5 µm; a small portion of the conidia
larger, globose, 3.0–3.5 µm diam.
Extrolites: The extrolite pattern of P. cairnsense is rather diverse.
CBS 126226, CBS 117982, CBS 118028 and CBS 117962 produce
the extrolites benzomalvins, citreoviridin, phoenicin and decaturin;
CBS 124325, CBS 126225 and DTO 87B9 produce citreoviridin,
terrein and/or quinolactacin. Other extrolites: “KUM”, “MIF”, “MIM”,
“RAI”, “SENGA”.
Diagnostic characters: Red or blackish reverse on YES and/
or DG18, colonies on CYA 29–39 mm, restricted, but consistent
growth on CYA30, ratio CYAS:CYA 1.0–1.2, pale orange to orangebrown sclerotia.
Similar species: See P. miczynskii. Penicillium quebecense is
morphologically similar, but has a CYAS:CYA ratio lower than 1.
Etymology: Named after Cairns (Australia), the city near the
location where the type culture was collected.
Barcode & molecular based ID: GenBank no. JN617669 (CBS 124325T),
JN617664 (CBS 117982). The strains CBS 124324, CBS 124326,
CBS 124325T, CBS 126225 have identical and unique ITS sequences.
The P. cairnsense strains isolated nuts of Carya cordiformis (bitternut),
Niagara Falls, Ontario, Canada (CBS 117982 and CBS 117962) differ
one base pair from CBS 124325T and share ITS sequences with the
type cultures of P. quebecense and P. neomiczynskii.
Differt ab omnibus speciebus afinibus reverso rubro vel subnigro coloniae in agaro
YES et/vel DG18, coloniis in agaro CYA 29–39 mm, constrictis, sed in agaro CYA30
continenter crescentibus, ratione CYAS:CYA 1.0–1.2, sclerotiis pallide aurantiacis
vel aurantiaco-brunneis.
Distribution and ecology: Worldwide; isolated from soil, ants
(Camponotus sp.), decaying basidioma of Lactarius sp. and nut of
Carya cordiformis (bitternut).
Typus: ex soil, Atherton Tableland, Australia, J. Houbraken (CBS
H-20686 – holotype, cultures ex-type CBS 124325 = DTO 30E6 =
IBT 29042).
Taxonomy and phylogeny: Pitt (1980) mentioned in the description
of P. miczynskii that some isolates of this species can produce
red soluble pigment on MEA. These isolates were probably P.
cairnsense, P. quebecense or P. manginii.
Penicillium cairnsense Houbraken, Frisvad & Samson, sp.
nov. MycoBank MB563184. Fig. 14.
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83
Houbraken et al.
Fig. 14. Penicillium cairnsense. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–C. Sclerotia. D–G. Conidiophores. H. Conidia. Scale bars = 10 µm.
84
taxonoMy of Penicillium Section citrina
Penicillium christenseniae Houbraken, Frisvad & Samson,
sp. nov. MycoBank MB563187. Fig. 15.
Etymology: Named after Martha Christensen who collected and
isolated the type culture of this species.
Differt ab omnibus speciebus afinibus stipitibus brevibus et conidiophoris
compactis, coloniis in agaro MEA velutinis, in agaro CREA modice crescentibus et
haud crescentibus in agaro CYA ad 30 °C.
Typus: ex soil in native forest, east/north east side of Costa Rica,
about 30 km inland from Limon and the Caribbean, M. Christensen
(CBS H-20656 – holotypus, cultures ex-type CBS 126236 = DTO
76C3 = IBT 23355).
Description: Colony diam, 7 d, in mm: CYA 31–37; CYA15°C
20–26; CYA30°C and CYA37°C no growth; MEA 21–28; YES
33–38; DG18 21–26; ratio CYAS:CYA 1.0–1.2 creatine agar 16–22,
moderate growth and no acid production.
Good sporulation on CYA, velvety, conidia dull green, mycelium
white, exudate produced in clear droplets, soluble pigments
absent, margin entire, reverse light brown with orange sulcations
in centre. Good sporulation on YES, conidia dull green, mycelium
inconspicuous, soluble pigments absent. Good sporulation on
DG18, conidia dull or dull-grey green, reverse bright yellow or
yellow-orange. Good sporulation on MEA, conidia dull-grey green,
colony texture velvety, mycelium inconspicious. Ehrlich reaction
negative.
Sclerotia absent. Conidiophores predominantly symmetrically
biverticillate and occasionally with an additional branch; stipes
relatively short, up to 250 µm, smooth walled, width, 2.0–3.0 µm;
metulae in a compact terminal whorls of 4–8 (–10), rather equal in
length, vesiculate, 10–15 × 2.0–3.0 µm; phialides ampulliform, 7–9
× 2.0–3.0 µm. Conidia globose to subglobose, inely roughened,
2.0–3.0 µm diam.
Extrolites: Citrinin, quinolactacin, “FON”, “KUM”, “MIF”, “RYLA”.
Diagnostic characters: This species is characterised by its short
stipes (compared with other related species) and compact
conidiophores, velvety colonies on MEA, moderate growth on
CREA and no growth on CYA incubated at 30 °C.
Penicillium chrzaszczii Zaleski, Bull. Int. Acad. pol. Sci.
Lett., Sér. B.: 464. 1927. Fig. 16.
= P. turolense Ramírez & Martínez, Mycopathol. 74: 36. 1981.
Typus: ex woodland soil, Puszcza Bialowieska Forest, Poland
(CBS 217.28 – lectotype, designated here; cultures ex-type IBT
18226 = IBT 11222 = IBT 16409 = DTO 22E4 = FRR 903 = MUCL
29167 = NRRL 903 = NRRL 1741).
Description: Colony diam, 7 d, in mm: CYA 25–33; CYA15°C 16–
22; CYA30°C and CYA37°C no growth; MEA 21–28; YES 28–36;
DG18 20–27; ratio CYAS:CYA 0.95–1.1; creatine agar 15–20, weak
growth and no acid production.
No or weak sporulation on CYA, velvety, conidia grey-green,
mycelium inconspicuous, exudate absent or sparsely present as
minute clear droplets, soluble pigments present in fresh isolates
and weak yellow coloured, margin slightly polygonal, reverse
(pale) yellow-orange. Sporulation on YES absent, mycelium white,
soluble pigments absent, reverse vivid yellow or yellow-orange.
No or poor sporulation on DG18, white mycelium, yellow soluble
pigments produced in time, reverse pale or vivid yellow. Weak to
moderate sporulation on MEA, conidia grey green when young
and becoming dull green in age, colony texture loccose. Ehrlich
reaction negative.
Sclerotia absent. Conidiophores symmetrically biverticillate and
often with an divergent branch, often starting 40–60 µm below the
terminal verticil; stipes rather long, up to 500 µm, smooth, 2.5–3.5
µm wide; metulae in a compact terminal verticil, 4–7 (–9), unequal
in length, vesiculate, 10–14 × 2.5–3.5 µm; phialides ampulliform,
7–9 × 2–3 µm. Conidia globose to subglobose, inely roughened,
2.0–3.0 µm diam.
Extrolites: Citrinin, terrein, “MIF”, “MIM”, “RAI”, “3T”, “VERN” (also
see Christensen et al. 1999).
Diagnostic characters: No or poor sporulation on CYA, inely
roughened conidia, no growth at 30 °C, often with terverticillate
structures, yellow soluble pigment production on CYA, reverse on
DG18 in shades of yellow (pale or vivid).
Similar species: This species produces inely rough walled globose
conidia and does not grow at 30 °C, which is also observed in
species such as P. westlingii, P. waksmanii and P. godlewskii.
However, the moderate growth on CREA, the velvety colonies on
MEA and short stipes are characteristic for this species.
Similar species: Phylogenetically, P. chrzaszczii is related to P.
godlewskii and P. waksmanii. The reverse on CYA of P. waksmanii
is in shades of beige-brown, while P. godlewskii and P. chrzaszczii
have reverses in shades of yellow and/or orange. Penicillium
godlewskii is more restricted in its growth on CYA (15–25 mm)
than P. chrzaszczii (25–33 mm). Penicillium chrzaszczii can
be distinguished from P. miczynskii and related species by the
formation of globose, roughened conidia.
Distribution and ecology: Soil of a native forest and litter of Manilkara
bidenta or Guarea guidonia; Costa Rica and Puerto Rico, USA.
Distribution and ecology: This species is not commonly occurring
and was previously isolated from soil in Poland and France.
Barcode & molecular based ID: GenBank no. JN617674.
Penicillium christenseniae has unique β-tubulin, calmodulin and
ITS sequences.
Barcode & molecular based ID: GenBank no. GU944603.This
species shares identical ITS sequences with P. decaturense,
but can be identiied based on partial β-tubulin and calmodulin
sequences.
Taxonomy and phylogeny: This species is phylogenetically unique
and belongs to the P. westlingii-clade. However, it does shares the
production of quinolactacin and “FON” with P. steckii.
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Taxonomy and phylogeny: Penicillium chrzaszczii was described
by Zaleski (1927) in the subsection “concentrice-undulata”, which
is characterised by concentric sulcated colonies. This feature was
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Houbraken et al.
Fig. 15. Penicillium christenseniae. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
Fig. 16. Penicillium chrzaszczii. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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Houbraken et al.
not observed on the agar media used in this study. Raper & Thom
(1949) placed P. chrzaszczii in synonymy with P. jensenii and Pitt
(1980) synonymised this species with P. miczynskii. Molecular
data indicate that P. turolense (CBS 176.81) is a synonym of P.
chrzaszczii. Our strain of P. turolense is degenerated and sporulates
weakly on most agar media. The original description shows typical
ornamented conidia and biverticillate conidiophores (Ramírez &
Martinez 1981) and therefore this species can be conidentially
placed in synonymy.
Penicillium citrinum Thom, Bull. U.S. Dep. Agric., Bur.
Animal Indus. 118: 61. 1910. Fig. 17.
= Citromyces subtilis Bainier & Sartory, Saccardo’s Syll. fung. XXV: 684. 1912.
= Penicillium subtile (Bainier & Sartory) Biourge, Cellule 33: 106. 1923. (nom.
illegit.,Art. 64; non Berk. 1841.
= Penicillium auriluum Biourge, Cellule 33: 250. 1923.
= Penicillium phaeojanthinellum Biourge, Cellule 33: 289. 1923.
= Penicillium implicatum Biourge, Cellule 33: 278. 1923.
= Penicillium sartoryi Thom [as ‘sartorii’], The Penicillia: 233. 1930.
= Penicillium botryosum Bat. & H. Maia, Anais Soc. Biol. Pernambuco 15: 157.
1957.
Typus: unrecorded source (IMI 92196ii, type of both P. citrinum and
P. auriluum; cultures ex-type DTO 22F3 = CBS 139.45 = Biourge
53 = Thom 4733.14 = ATCC 1109 = ATCC 36382 = CECT 2269 =
FRR 1841 = IMI 091961 = IMI 092196 = LSHB P25 = LSHB P6 =
LSHB Ad95 = MUCL 29781 = NRRL 1841 = NRRL 1842).
Description: Colony diam, 7 d, in mm: CYA 27–33; CYA15°C 5–10;
CYA30°C 27–40; CYA37°C 2–12; MEA 18–25; YES 29–37; DG18
15–23; ratio CYAS:CYA 0.9–1.2; creatine agar 10–19, poor growth,
no or weak acid.
Moderate sporulation on CYA, conidia grey green or blueish grey
green, mycelium inconspicuous, small exudate droplets produced
by some strains and clear or pale yellow coloured, soluble pigments
yellow, margin entire, reverse brownish-yellow. Moderate to good
sporulation on YES, conidial colour variable: grey green to dark
green, soluble pigment present in majority of strains and strong
yellow or yellow-orange coloured, reverse yellow to yellow-orange.
Moderate to good sporulation on DG18, conidia grey green, reverse
pale and occasionally pale with yellow centre. Moderate to good
sporulation on MEA, conidia grey green with a strong blue element,
colony texture velvety. Ehrlich reaction negative.
Sclerotia absent. Conidiophores arising from mycelial mat,
predominant symmetrically biverticillate, terverticillate structures
abundantly produced in fresh isolates; stipes smooth, 100–300 ×
2.0–3.0 µm. Metulae in whorls of 3–4 (–6), 12–16 × 2.0–3.0 µm.
Phialides ampulliform, 7.5–10 × 2.0–2.5 µm. Conidia globose to
subglobose, smooth, 2.0–2.5 × 2.0–2.5 µm.
Extrolites: Citrinin, quinolactacins, citrinadins, perinadine, several
anthraquinones, “CITY”, “met k” and “shamix” (Houbraken et al.
2010).
Diagnostic characters: Growth on CYA when incubated at 37 °C,
2–12 mm in diam, reverse on CYA in shades of yellow, soluble
pigment production on CYA and YES, globose, smooth walled
conidia.
Similar species: Penicillium citrinum belongs to the P. citrinumclade and can be differentiated by other members of this series by
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its ability to grow at 37 °C and the formation of yellow or yelloworange soluble pigments on YES.
Distribution and ecology: This species has a worldwide distribution
and occurs more frequently in the (sub)tropics than in temperate
regions. Penicillium citrinum is isolated from soils, but also from
indoor air, food and as an endophyte of root, stem, leaves of coffee
plants (Posada et al. 2007) and roots of Ixeris repens (Khan et al.
2008; identity based on ITS sequences deposited in GenBank).
Barcode & molecular based ID: GenBank no. GU944562. A gap
of 36–38 bp was observed in the alignment of the ITS1 region
of all P. citrinum isolates, when compared to most other species
of this series. This species has unique ITS, partial β-tubulin and
calmodulin sequences.
Taxonomy and phylogeny: Penicillium implicatum is synonymised
with P. citrinum (Houbraken et al. 2010). Pitt (1980) considered
the type strain of P. implicatum lost and designated IMI 190235
(= CBS 184.81) as the neotype. However, the type culture of P.
implicatum, deposited by Thom, is maintained at the CBS under
CBS 232.38 and resembles P. citrinum in many aspects (Frisvad et
al. 1990a, Houbraken et al. 2010). Houbraken et al. (2010) placed
P. phaeojanthinellum and P. botryosum in synonymy with P. citrinum
and more details about the taxonomy of P. citrinum can be found
there.
Penicillium copticola Houbraken, Frisvad & Samson, sp.
nov. MycoBank MB563205. Fig. 18.
Etymology: Referring to pastery, the substrate where the type strain
was growing on.
Differt ab omnibus speciebus afinibus coloniis in agaro CREA bene crescentibus,
in agaro CYA ad 33 °C quoque crescentibus, coloniis in agaro MEA loccosis,
conidiophoris biverticillatis.
Typus: ex tortilla, USA, J. Murray (CBS H-20643 – holotypus,
cultures ex-type CBS 127355 = DTO 19H7 = IBT 30771).
Description: Colony diam, 7 d, in mm: CYA 31–37; CYA15°C 7–11;
CYA30°C 13–17; CYA37°C no growth; MEA 25–34; YES 35–41;
DG18 27–35; ratio CYAS:CYA 1.0–1.2; creatine agar 18–25, good
growth, weak acid production followed by (delayed) base reaction.
Moderate or good sporulation on CYA, velvety, conidia dull green
or dull-pure green, mycelium inconspicuous, exudate produced
as minute clear droplets, soluble pigments absent, reverse pale
beige or crème. Good sporulation on YES, conidia dull green,
soluble pigment absent, reverse yellow to dark beige, with a darker
greenish centre. Dull green conidia on DG18, reverse transparent
or pale with a pale-cream centre. Colonies on MEA pure green or
dull-pure green, colony texture loccose. Ehrlich reaction negative.
Sclerotia absent. Conidiophores predominantly symmetrically
biverticillate, young conidophores monoverticillate, stipes up to
500 µm long, smooth, 2.0–3.0 µm wide; metulae in a compact
terminal whorls of 2–4, equal or unequal in length, 12–16 × 2.0–3.5
µm, occasionally vesiculate. Phialides ampulliform to cylindrical,
7.5–9 × 2.0–3.0 µm. Conidia broadly ellipsoidal, smooth, 2.5–3.0
× 2.0–2.5 µm.
taxonoMy of Penicillium Section citrina
Fig. 17. Penicillium citrinum. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse, CREA
obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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Houbraken et al.
Fig. 18. Penicillium copticola. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse, CREA
obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
Extrolites: “GULLA”, “HAEN”, “PRS”, “VERSI”.
Diagnostic characters: Good growth on CREA with base production,
growth on CYA incubated at 33 °C, loccose colonies on MEA,
biverticillate conidiophores.
Similar species: See P. terrigenum.
Distribution and ecology: This species has a worldwide distribution.
It is isolated from tortillas (USA), seed from ripe coffee berry
(Hawaii, USA; NRRL 32575, GenBank DQ123664ITS), dried lowers
of Cannabis sativa, the Netherlands and air of a toilet in Germany.
Barcode & molecular based ID: GenBank JN617685. This species
can be identiied with ITS, partial β-tubulin and/or calmodulin
sequences.
Taxonomy and phylogeny: Isolate NRRL 32575 was listed as
Penicillium sp. by Vega et al. (2006) and comparison of the ITS
sequence of this strain deposited in GenBank (DQ123664) shows
that it is P. copticola.
Penicillium cosmopolitanum Houbraken, Frisvad &
Samson, sp. nov. MycoBank MB563188. Fig. 19.
Etymology: Named after the worldwide distribution of this species.
Differt ab omnibus speciebus afinibus conidiis exasperatis, coloniis haud
crescentibus ad 30 °C, reverso psammocolorato-brunneo in agaro CYA, reverso
pallide lavido vel eburneo in agaro YES, conidiis in agaro CYA et YES haud vel vix
formantibus.
Typus: ex heathland soil, Cartier heide, Eersel, the Netherlands,
J. Houbraken (CBS H-20665 – holotypus, cultures ex-type CBS
126995 = DTO 92E8 = IBT 30681).
Description: Colony diam, 7 d, in mm: CYA 25–32; CYA15°C 15–
20; CYA30°C and CYA37°C no growth; MEA 20–29; YES 27–36;
DG18 16–25; ratio CYAS:CYA 0.8–1.0 (–1.1); creatine agar 10–18,
weak growth and no acid production.
Sporulation on CYA in most isolates absent or weak, occasionally
moderate to good, velvety, conidia dull green, mycelium white,
exudate occasionally present as small clear droplets, soluble
pigments absent, margin polygonal or entire, reverse beigebrown with orange coloured sulcations giving the colony a pinkish
tinge, some isolates pale beige or beige (CBS 200.86 and CBS
124316). Sporulation on YES mostly absent, mycelium white,
soluble pigments absent, reverse cream, cream-buff or light beige.
Sporulation on DG18 moderate to good, conidia dull or grey green,
reverse transparent, pale beige or cream. Colonies on MEA poorly
sporulating, conidia blueish green or dull green, colony texture
loccose. Ehrlich reaction negative.
Sclerotia absent. Conidiophores symmetrically biverticillate,
often with an divergent branch that is shorter than the main axis,
occasionally quaterverticillate; stipes long, up to 500 µm, smooth,
2.5–4.0 µm wide; metulae in a compact terminal verticil, 3–6 (–8),
more or less even in length, vesiculate and non-vesiculate, 9–13
(–15) × 2.0–3.5 µm; phialides ampulliform, 6.5–8.5 × 2–3 µm.
Conidia globose, rough, 2.5–3.0 µm diam.
www.studiesinmycology.org
Extrolites: Citrinin, okaramin, perinadine, territrems, “CURVO”,
“HAEN”, “PHOE”, “ROTO”, “SENGA”, “TRIP”, “VERSI”,
“XANTHOC”.
Diagnostic characters: Rough walled conidia, no growth at 30 °C,
reverse on CYA beige-brown, reverse on YES pale yellow to cream,
no or weak sporulation on CYA and YES.
Similar species: See P. westlingii.
Distribution and ecology: This species is frequently isolated from
soils in the Netherlands, Poland, Denmark and New Zealand.
Barcode & molecular based ID: GenBank no. JN617691 (Fig. 3,
clade 1, 2 and 3), JN617682 (Fig. 3; clade 4). Clades 1, 2 and
3 in P. cosmopolitanum have identical ITS sequences, and these
sequences are also shared by certain isolates of P. westlingii
(CBS 124312, CBS 124313, CBS 127003, CBS 127040, see
also description of P. westlingii). Members of clade 4 share ITS
sequences with certain strains of P. godlewskii and P. nothofagi.
Taxonomy and phylogeny: Molecular analysis of partial β-tubulin and
calmodulin data shows that this species can be subdivided into four
subclades (Fig. 3). No clear morphological differences were observed
among these clades, although strains of clade 2 have slightly paler
reverse colours on CYA (e.g. CBS 126995T, CBS 200.86).
Penicillium decaturense S.W Peterson, Bayer & Wicklow,
Mycologia 96: 1290. 2004. Fig. 20.
Typus: ex old resupinate fungus, Ramsey Lake State Park,
Decatur, Illinois, USA (BPI 842267 – holotypus, cultures ex-type
CBS 117509 = IBT 27117 = DTO 3F7 = NRRL 28152).
Description: Colony diam, 7 d, in mm: CYA 32–40; CYA15°C 12–
18; CYA30°C 5–15; CYA37°C no growth; MEA 27–34; YES 39–47;
DG18 23–30; ratio CYAS:CYA 0.9–1.1; creatine agar 11–18, weak
growth and no acid production.
Good sporulation on CYA, velvety, condia dark-green or bluegrey-green, mycelium inconspicuous, exudate production variable,
absent, sparsely or predominant, clear or light yellow, soluble
pigments absent, margin entire, reverse orange-beige to skin
coloured, occasionally with beige-brown centre. Good sporulation
on YES, conidia dark green, mycelium white, soluble pigments
absent, reverse yellow-orange, in some isolates yellow. Good
sporulation on DG18, conidia dull-grey green, reverse pale, cream
or pale yellow. Good sporulation on MEA, conidia blue-green or
blueish-dark green, colony texture loccose to velvely. Ehrlich
reaction negative.
Sclerotia absent. Conidiophores symmetrically biverticillate,
occasionally with an divergent branch that is shorter than the main
axis; stipes up to 300 µm, smooth to very inely rough, 2.0–3.5
µm; metulae in a compact terminal verticil, 3–5 (–7), unequal in
length, vesiculate, 10–16 x 2.0–3.5 µm; phialides ampulliform,
broad, 7.0–9.0 × 2.0–3.5 µm. Conidia globose to subglobose, inely
roughened, 2.0–2.5 µm diam.
Extrolites: Daldinin D, decaturin A and deoxyoxalicine B (Zhang et
al. 2003), terrein, “SENGA”, “SNIL”, “SVOL”, “VERSI”, “XANTHOC”.
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Houbraken et al.
Fig. 19. Penicillium cosmopolitanum. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
Fig. 20. Penicillium decaturense. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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Houbraken et al.
Diagnostic characters: Finely roughened conidia, all examined
isolates grow at 30 °C and some up to 33 °C, fast growing: 32–40
mm on CYA in 7 d at 25 °C.
Similar species: Penicillium decaturense forms inely roughened
(sub)globose conidia. This feature is shared by several other
species, such as P. godlewskii, P. pancosmium, P. ubiquetum, P.
cosmopolitanum, P. westlingii and P. chrzaszczii. This species can
be differentiated from the above mentioned species by its ability to
grow consistently at 30 °C (5–15 mm).
Distribution and ecology: This species has been isolated as a
colonist of fungal sporocarps (Trichaptum biformis and Ischnoderma
sp.), collected in Illinois, Georgia and Florida, USA (Peterson et al.
2004).
Barcode & molecular based ID: GenBank no. GU944604. This
species shares ITS sequences with P. chrzaszczii. Partial β-tubulin
and calmodulin sequences can be used for identiication.
Taxonomy and phylogeny: This species is a unique member of the
P. westlingii-clade, because it is able to grow up to 33 °C. Penicillium
decaturense is phylogenetically related to P. pancosmium.
Penicillium euglaucum van Beyma, Ant. van Leeuwenhoek
6: 269. 1940. Fig. 21.
= Eupenicillium euglaucum (van Beyma) Stolk & Samson, Stud. Mycol. 23:
90. 1983.
Typus: ex soil, Argentina (CBS 323.71 – neotype, Stolk & Samson
1983; cultures ex-type DTO 23B9 = IBT 30767).
Description: Colony diam, 7 d, in mm: CYA 23–29; CYA15°C 3–8;
CYA30°C 21–30; CYA37°C (0–)5–15; MEA 22–26; YES 23–30;
DG18 23–29; ratio CYAS:CYA 0.9–1.1; creatine agar 8–16, weak
growth, weak acid and no base production.
Sporulation on CYA absent or inconspicuous in fresh isolates,
moderate to good sporulation in cultures maintained for longer
periods in culture, conidia blue-grey green, cleistothecia abundantly
produced, pale yellow when young, becoming warm grey in
age, mycelium inconspicuous or light yellow, exudate produced
in large clear or light yellow coloured droplets, soluble pigment
production strong, yellow coloured, margin entire, reverse yellow
or yellow-brown and becoming dark brown in age. Sporulation
on YES inconspicuous in fresh cultures, cleistothecia abundantly
produced in age, warm-grey coloured, mycelium light yellow, strong
yellow soluble pigments production, reverse in shades of yellowbrown. Sporulation on DG18 weak in fresh cultures and strong in
degenerated cultures, conidia grey-green, mycelium white, reverse
yellow. Sporulation on MEA inconspicuous and not inluencing the
colony colour, cleistothecia abundantly produced light yellow to
grey coloured when young and becoming warm grey in age. Ehrlich
reaction negative.
Cleistothecia abundantly produced on CYA, MEA and YES, globose
or subglobose, up to 400 µm diam, consisting of sclerotioid masses
of polygonal cells, ripening after 4–5 wk or more; warm-grey on MEA
and CYA, grayish-brown on oatmeal agar. Ascospores ellipsoidal,
with 2 appressed equatorial ridges, inely roughened valves in
light microscope, reticulate with SEM, 3.0–4.0 x 2.5–3.0 µm.
Conidiophores simple when young becoming biverticillate in age,
94
stipes 5–60 (–100) µm long, occasionally longer, smooth walled or
nearly so, 1.5–3.0 µm wide. Metulae, when present, in verticils of
2–3 (–4), unequal in length, 10–20 × 1.5–3.0 µm, often inlated at
the apex, 2.5–5.0 µm wide. Phialides ampulliform, 7.0–9.0 × 2–3
µm. Conidia globose, inely roughened, 2.0–2.5 µm diam.
Extrolites: Terrein, “ALK”, “FRIL”, “GLAD”, “RAI”, “SPOKO”, “3-T”.
Diagnostic characters: Penicillium euglaucum is characterised by
the production of warm-grey coloured cleistothecia, strong yellow
soluble pigment production, good growth at 30 °C and ascospores
3.0–4.0 x 2.5–3.0 µm.
Similar species: See P. anatolicum.
Distribution and ecology: Penicillium euglaucum is isolated from
Argentinean soil.
Barcode & molecular based ID: GenBank no. JN617699. This
species has unique ITS, β-tubulin and calmodulin sequences.
Taxonomy and phylogeny: Penicillium euglaucum was neotypiied
by Stolk & Samson (1983) with CBS 323.71, which resembles
van Beyma’s original notes of P. euglaucum. They noted that
Penicillium citreonigrum is the anamorph of E. euglaucum and
thirty-seven species were placed in synonymy with these two
species (Stolk & Samson 1983). Houbraken & Samson (2011)
show that the type culture of P. citreonigrum, CBS 258.29, is
phylogenetically unrelated to P. euglaucum. Analysis of the other
synonyms mentioned shows that P. euglaucum is unrelated to any
of those species (J. Houbraken, unpublished results) and therefore
P. euglaucum is not as commonly occurring as suggested by Stolk
& Samson (1983).
Penicillium gallaicum Ramírez, Martínez & Berenguer,
Mycopathol. 72: 29. 1980. Fig. 22.
= Penicillium alicantinum Ramírez & Martínez, Mycopathol. 72: 185. 1980.
= Penicillium syriacum Baghdadi, Novosti Sist. Nizs. Rast. 1968: 111. 1968
(pro parte).
Typus: ex air, Madrid, Spain (IJFM 5597 – holotype, cultures ex
type DTO 34G3 = CBS 167.81 = ATCC 42232 = IMI 253794 = VKM
F-2190 = IBT 22016).
Description: Colony diam, 7 d, in mm: CYA 19–25; CYA15°C 3–6;
CYA30°C 18–25; CYA37°C 0–5; MEA 24–30; YES 26–32; DG18
24–30; ratio CYAS:CYA 0.9–1.1; creatine agar 7–17, weak growth
and acid production absent or only beneath the colony.
Sporulation on CYA absent, weak or moderate, conidia dull or pale
grey green, mycelium pale yellow or pale crème, exudates present
as droplets pale yellow, strong yellow-orange soluble pigments
production, margin entire, reverse yellow-orange and becoming
yellow brown in age or yellow-brown. Sporulation on YES absent
or weak, conidia grey-green, mycelium white or pale beige,
soluble pigments yellow-orange, reverse orange or orange-brown.
Sporulation on DG18 absent or weak, obverse dull-grey green
because of conidia or as white mycelium, reverse vivid yellow or
yellow with conidial colour visible through the colony. Colonies
on MEA weakly sporulating, mycelium white, crème or light grey
coloured. Ehrlich reaction negative.
taxonoMy of Penicillium Section citrina
Fig. 21. Penicillium euglaucum. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B. Ascomata. C–D. Ascospores. E–G. Conidiophores. H. Conidia. Scale bars = 10 µm.
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Houbraken et al.
Fig. 22. Penicillium gallaicum. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse, CREA
obverse. B. Sclerotia. C–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
Sclerotia inconspicuously formed under a layer of mycelium or
conidiophores; white and soft when young, becoming hard and
orange-brown in age, 60–100 (–150) µm; asci and ascospores
not observed after prolonged incubation. Conidiophores
monoverticillate occasionally with additional branch, stipes up to
50 µm, smooth walled, 2.0–3.0 µm. Phialides ampulliform, 8.0–10
× 2–3.5 µm. Conidia globose or subglobose, smooth, 2.0–2.5 µm
diam.
Extrolites: Citreoviridin (Frisvad et al. 1990b), “KOKSO”, “3-S”,
“TIDL”, “VYL”.
Diagnostic characters: Short monoverticillate conidiophores,
yellow-orange soluble pigments on CYA and YES, and yelloworange reverse becoming brown yellow brown on CYA, sclerotia
production.
Similar species: Penicillium gallaicum is unique in section Citrina
and shares monoverticillate conidiophores with P. roseopurpureum
and P. sanguiluum. However, these species produce reddish
soluble pigments. Macromorphologically, P. gallaicum resembles
P. citreonigrum and both species produce citreoviridin (Frisvad et
al. 1990b).
Distribution and ecology: Three strains were studied, two from air in
Madrid, Spain and one from soil in Syria.
Barcode & molecular based ID: GenBank no. JN617690. This
species has unique ITS, β-tubulin and calmodulin sequences.
Taxonomy and phylogeny: Christensen et al. (1999) examined extype material of P. syriacum and indicated that this strain is a mixed
culture. One of the isolates originating from the type of P. syriacum
(CBS 418.69) is a P. galliacum. This strain has monoverticillate
conidiophores and does not resemble Baghdadi’s original
description (Baghdadi 1968).
Penicillium godlewskii Zaleski, Bull. Int. Acad. pol. Sci.
Lett., Sér. B.: 466. 1927. Fig. 23.
= Penicillium kapuscinskii Zaleski, Bull. Int. Acad. pol. Sci. Lett., Sér. B: 484.
1927.
Typus: ex soil under pine, Bialowieska, Poland (CBS 215.28 –
lectotype, designated here; cultures ex type DTO 22E2 = ATCC
10449 = ATCC 48714 = FRR 2111 = IFO 7724 = IMI 040591 =
MUCL 29243 = NRRL 2111 = QM 7566 = VKM F-1826).
Description: Colony diam, 7 d, in mm: CYA 15–25; CYA15°C 13–
20; CYA30°C and CYA37°C no growth; MEA 12–20; YES 20–30;
DG18 15–23; ratio CYAS:CYA 1.0–1.4; creatine agar 10–17, weak
growth and no acid production.
Moderate to good sporulation on CYA, velvety, conidia grey-green,
mycelium inconspicuous, exudate absent, soluble pigment absent,
margin entire to slightly polygonal, reverse in shades of orange,
often beige-orange. Sporulation on YES variable, absent to good,
mycelium white, soluble pigments absent, reverse beige, beigeorange or yellow-orange. Moderate to good sporulation on DG18,
conidia dull-green or grey-green, reverse pale. Moderate to good
sporulation on MEA, conidia grey green, becoming blue-grey green
in age, colony texture velvety with loccose centre. No reaction with
Ehrlich test.
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Sclerotia absent. Conidiophores symmetrically biverticillate and
often with an divergent branch, starting often 30–50 µm under
terminal verticil; stipes long, up to 700 µm, smooth and rather
broad, 2.5–4.0 µm; metulae in a compact terminal verticil, 5–8
(–10), unequal in length, vesiculate, 9–13 (–15) × 2.5–3.5 µm;
phialides ampulliform, 6.5–8.5 × 2–3 µm. Conidia globose to
subglobose, inely roughened, 2.0–2.5 µm diam.
Extrolites: Citrinin, citreoviridin, decaturin, an okaramin, perinadine,
“TRIP”.
Diagnostic characters: Finely roughened conidia, weak growth on
CYA incubated at 27 °C (0–5 mm), reverse on CYA in shades of
yellow-orange.
Similar species: See P. chrzaszczii.
Distribution and ecology: Soil appears to be the primary habitat,
but also isolated from butter; known from Poland, Germany and
the Netherlands.
Barcode & molecular based ID: GenBank no. JN617692.
Penicillium godlewskii shares ITS sequences with P. nothofagi and
certain strains of P. cosmopolitanum (Fig. 3, clade 4) (CBS 126997,
CBS 127038). Penicillium godlewskii can be identiied using partial
β-tubulin and/or calmodulin sequences.
Taxonomy and phylogeny: Penicillium godlewskii was described
by Zaleski (1927). Raper & Thom (1949) gave it as a separate
species status in their monograph, while Pitt (1980) placed this
species in synonymy with P. jensenii. Type material of this species
(CBS 215.28T) is degenerated. Sequences generated from this
strain indicate that P. godlewskii is distinct and belongs to the P.
westlingii-clade. Raper & Thom (1949) placed P. kapuscinskii in
the Penicillium nigricans series and Pitt (1980) accommodated this
species in the Canescentia series. The main reason for this was the
formation of ornamented conidia. However, molecular data indicate
that this species is a synonym of P. godlewskii, a species that
also forms (inely) roughened conidia. Furthermore, the original
drawing of Zaleski (1927:55) shows that P. kapuscinskii produces
symmetrically biverticillate structures, indicating a relation with
section Citrina. The isolate maintained in the CBS collection is
degenerated and produces conidiophores sparsely.
Penicillium gorlenkoanum Baghdadi, Nov. sist. Niz. Rast.,
1968: 97. 1968. Fig. 24.
= Penicillium damascenum Baghdadi, Nov. sist. Niz. Rast., 1968: 101. 1968.
Typus: ex soil, Syria (CBS 408.69 – type; cultures ex-type DTO
34E3 = FRR 511 = IMI 140339 = VKM F-1079).
Description: Colony diam, 7 d, in mm: CYA 26–31; CYA15°C 8–12;
CYA30°C 20–30; CYA37°C no growth; MEA 20–27; YES 26–30;
DG18 18–26; ratio CYAS:CYA 1.0–1.1; creatine agar 13–19, weak
growth and no or weak acid production.
Moderate or good sporulation on CYA, velvety with loccose
centre, conidia grey, dull green or dark green, mycelium
inconspicuous, exudate droplets minute and clear or weak yellow
coloured, soluble pigments absent, margin entire, reverse pale
yellow or crème-brown. Degree of sporulation on YES variable:
weak (CBS 409.69) to strong (CBS 408.69), conidia grey green,
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Houbraken et al.
Fig. 23. Penicillium godlewskii. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
Fig. 24. Penicillium gorlenkoanum. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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Houbraken et al.
soluble pigment absent, reverse pale yellow. Sporulation on
DG18 variable, absent to strong, condia grey green or dark dull
green, reverse pale or pale-light yellow. Variable sporulation on
MEA, conidia grey green, colony texture velvety to loccose.
Ehrlich reaction negative.
Sclerotia absent. Conidiophores from aerial hyphae, predominantly
irregularly biverticillate, stipes smooth, width 2.0–2.7. Metulae
terminal in whorls of 2–3, 12–17 × 2.2–3.0 µm. Phialides
ampulliform, 7.5–9.0 × 2.0–3.0 µm. Conidia globose to subglobose,
smooth to inely roughened, variable in size, predominantly 2.0–2.5
µm, smaller portion of conidia larger, 2.5–3.0 µm diam.
Extrolites: Citrinin, costaclavin, chanoclavine-I (Kozlovskiĭ et al.
1981a, 1981b), “KUSK”, “PHOE”, “WK”, “WS”, “WT” and “WØ”
(Houbraken et al. 2010).
Diagnostic characters: No growth at 37 °C, production of
chanoclavine-I.
Similar species: Penicillium gorlenkoanum is related to P. citrinum
and related species. It can be distinguished from these species by
the production of chanoclavine-I, a crème-brown reverse on CYA,
absence of cleistothecia, and no growth at 37 °C.
Distribution and ecology: This species is only known from Syrian soil.
Barcode & molecular based ID: GenBank no. GU944581. This
species has unique ITS, β-tubulin and calmodulin sequences.
Taxonomy and phylogeny: Only two strains of this species were
available for examination (CBS 408.69 and CBS 409.69) and both
lacked typical terminal metulae in whorls of 5–8, as reported and
shown in the original descriptions (Baghdadi 1969). This might
be a result of degeneration of these cultures during preservation.
The conidial size and the original drawings of the conidiophores
indicate that this species belongs to section Citrina. Combined
morphological, molecular and extrolite data show that Penicillium
gorlenkoanum is conspeciic with and P. damascenum.
Penicillium hetheringtonii Houbraken, Frisvad & Samson,
Fung. Divers. 44: 125. 2010. Fig. 25.
Typus: ex soil, Treasure Island, Florida, USA, R.A. Samson (CBS
122392 – holotype, cultures ex-type DTO 5H9 = IBT 29057).
Description: Colony diam, 7 d, in mm: CYA 26–32; CYA15°C 7–11;
CYA30°C 26–34; CYA37°C 0–2; MEA 17–23; YES 27–35; DG18
16–25; ratio CYAS:CYA 0.8–1.0; creatine agar 13–17, poor growth
on creatine agar, no acid production.
Moderate to good sporulation on CYA, velvety, conidia dull green
or dark green, mycelium inconspicuous, small hyaline exudate
droplets, diffusible pigments absent, margin entire, reverse colour
crème-brown. Moderate to good sporulation on YES, conidia dark
green, mycelium inconspicuous, soluble pigments absent, reverse
orange. Good sporulation on DG18, conidia grey green, reverse in
shades of yellow (varying from pale to bright). Good sporulation on
MEA, conidia dark grey green, colony texture velvety and loccose
in centre. Ehrlich reaction negative.
100
Sclerotia absent. Conidiophores borne from surface hyphae,
predominant
symmetrically
biverticillate,
terverticillate
conidiophores occasionally present; stipes smooth, 2.5–3.5 µm
wide. Metulae in compact whorls of 4–8 (–12), 11–15 × 2.5–3.5
µm, vesticulated, even in length. Phialides ampulliform, 7.0–9.2
× 2.0–3.0 µm. Conidia globose to subglobose, smooth to inely
roughened, 2.0–2.5 µm diam.
Extrolites:
Citrinadine,
citrinin,
quinolactacin,
two
anthraquinones,“SHAMIX”, “FON”, “CITY”, “PR1-x” (Houbraken et
al. 2010).
Diagnostic characters: Metulae in verticils of 4–8 (–12), crèmebrown reverse on YES, lacking diffusible soluble pigments on
YES and CYA, CYAS:CYA 0.8–1.0, production of uncharacterised
metabolite PR1-x.
Similar species: Penicillium hetheringtonii resembles P. citrinum in
having similar growth rates on agar media and an orange reverse
on YES, but differs from P. citrinum in having broader stipes, 4–8
closely appressed metulae and lacking the production of soluble
pigments on YES and CYA.
Distribution and ecology: This species probably has a worldwide
distribution and has a preference for warmer climates. It has
been isolated from soil in Florida, USA and Queensland,
Australia.
Barcode & molecular based ID: GenBank no. GU944558. This
species can be identiied with ITS sequences. It has a 36–38 bp
deletion in the ITS1 when compared with other members of section
Citrina. This deletion was also observed in all isolates of P. citrinum
and CBS 327.79 (P. manginii).
Taxonomy and phylogeny: None.
Penicillium manginii Duché & Heim, Recl. Trav. Cryptog.
Louis Mangin: 20. 1931. Fig. 26.
= Penicillium pedemontanum Mosca & Fontana, Allionia 9: 40. 1963.
Typus: unrecorded source (CBS 253.31 – neotype, designated by
Pitt et al. 2000; cultures ex-type DTO 22E9 = NRRL 2134 = IMI
191732 = FRR 2134 = IBT 18224).
Description: Colony diam, 7 d, in mm: CYA 28–40; CYA15°C 19–
27; CYA30°C 0–8; CYA37°C no growth; MEA 25–37; YES 35–47;
DG18 18–27; ratio CYAS:CYA (0.85–) 1.0–1.3; creatine agar 16–
22, weak growth and no acid production.
Moderate to good sporulation on CYA, velvety, conidia grey-green,
mycelium light-yellow, exudate in some strains produced as minute
clear or yellow droplets, soluble pigment yellow, margin in most
isolates entire, in some strains polygonal, reverse orange or orange
with red centre. Moderate to good sporulation on YES, conidia
grey green, mycelium light-yellow, strong red soluble pigment
production, reverse blackish-red or dark red-brown. Moderate to
good sporulation on DG18, conidia grey green, reverse in most
isolates deep-red with red soluble pigments, occasionally yellow
or pale, conidia. Sporulation variable on MEA, varying from absent
to good, conidia grey green, colony texture velvety, becoming
loccose in age. Ehrlich reaction negative.
taxonoMy of Penicillium Section citrina
Fig. 25. Penicillium hetheringtonii. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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101
Houbraken et al.
Fig. 26. Penicillium manginii. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse, CREA
obverse. B–C. Sclerotia. D–G. Conidiophores. H. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
Sclerotia light yellow-brown and soft when young, becoming orange
brown and hard in age, consisting of large polygonal cells, with red
brown pigmented hyphe present on the sclerotial body, 100–250
µm, irregular in shape. No ascospores observed after incubation
on OA for 3 mo. Conidiophores predominantly symmetrically
biverticillate and, depending on the isolate, additional branches can
occur; stipes 200–500 µm long, inely rough walled occasionally
smooth walled, width variable, 2.0–4.0 µm; metulae in a compact
terminal whorls of 2–4 (–6), even in length, non-vesiculate, 10–14
× 2.0–3.5 µm; phialides ampulliform, 7–9 × 2.0–3.0 µm. Conidia
(broadly) ellipsoidal, smooth, 2.5–3.0 × 2.0–2.5 µm.
Extrolites: Citrinin, citreomontanin (Rebuffat et al. 1980),
citreoviridin A (Nagel et al. 1972, Rebuffat et al. 1984, Frisvad &
Filtenborg 1990), citreoviridinol A1 and A2 (Rebuffat et al. 1984),
epicitreoviridinol (Lai et al. 1990), phoenicin, “MIF”, ”MIM”.
Phoenicin was not detected in CBS 235.31, CBS 263.29, CBS
378.65 and CBS 126233, but all other 20 strains of P. manginii
examined produced this compound. This compound contributes
to the red colour of the diffusible pigment of P. manginii, but the
species also produces some red anthraquinone secondary
metabolites. Citrinin was produced by CBS 235.31, CBS 265.65,
CBS 263.29, CBS 408.65, CBS 409.65, CBS 122403, CBS 126232
and seven additional strains. Citreoviridin was produced by all
strains examined. CBS 126233 shares extrolites with other strains
of P. manginii, but is unique in producing decaturins and alavinintype apolar sclerotial indolterpenes.
Diagnostic characters: Yellow mycelium (citreoviridins) (CYA15°C),
fast growth rate on YES with red soluble pigments, light brown or
orange brown sclerotia.
Similar species: The production of yellow mycelium is shared
with P. vancouverense, but P. manginii grows faster, produces red
soluble pigment and can have inely rough walled stipes.
Distribution and ecology: Worldwide. Isolated from soil in Norway,
Congo, Madagascar and UK; air in the Netherlands and Spain,
mycorrhizae of Fagus sylvatica, Italy and rhizosphere of Triticum
aestivum, UK.
Barcode & molecular based ID: GenBank no. GU944599. The
ITS region of the majority of the analysed P. manginii isolates
were invariable. Isolate CBS 327.79 was an exception and had
37 bp deletion in the ITS1 region. This deletion in also observed
in P. citrinum and P. hetheringtonii, but not in other strains of the
P. westlingii-clade. Phylogenetic analysis of partial β-tubulin and
calmodulin data shows that isolates CBS 378.65, CBS 108.66 and
CBS 126233 are deviating from the majority of the analysed P.
manginii isolates and each strain has a unique sequence. However,
these three strains have similar ITS sequences (0, 1 and 4 bp
difference, respectively) as the type of P. manginii, CBS 253.31T.
Taxonomy and phylogeny: Penicillium manginii was placed in
synonymy with P. miczynskii by Raper & Thom (1949), Pitt (1980)
and Ramírez (1982), but this was not followed by Stolk & Samson
(1983), who maintained it as a separate species on the basis of
conidiophore ornamentation and conidial shape. Molecular data
supports the conclusions of Stolk & Samson (1983). Penicillium
pedemontanum is synonymised with P. manginii. The type of P.
pedemontanum (CBS 265.65T) once produced large light brown
sclerotia, but the culture maintained at CBS has lost this ability.
www.studiesinmycology.org
Molecular data shows variation among the analysed P. manginii
isolates and this species is probably a complex. Of all P. manginii
strains analysed, CBS 378.65 was the only strain with a CYAS:CYA
ratio lower than 1 (0.85). CBS 126233 produced decaturins and
alavinin-type apolar sclerotial indolterpenes and did not produce
red soluble pigments. However, this latter feature was also observed
in some other P. manginii strains. These strains might represent
new species, but we wait with the description until more strains are
collected and investigated. Several strains originally identiied as P.
pulvillorum (Nagel et al. 1972) proved to be P. manginii (CSIR 1405,
CSIR 1406, IMI 059911, IMI 089983, IMI 096225, IMI 096290 and
IMI 099085). Comparison of deposited calmodulin sequences of
NRRL 29865 (AY443481) and NRRL 29736 (AY443483) suggests
that these strains are closely related to P. manginii and might
represent a new species.
Penicillium miczynskii Zaleski, Bull. Int. Acad. pol. Sci.
Lett., Sér. B.: 482. 1927. Fig. 27.
Typus: ex soil under conifer, Tatry mountains, Poland (IMI 40030 –
lectotype, Pitt 1980; cultures ex-type CBS 220.28 = ATCC 10470 =
DSM 2437 = FRR 1077 = IFO 7730 = IMI 040030 = MUCL 29228 =
NRRL 1077 = QM 1957 = IBT 5491)
Description: Colony diam, 7 d, in mm: CYA 21–27; CYA15°C
15–23; CYA30°C and CYA37°C: no growth; MEA 17–25 mm; YES
26–33 mm; DG18 18–25; ratio CYAS:CYA 0.85–1.0; creatine agar
9–13 mm, weak growth and no acid production.
Degree of sporulation on CYA generally poor, occasionally good
sporulation (CBS 126223), velvety, conidia grey green, mycelium
white or light yellow, exudate absent or sparsely produced as
small clear droplets, soluble pigments absent and in some strains
yellow, margin of most isolates polygonal, occasionally entire,
reverse beige to beige brown in the majority of strains, occasionally
yellow-orange (CBS 126222). No or weak sporulation on YES,
soluble pigments absent (except CBS 126223, which has strong
sporulation and yellow soluble pigments), reverse yellow-orange or
yellow-brown. Moderate to good sporulation on DG18, conidia grey
green, reverse (bright) yellow. Sporulation on MEA variable, conidia
grey green, colony texture velvety to slightly loccose. No reaction
with Ehrlich test; with exception of CBS 126222.
Sclerotia produced on oatmeal agar under large, clear exudate
droplets and a thin layer of conidiophores. Sclerotia pale orange
becoming orange-brown in age, 125–250 (–300 µm), soft when
young becoming hard with age, consisting of polygonal cells,
red-brown pigmented spots often present on the surface. Asci
and ascospores not observed. Conidiophores predominantly
symmetrical biverticillate with occasionally an additional branch,
stipes 200–400 µm long, smooth walled, 2.5–4.0 µm wide; metulae
in terminal whorls of 3–6 (–8) and often uneven in length, 10–12
× 2.5–4.0 µm; phialides ampulliform, 7–9 × 2.0–3.0 µm. Conidia
subglobose to broadly ellipsoidal, smooth, 2.0–3.0 × 2.0–2.5 µm.
Extrolites: Citreoviridin, cyclopiazonic acid, quinolactacin, terrein,
“met OE”, “MIF”, “TERRIT”, “XANTHOC”.
Diagnostic characters: Colonies on CYA 21–27 mm; no growth on
CYA30, ratio CYAS:CYA 0.85–1.0, orange-brown sclerotia.
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Houbraken et al.
Fig. 27. Penicillium miczynskii. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–C. Sclerotia. D–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
Similar species: This species is phylogenetically related to P.
cairnsense, P. aurantiacobrunneum, P. neomiczynskii and P.
quebecense. Penicillium miczynskii deviates from P. cairnsense
and P. quebecense in having smaller colony diameters on
YES, MEA and CYA and does not grow at 30 °C. In addition, P.
cairnsense and P. quebecense often produce red soluble pigments
and have many exudate droplets on CYA. The ratio CYAS:CYA of
P. miczynskii is lower than 1 and this character can be used to
distinguish P. miczynskii from the morphologically similar species P.
aurantiacobrunneum and P. neomiczynskii.
3.5 µm wide. Metulae in a terminal whorl of 3–6 metulae, often
unequal in length, 10–13 × 2.5–3.5 µm. Phialides ampulliform, 7–9
× 2.5–3.0 µm. Conidia subglobose to broadly ellipsoidal, smooth,
2.0–3.0 × 2.0–2.5 µm, larger conidia also present, globose, 3.0–3.5
µm diam.
Distribution and ecology: Worldwide, commonly occurring in soil.
Similar species: Penicillium neomiczynskii resembles P. miczynskii
and P. aurantiacobrunneum. It differs from P. aurantiacobrunneum
in its negative Ehrlich reaction and can be differentiated from P.
miczynskii by its CYAS:CYA ratio of 1.1–1.2.
Barcode & molecular based ID: GenBank no. GU944600.
Penicillium miczynksii and P. aurantiacobrunneum share the same
ITS sequence. These species can be distinguished by partial
β-tubulin and/or calmodulin sequences.
Taxonomy and phylogeny: Penicillium miczynskii was described by
Zaleski (1927) and the taxonomy of this species was considered
in various taxonomic studies (Raper & Thom 1949, Pitt 1980,
Ramírez 1982, Christensen et al. 1999). Thom (1930: 488)
placed this species in a miscellaneous group after his section
Biverticillata-Symmetica, while Raper & Thom (1949) included it
in the P. janthinellum series. Subsequently, Pitt (1980) placed this
species in the series Citrina and broadened the species concept
to include sclerotigenic strains. The ex-type culture CBS 220.28
does not produce sclerotia, but most recently isolated strains
do. This feature appears to be quite common for P. miczynskii
isolates and other phylogenetically related species. Although Pitt
(1980) synonymised P. chrzaszczii, P. soppii, P. matris-meae, P.
manginii, P. pedemontanum, P. atrosanguineum and P. syriacum
with P. miczynskii, our study shows that none of these species are
conspeciic with P. miczynskii.
Penicillium neomiczynskii AJL Cole, Houbraken, Frisvad &
Samson, sp. nov. MycoBank MB563192. Fig. 28.
Etymology: This species is closely related to P. miczynskii.
Differt ab omnibus speciebus afinibus ratione CYAS:CYA 1.1–1.2, coloniis in agaro
CYA ad 30 °C haud crescentibus, coloniis in agaro MEA 12–18 mm.
Typus: ex soil, New Zealand, T. Cole (CBS H-20661 – holotypus,
cultures ex-type CBS 126231 = DTO 78C2 = IBT 23560).
Description: Colony diam, 7 d, in mm: CYA 21–27; CYA30°C no
growth; CYA37°C: no growth; MEA 12–18 mm; YES 25–31 mm;
DG18 16–22; ratio CYAS:CYA 1.1–1.2; creatine agar 9–13 mm,
weak growth and no acid production.
Good sporulation on CYA, velvety to loccose, conidia grey-blue
green, mycelium inconspicuous, exudate in minute clear droplets,
soluble pigments yellow-brown, margin irregular, reverse yellowish
brown. Good sporulation on YES, conidia grey green, soluble
pigments absent, reverse yellow-beige. Good sporulation on DG18,
conidia dull green, mycelium inconspicuous, reverse pale. Good
sporulation on MEA, conidia dull green, colony texture velvety.
Ehrlich reaction negative.
Sclerotia absent. Conidiophores 200–400 µm long, both
symmetrically biverticillate and terverticillate, stipes smooth, 2.5–
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Extrolites: Citreoviridin, terrein, “MIF”, “OFSO”.
Diagnostic characters: CYAS:CYA ratio 1.1–1.2, no growth on
CYA30°C, colonies on MEA 12–18 mm.
Distribution and ecology: Penicillium neomiczynskii is only known
from its type culture, which was isolated from soil from New
Zealand.
Barcode & molecular based ID: GenBank no. JN617671. The
sequences of the ITS regions of P. neomiczynskii are identical to
those of the type of P. cairnsense (CBS 124325T) and P. quebecense
(CBS 101623T). Partial β-tubulin and calmodulin sequences can be
used for identiication of this species.
Taxonomy and phylogeny: This species is phylogenetically and
morphologically related to P. miczynskii and P. aurantiacobrunneum.
Penicillium nothofagi Houbraken, Frisvad & Samson, sp.
nov. MycoBank MB563189. Fig. 29.
Etymology: Isolated from soil under Nothofagus sp.
Differt ab omnibus speciebus afinibus coloniis in agaro CYA, MEA et YES restricte
crescentibus, conidiis leniter vel distincte exasperates.
Typus: ex soil under Nothofagus sp., Chile (CBS H-20655 –
holotypus, cultures ex-type CBS 130383 = DTO 76C2 = IBT 23018).
Description: Colony diam, 7 d, in mm: CYA 5–10; CYA15°C 8–14;
CYA30°C and CYA37°C 0; MEA 4–8; YES 10–15; DG18 10–15;
ratio CYAS:CYA 2.0–3.0; creatine agar 3–6, weak growth and no
acid production.
Moderate sporulation on CYA, velvety, conidia dark green conidia,
mycelium inconspicuous, exudates absent, soluble pigment
absent, margin entire, reverse pale beige. Sporulation on YES
absent, mycelium white, soluble pigments absent, reverse beige.
Moderate sporulation on DG18, conidia dull green to grey green,
reverse pale to pale-cream. No sporulation on MEA after 7 d of
incubation, after 14 d moderate sporulation, conidia blue green,
colony texture velvety to granulose. Ehrlich reaction negative.
Sclerotia absent. Conidiophores mostly symmetrically biverticillate
and occasionally with an additional divergent branch; stipes variable
in length, 50–400 µm long, smooth, 2.0–3.0 µm wide; metulae in
a divergent terminal verticil, 2–4 (–7), unequal in length, with a
distinct vesicle, long compared to related species, 11–17 × 2.5–3.5
µm, additional branches up to 25 µm; phialides ampulliform, 7.5–
10 × 2.5–3.5 µm. Conidia globose to subglobose, inely to distinct
roughened, 2.5–3.5 µm diam.
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Houbraken et al.
Fig. 28. Penicillium neomiczynskii. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
Fig. 29. Penicillium nothofagi. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse, CREA
obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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107
Houbraken et al.
Extrolites: Citrinin, “CURVU”, “SENTRIP”, “SKAEM”.
Diagnostic characters: Restricted growth on CYA, MEA and YES,
inely to distinct rough walled conidia.
Similar species: This species is phylogenetically related to P.
westlingii and P. cosmopolitanum. It differs from those species
by a slower growth rate on the CYA, YES and MEA. Penicillium
wellingtonense is phenotypically similar, but produces has an
orange coloured reverse on CYA and subglobose to broadly
ellipsoidal conidia.
Distribution and ecology: Soil under Nothofagus sp. in Chile and
soil, Brazil.
Barcode & molecular based ID: GenBank no. JN617712. CBS
130383T shares ITS sequences with P. godlewskii and with P.
cosmopolitanum strains belonging to subclade 4 (Fig. 3).
Taxonomy and phylogeny: Phylogenetically related to P. westlingii
and P. cosmopolitanum.
Penicillium pancosmium Houbraken, Frisvad & Samson,
sp. nov. MycoBank MB563191. Fig. 30.
Etymology: Referring to the worldwide distribution of this species.
Differt ab omnibus speciebus afinibus conidiis subtiliter exasperatis, coloniis ad
30 °C haud crescentibus, ad 28–35 mm diam post hebdomatem, reverso lavoaurantiaco vel aurantiaco in agaro YES.
Typus: ex old Armillaria mellea, on hardwood log; Meach Lake,
Gatineau Park, Gatineau County, Quebec, Canada (CBS H-20651
– holotypus, cultures ex-type CBS 276.75 = DTO 31B4 = DAOM
147467 = IBT 29991).
Description: Colony diam, 7 d, in mm: CYA (23–) 28–35; CYA15°C
15–21; CYA30°C 0 or germination; CYA37°C no growth; MEA
(20–)25–31; YES (26–) 30–40; DG18 (16–) 22–30; ratio CYAS:CYA
0.9–1.1; creatine agar 15–20, weak growth and no acid production.
Good sporulation on CYA, velvety or loccose, conidia dull-green or
grey-green, mycelium inconspicuous, exudate absent or sparsely
present as minute clear droplets, soluble pigments absent in most
isolates, except CBS 118007, which produces light red pigments,
margin entire or polygonal, reverse pale, light beige or pinkish beige
(towards skin colour), often with orange pigments in sulcations.
Sporulation on YES variable, absent to strong, mycelium white,
soluble pigments absent or yellow, reverse yellow-orange or orange.
Variable sporulation on DG18, condia dull green, reverse pale or
cream. Good sporulation on MEA, conidia blue-green or blueish-grey
green, colony texture loccose. Ehrlich reaction negative.
Sclerotia absent. Conidiophores symmetrically biverticillate, often
with an divergent branch that is shorter than the main axis; stipes
long, up to 500 µm, smooth, 2.5–4.0 µm; metulae in a compact
terminal verticil, 4–6 (–8), unequal in length, vesiculate, 9–13
(–15) × 2.0–3.5 µm; phialides ampulliform, broad, 6.5–9 × 2–3
µm. Conidia globose to subglobose, inely roughened, 2.0–3.0 µm
diam, except CBS 126432, which has inely roughened ellipsoidal
conidia, 2.5–3.0 × 1.8–2.5 µm.
108
Extrolites: Citrinin, daldinin D, decaturin, terrein, “MELI”, “ORAN”,
“SENGA”, “XANTHOC”.
Diagnostic characters: Finely roughened conidia, no growth at 30
°C, colonies attaining a diameter of 28–35 mm in 7 d at 25 °C,
reverse on YES yellow-orange or orange.
Similar species: Penicillium pancosmium is phylogenetically
related to P. ubiquetum. The species are phenotypically similar, but
the latter has an orange-red reverse on YES and dark-dull green
conidia on CYA, while P. pancosmium forms a yellow-orange or
orange reverse on YES and has dull green or grey green conidia
on CYA. Futhermore, P. pancosmium tends to grow faster on
MEA than P. ubiquetum. Penicillium chrzaszczii produces yellow
reverse on DG18 and sporulation on CYA is absent or poor, while P.
pancosmium and P. ubiquetum isolates sporulate well on CYA and
have a pale (or very pale yellow) reverse on DG18.
Distribution and ecology: Isolated from soil, old Armillaria mellea on
a hardwood log, Piptoporus (on Betula sp), nut of Juglans cinerea
(butternut) and porcupine dung. This species has a worldwide
distribution and was isolated in Tunisia, Canada (Ontario and
Quebec) and USA (New Jersey).
Barcode & molecular based ID: GenBank no. JN617660. This
species has unique ITS, β-tubulin and calmodulin sequences.
Taxonomy and phylogeny: Based on partial β-tubulin and calmodulin
data, CBS 118007 and CBS 126431 are phylogenetically closely
related, but distinct from CBS 276.75T. These isolates differ from
the other P. pancosmium strains in having smaller colonies and
a pinkish-brown reverse on CYA. CBS 126432 differs in having
ellipsoidal conidia and a different β-tubulin, calmodulin and ITS
sequence than CBS 276.75T. It needs to be noted that the variation
within P. pancosmium is large, and it could be that this species
represents a complex.
Penicillium pasqualense Houbraken, Frisvad & Samson,
sp. nov. MycoBank MB563190. Fig. 31.
Etymology: Referring to Easter Island, the locality of the type strain.
Differt ab omnibus speciebus afinibus (sect. Citrina) coloniis in agaro CYA30
crescentibus, reverse atro-brunneo in agaro CYA, conidiis leviter majoribus.
Typus: ex soil, Easter Island, Chile (CBS H-20663 – holotypus,
cultures ex-type CBS 126330 = DTO 80D5 = IBT 14235).
Description: Colony diam, 7 d, in mm: CYA 25–35; CYA15°C 15–
20; CYA30°C 5–15; CYA37°C 0; MEA (15–) 25–30; YES 25–35;
DG18 17–25; ratio CYAS:CYA 0.75–0.95; creatine agar 13–18,
varying from weak (CBS 122402 & CBS 126330) to moderate (CBS
124327) growth, no or weak acid production.
Good sporulation on CYA (except CBS 126329), velvety, conidia
dull dark green, mycelium inconspicuous, exudate produced
in both small and large droplets, which are clear or pale yellow
coloured, soluble pigment absent, margin entire, reverse dark
brown or blackish brown. Weak to moderate sporulation on YES,
conidia dull green, soluble pigments absent, reverse beige-brown
or brown. Good sporulation on DG18, conidia dull-green, reverse
pale with a cream centre. Good sporulation on MEA, conidia
taxonoMy of Penicillium Section citrina
Fig. 30. Penicillium pancosmium. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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109
Houbraken et al.
Fig. 31. Penicillium pasqualense. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–D. Sclerotia. E–G. Conidiophores. H. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
dark green or dark-blue green, colony texture velvety to loccose,
reverse medium-brown. Ehrlich reaction negative.
Sclerotia orange brown or brown, hard, consisting of hyaline
polygonal cells with very thick walls, red-brown mycelium strands
present present on the sclerotium. Asci and ascospores not
observed. Conidiophores predominantly symmetrically biverticillate
and often additional branches occur which are equal in length
as the main axis and also consist of symmetrically biverticillate
structures (“double symmetrically biverticillate”); stipes rather long,
200–400 µm, smooth, 2.5–3.0 µm wide; metulae in a divergent
terminal vertical, 2–4, unequal in length, longer than in related
species, 11–17 × 2.5–3.5 µm, branches longer up to 25 µm;
phialides ampulliform, 7.5–10 × 2.5–3.5 µm. Conidia globose to
subglobose, spinose, 2.5–3.5 µm diam.
Extrolites: Pyrenocines, indol alkaloids, “PAS”.
Diagnostic characters: Growth on CYA30, dark brown reverse on
CYA, orange brown or brown sclerotia, dark blue green spinose
conidia on MEA, slightly larger conidia than most other members
of section Citrina.
Similar species: The formation of orange-brown sclerotia indicates
a relationship with P. miczynskii and related species, but P.
pasqualense is less colourful, has a dark brown reverse on CYA
and forms typical dark blue green, spinose conidia on MEA.
Distribution and ecology: This species was isolated from various
soils and indoor air of a bakery. World-wide distribution: Easter
Island, Chile, NSW, Australia, the Netherlands and Wyoming, USA.
Barcode & molecular based ID: GenBank no. JN617676. Penicillium
pasqualense can be identiied using ITS, partial β-tubulin and
calmodulin sequences.
green or dull-blue green, mycelium white, soluble pigments absent,
reverse (pale) crème or pale yellow. Strong sporulation on DG18,
conidia dull green, reverse commonly pale, occasionally pale with
pale yellow centre. Strong sporulation on MEA, conidia dull green,
also dull green and blue green, colony texture loccose. Ehrlich
reaction negative.
Extrolites: Paxillin, dehydroxypaxillin, 1’-O-acetylpaxillin (Frisvad
& Filtenborg 1990), meleagrin, pyrenocines, “PU”, “PUX”, “TOTO”.
The paxillin biosynthetic pathway of P. paxilli (ATCC 26601 = CBS
547.77) was intensively studied (e.g. Young et al. 2001, McMillan
et al. 2003).
Diagnostic characters: Rough walled stipes, predominantly
biverticillate with appressed terminal whorl of 4–8 metulae, good
growth on CYA incubated at 30 °C and good growth on DG18.
Similar species: Penicillium paxilli can be distinguished from P.
citrinum by its inability to grow at 37 °C; from P. sumatrense and P.
hetheringtonii by its pale reverse on CYA, and from P. steckii by its
rough walled stipes.
Distribution and ecology: This species has a worldwide distribution
and has a preference for (sub)tropic regions. Penicillium paxilli was
isolated from various substrates, such as soil, wood in a tropical
rainforest, the surface of a melon, mangrove, leaves, nut of Carya
cordiformis (bitternut), termite mounds, Garcinia sp. (Rungjindamai
et al. 2006) and as an endophyte of wild rubber trees (Hevea
brasiliensis) (Gazis & Chaverri 2010).
Barcode & molecular based ID: GenBank no. GU944577. This
species can be identiied with ITS and partial β-tubulin and
calmodulin sequences.
Taxonomy and phylogeny: Analysis of partial β-tubulin and
calmodulin sequences shows variation among various isolates of P.
paxilli and this species might be a complex. A thorough population
study is needed to clarify the taxonomy of this species.
Taxonomy and phylogeny: Phylogenetic analysis of partial
β-tubulin and calmodulin data shows that this species is related
to P. vancouverense and P. wellingtonense (99 % bs), but can
differentiated by various phenotypic characters, such as growth at
30 °C, spinose conidia and sclerotium formation. The divergent long
metulae and branching pattern of this species supericially resemble
some species related to P. simplicissimum and P. janthinellum. It
shares the production of of pyrenocines with P. paxilli.
Penicillium quebecense Seifert, Houbraken, Frisvad &
Samson, sp. nov. MycoBank MB563202. Fig. 33.
Penicillium paxilli Banier, Bull. trimest. Soc. mycol. Fr. 23:
95. 1907. Fig. 32.
Differt ab omnibus speciebus afinibus reverso atro-rubro coloniae in agaro YES,
coloniis in agaro CYA usque ad 38–42 mm et in agaro CYA30 16–20 mm, ratione
CYAS:CYA 0.85–1.0, sclerotiis pallide aurantiacis efferentibus.
Typus: ex optical instrument, Barro Colorado Island, Panama (IMI
40226 – neotype, Pitt 1980; cultures ex-type CBS 360.48 = DTO 31A6
= ATCC 10480 = FRR 2008 = NRRL 2008 = QM 725 = IBT 16202).
Typus: ex air in sawmill, Quebec, Canada (CBS H-20666 –
holotypus, cultures ex-type CBS 101623 = DTO 9B8 = IBT 29050).
Description: Colony diam, 7 d, in mm: CYA 30–37; CYA15°C 10–
20; CYA30°C (9–) 18–25; CYA37°C no growth; MEA 28–35; YES
38–46; DG18 (25–) 30–37; ratio CYAS:CYA 1.0–1.3; creatine agar
11–20, weak growth and no acid production.
Good sporulation on CYA, velvety, conidia dull green or dull-blue
green, mycelium white, exudate droplets clear, occasionally absent,
soluble pigments absent, margin slightly polygonal, reverse pale or
pale with pale beige centre. Strong sporulation on YES, conidia dull
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Etymology: Named after the location where the type strain was
isolated, Quebec (Canada).
Description: Colony diam, 7 d, in mm: CYA 38–42; CYA30°C 16–
20; CYA37°C: no growth; MEA 30–35 mm; YES 42–48 mm; DG18
24–29; ratio CYAS:CYA 0.85–1.0; creatine agar 17–24 mm, weak
growth and no acid production.
Good sporulation on CYA, velvety, conidia dull grey green, many minute
clear exudate droplets, soluble pigments yellow, margin entire, reverse
yellow, yellow-orange in the centre. Good sporulation on YES, conidia
dull green, soluble pigments red, reverse deep dark red in center with
brown edge. Good sporulation on DG18, conidia grey green, reverse
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Houbraken et al.
Fig. 32. Penicillium paxilli. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse, CREA
obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
Fig. 33. Penicillium quebecense. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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Houbraken et al.
pale. Moderate to good sporulation on MEA, conidia grey green, colony
texture velvety. Ehrlich reaction negative.
Sclerotia absent. Conidiophores predominantly symmetrically
biverticillate and occasionally with additional branch; stipes up
to 300–500 µm long, smooth or inely rough walled, 2.0–3.0 µm
wide; metulae in compact terminal whorls of 4–8 (–10), equal in
length, non-vesiculate, 10–14 × 2.0–3.5 µm. Phialides ampulliform,
7–9 × 2.0–3.0 µm. Conidia smooth or inely rough walled, broadly
ellipsoidal, 1.8–2.5 × 2.0–2.5 µm.
Sclerotia white when young, becoming pale orange in age,
150–250 µm, inconspicuously, produced on oatmeal agar under
a dense layer of conidiophores, hard, consisting of polygonal
cells; no asci or ascospores observed. Conidiophores 200–400
µm long, predominantly biverticillate, rarely terverticillate,
stipes smooth, 2.5–3.5 µm wide. Metulae, in terminal whorl
of 3–7, mostly equal in length, 10–14 x 2.5–3.5 µm. Phialides
ampulliform, 7–9 × 2–3 µm. Conidia subglobose, smooth, 2.0–
2.5 × 2.0–3.0 µm diam.
Extrolites: CBS 126234T produces citrinin, “FON”, “MIF”,”KUM”,
“LOST”,“PHOE”, and “TRIP”; CBS 126235, possibly a P. raphiae,
produces citrinin, quinolactacin,”FON”, “MIF”, “KUM”, “MIM”,
“REJS”, “SENGA”, and “XANTHOC”.
Extrolites: Citreoviridin, phoenicin, terrein, “SENOE” (verrucofortinetype molecule), “MIF”, “MIM”, “SENGA”, “alk-770”.
Diagnostic characters: No growth on CYA30, broadly ellipsoidal
conidia, predominantly symmetrically biverticillate conidiophores.
Diagnostic characters: Dark red reverse on YES, colonies on CYA
38–42 mm, colonies on CYA30 16–20 mm, ratio CYAS:CYA 0.85–
1.0, pale orange sclerotia.
Similar species: The species is phenotypically related to P. steckii,
P. copticola and P. terrigenum. Penicillium raphiae does not grow at
30 °C, while the other related species do grow at this temperature.
Similar species: Penicillium quebecense morphologically
resembles P. cairnsense, but differs in a higher growth rate at
CYA30°C. Additional strains should be compared to determine if
this character is consistent among multiple strains.
Distribution and ecology: This species is only known from its type
strain, which was isolated from soil in a primary forest under Raphia
palm in Costa Rica.
Distribution and ecology: This species is only known from its type
culture, isolated from the air in a sawmill in Quebec, Canada.
Barcode & molecular based ID: GenBank no. JN617661. The ITS
regions of P. quebecense are identical to those of the type of P.
cairnsense (CBS 124325T) and P. neomiczynskii (CBS 126231T).
Partial β-tubulin and calmodulin sequences can be used for the
identiication of this species.
Taxonomy and phylogeny: None.
Penicillium raphiae Houbraken, Frisvad & Samson, sp.
nov. MycoBank MB563203. Fig. 34.
Etymology: This species was isolated from soil under Raphia palm.
Differt ab omnibus speciebus afinibus coloniis in agaro CYA30 haud crescentibus,
conidiis late ellipsoideis, conidiophoris saepe symmetrice biverticillatis.
Typus: ex soil under Raphia palm in primary forest, Las Alturas,
Costa Rica (CBS H-20660 – holotypus, cultures ex-type CBS
126234 = DTO 78B8 = IBT 22407).
Description: Colony diam, 7 d, in mm: CYA 32–36; CYA15°C 18–
22; CYA30°C and CYA37°C no growth; MEA 21–25; YES 31–35;
DG18 23–27; ratio CYAS:CYA 1.0–1.2; creatine agar 10–15, weak
growth and no acid production.
Good sporulation on CYA, velvety, conidia blue-green, mycelium
inconspicuous, exudate absent, soluble pigments absent, margin
slightly irregular or polygonal, reverse creme to light-brown. Good
sporulation on YES, conidia grey green, soluble pigments absent,
reverse (light-) brown. Good sporulation on DG18, conidia light
blue green or dull green, reverse cream or light yellow. Moderate to
good sporulation on MEA, conidia light-blue green, colony texture
velvety. Ehrlich test negative.
114
Barcode & molecular based ID: GenBank no. JN617673. This
species has unique ITS, partial β-tubulin and calmodulin sequences.
Taxonomy and phylogeny: This species is phylogenetically unique
in the P. westlingii-clade. Sequence and extrolite data indicate that
CBS 126235 is a new species. However, CBS 126234T and CBS
126235 are phenotypically similar and we wait with the description
of this species until more strains are collected and studied.
Penicillium roseopurpureum Dierckx, Annls Soc. Scient.
Brux. 25: 86. 1901. Fig. 35.
= Penicillium carminoviolaceum Dierckx Annls Soc. Scient. Brux. 25: 86. 1901.
= Citromyces cesiae Bainier & Sartory, Bull. Trimest. Soc. Mycol. Fr. 29:148.
1913.
= Penicillium cesiae (Bainier & Sartory) Biourge, La Cellule 33: 101. 1923.
Typus: unrecorded source (IMI 40573 – neotype, cultures ex-type
CBS 266.29 = DTO 9E3 = ATCC 10492 = ATHUM 2895 = FRR
2064 = IMI 040573 = MUCL 28654 = MUCL 29237 = NRRL 2064
= NRRL 2064A).
Description: Colony diam, 7 d, in mm: CYA 7–16; CYA15°C 7–13;
CYA30°C and CYA37°C no growth; MEA 9–19; YES 12–18; DG18
14–22; ratio CYAS:CYA 1.2–1.9; creatine agar 3–6, weak growth
and no acid production.
Sporulation absent or sparse on CYA and becoming velvety in
time, with pale grey green conidia, mycelium white or pale yellow,
exudate absent or sparsely present as dark red brown droplets,
soluble pigments orange, reverse red brown or orange brown,
margin varying form entire to irregular, reverse in shades of brown
(red-brown, caramel or yellow-brown). Sporulation on YES variable
or poor, mycelium white or pale yellow, soluble pigments absent or
yellow-brown, reverse yellow with red-brown centre, orange-red or
yellow. No sporulation on DG18, white mycelium, reverse yelloworange, vivid yellow or pale yellow. Sporulation on MEA sparsely,
becoming grey-green in time, colony texture velvety or loccose.
Ehrlich reaction negative.
taxonoMy of Penicillium Section citrina
Fig. 34. Penicillium raphiae. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse, CREA
obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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115
Houbraken et al.
Fig. 35. Penicillium roseopurpureum. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
116
taxonoMy of Penicillium Section citrina
Sclerotia absent. Conidiophores monoverticillate when young,
becoming irregularly branched with divergent lower branchlike metulae or symmetrically biverticillate in age; length of stipe
of main conidiophore 50–150 µm, lower branch-like metulae
shorter, smooth, 2.0–3.0 µm wide; metulae branch-like, irregularly
formed and in some cases dificult to distinguish from stipes,
when produces terminally, then unequal in length, often gradually
enlarging at the apex, giving a clavate appearance or distinct
vesiculate, 15–25 × 2.0–3.5 µm at base, terminal up to 5.0 µm
diam; phialides ampulliform, formed terminally and subterminally,
6.0–8.0 × 2–3 µm. Conidia globose to subglobose, smooth or very
inely roughened, 1.8–2.5 µm diam.
Extrolites: Bisanthrons, roseopurpurin, sorbicillins (produced
by some isolates), “AQ” (other anthraquinones apart from
roseopurpurin), “SEL”.
Diagnostic characters: Monoverticillate or furcate conidiophores
with lower branch-like metulae, reverse on CYA in shades of red,
often with red-brown diffusible pigments, restricted growth on agar
media and no growth on CYA30°C.
Similar species: Penicillium sanguiluum is related to P.
roseopurpureum, but the latter grows slower on CYA and does not
grow on CYA incubated at 30 °C. Furthermore, P. roseopurpureum
has a higher CYAS:CYA ratio than P. sanguiluum.
Distribution and ecology: This species was isolated from soil
(Wyoming, USA) and indoor air (the Netherlands).
Barcode & molecular based ID: GenBank no. GU944605. This
species shares ITS sequences with most members of clade 1 of P.
sanguiluum (Fig. 4).
Taxonomy and phylogeny: Phylogenetic analysis shows that
P. roseopurpureum belongs to section Citrina. This species is
characterised by the formation of monoverticillate conidiophores,
becoming irregularly branched with divergent lower branch-like
metulae or symmetrically biverticillate condiophores in older parts
of the colony. This branching pattern is unusual for members of
section Citrina, which are in general symmetrically biverticillate.
Figure 4 shows that the type strain of P. carminoviolaceum (CBS
281.39) belongs to P. roseopurpureum. No cultures of P. cesiae
were available for analysis. Raper & Thom (1949) and Pitt (1980)
are followed here and this species is considered as a synonym of
P. roseopurpureum.
Penicillium sanguiluum (Sopp) Biourge, La Cellule 33:
105. 1923. Fig. 36.
Basionym: Citromyces sanguiluus Sopp, Skr. udgivne VidenskabsSelsk. Christiania 11: 115. 1912.
= Penicillium lacussarmientei Ramírez, Mycopathol. 96: 29. 1986.
= Penicillium vaccaeorum Quintanilla, Mycopathol. 80: 77. 1982.
Typus: ex soil, Calahonda, Costa del Sol, Spain, L. Janson (CBS
H-20645 – neotype, designated here; cultures ex-type CBS 127032
= DTO 20B7 = IBT 29041).
Description: Colony diam, 7 d, in mm: CYA (15–) 18–26; CYA15°C
7–14; CYA30°C microcolony–13; CYA37°C no growth; MEA 17–
26; YES 18–28; DG18 16–22; ratio CYAS:CYA 0.9–1.2; creatine
agar 5–14, weak growth and no or poor acid production.
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Sporulation on CYA variable, absent to moderate, velvety, conidia
grey-green, mycelium white or pale beige, exudate absent or dark
red brown, strong red soluble pigment production, margin entire or
irregular, reverse dark red brown or red. Sporulation on YES absent
or sparse, mycelium white, pale beige or pale yellow, soluble
pigments absent or orange, reverse orange, orange-brown with or
without orange-red centre. Sporulation absent or sparse on DG18,
conidia dull-green, reverse in shades or yellow (yellow-orange,
yellow or pale yellow). Colonies on MEA sporulating sparsely,
colony texture loccose. Ehrlich reaction negative.
Sclerotia not produced. Conidiophores produced on trailing
hyphe, monoverticillate, short, 15–50 µm, smooth, or with branchlike metulae scarcely formed, 1–3, unequal in length, strongly
vesiculate, (10–) 13–18 × 2.0–3.0 µm at base, vesicle up to 5
µm; phialides ampulliform, terminally and subterminally formed,
6.5–8 × 2–3 µm. Conidia globose to subglobose, smooth or inely
roughened, 2.0–2.5 µm diam.
Extrolites: Bisanthrons, roseopurpurin, β-hydroxycurvularin,
dehydrocurvularin, curvularin, “FOSI”, “FYKS”, “SNIT”, “TIDL”,
“VERN”.
Diagnostic characters: Monoverticillate conidiophores, dark red
brown reverse on CYA with red brown soluble pigment production,
growth on CYA30°C.
Similar species: See P. roseopurpureum.
Distribution and ecology: This species appears to have preference
for sandy soils and has a worldwide distribution. Penicillium
sanguiluum is isolated from soils in Spain, Manitoba, Canada, the
Netherlands, Turkey, Chile and Argentina.
Barcode & molecular based ID: GenBank no. JN617711 (clade
1) and JN617681 (clade 2). Two subclades are present in P.
sanguiluum (Fig. 4). CBS 127032T is positioned in clade 2 and
shares identical ITS sequences with other members of this clade.
Members of clade 1 share ITS sequences with P. roseopurpureum.
This clade also includes the type cultures of P. lacussarmientei and
P. vaccaeorum.
Taxonomy and phylogeny: Penicillium sanguiluum was considered
a synonym of P. roseopurpureum (Raper & Thom 1949, Pitt 1980).
Examination of the protologue of Citreomyces sanguiluus showed
that this species is not P. roseopurpureum (Sopp 1912: 115). It
has an optimal growth between 25 and 30 °C and the published
Figure (Sopp 1912: XXII, Fig. 3) shows rather well developed
colonies. These characters it better with P. sanguiluum than
with P. roseopurpureum. CBS 127032T approximates the orginal
description of P. sanguiluum and it is designated here as the
neotype of this species. This study shows that the faster growth
rate is a good feature for distinguishing P. roseopurpureum and
P. sanguiluum. Penicillium vaccaeorum and P. lacussarmientei
were considered synonyms of P. roseopurpureum by Frisvad et al.
(1990b). They noted that both species are fast growing variants
of P. roseopurpureum, and these species are treated here as
synonyms of P. sanguiluum. Penicillium sanguiluum and P.
roseopurpureum deviate from other members of section Citrina by
its monoverticillate or furcate conidiophores. Partial β-tubulin and
calmodulin sequences show that two subclades are present in P.
sanguiluum (Fig. 4). No phenotypic differences were observed
117
Houbraken et al.
Fig. 36. Penicillium sanguiluum. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
118
taxonoMy of Penicillium Section citrina
between these two clades, and therefore we did not describe them
as two distinct species.
Penicillium shearii Stolk & Scott, Persoonia 4: 396. 1967.
Fig. 37.
= Carpenteles asperum Shear, Mycologia 26: 107. 1934 (misapplied).
= Penicillium asperum (Shear) Raper & Thom Man. Penicillia: 263. 1949
(misapplied).
= Eupenicillium shearii Stolk & Scott, Persoonia 4: 396. 1967.
Typus: ex soil, Tela, Honduras (CBS 290.48 – holotypus, cultures
ex-type DTO 22F6 = IMI 39739 = ATCC 10410 = NRRL 715 = IFO
6088 = IBT 24588).
Description: Colony diam, 7 d, in mm: CYA 28–40; CYA15°C 6–10;
CYA30°C 22–36; CYA37°C (0–) 5–19; MEA 26–37; YES 25–37;
DG18 28–37; ratio CYAS:CYA (0.7–) 0.9–1.1; creatine agar 10–20,
weak growth, acid and base production absent.
Sporulation on CYA absent or sparse; cleistothecia abundantly
produced, dark grey coloured, mycelium inconspicuous, large clear
exudate droplets, soluble pigments absent, margin entire, reverse
(light) brown. Sporulation on YES absent or weak, cleistothecia
abundantly produced and dark-grey, mycelium white, soluble
pigments absent, reverse (pale) yellow-brown. Sporulation on
DG18 absent in fresh isolates or weakly produced in older cultures,
conidia grey green, mycelium white, reverse pale or pale yellow.
Sporulation on MEA absent or weak, not inluencing the colony
colour, cleistothecia abundantly produced and grey. Ehrlich
reaction negative.
Cleistothecia abundantly produced on CYA, MEA and YES, globose
or subglobose, up to 500 µm diam, consisting of sclerotioid masses of
polygonal cells, ripening after 4–5 wk or more. Ascospores ellipsoidal,
2.5–3.5 × 2.0–2.5 µm, with 2 appressed equatorial ridges up to
0.5 µm wide, valves roughened (towards warted). Conidiophores
biverticillate, occasionally with additional branch, stipes 100–500
µm long, smooth walled or nearly so, 2.0–3.0 µm wide. Metulae
in verticils of 2–5 (–8), unequal in length, 10–14 × 2.0–3.0 µm.
Phialides ampulliform, 7.0–9.0 × 2–3 µm. Conidia subglobose or
broadly ellipsoidal, smooth or nearly so, 2.5–3.0 × 1.8–2.5 µm.
Extrolites: Paxillin, paspalinine, shearinin A & B, “XX” and several
indole alkaloids (Belofsky et al. 1995, Tuthill & Frisvad 2004).
Diagnostic characters: Abundant production of dark grey coloured
cleistothecia, growth at 37 °C, ascospores produced after
prolonged incubation.
Similar species: Penicillium tropicum and P. tropicoides are
phenotypically similar species; however, these two species do not
grow on CYA at 37 °C. Penicillium shearii can be differentiated from
P. euglaucum and P. anatolicum by the absence of yellow soluble
pigments and from P. argentinense by its ability to grow at 37 °C.
Distribution and ecology: Penicillium shearii has a worldwide
distribution and has a preference for tropical and subtropical
soils (Honduras, Colombia, Mexico, Congo, Papua-New Guinea,
Tanzania, Malaysia; Tuthill & Frisvad (2004) also isolated this
species in Venezuela, Ivory Coast, Australia, Costa Rica and
India).
www.studiesinmycology.org
Barcode & molecular based ID: GenBank no. GU944606.
This species can be identiied with ITS, partial β-tubulin and/or
calmodulin sequences.
Taxonomy and phylogeny: According to Shear (1934), the type
strain of P. shearii (CBS 290.48) represented Brefeld’s ascosporic
species “Penicillium glaucum Link”. He proposed Carpenteles
asperum as a new name for Brefeld’s fungus. However, CBS
290.48 does not produce asci in chains, as described and igured
by Brefeld (1874), and consequently C. asperum Shear as well as
the combination P. asperum (Shear) Raper & Thom are interpreted
as misapplied names. That Shear’s fungus differs from Brefeld’s
is nomenclaturally irrelevant because Shear clearly regarded
Brefeld’s organism to be the type for his new name. Stolk & Scott
(1967) proposed the name Eupenicillium shearii for Shear’s fungus
and named the anamorph P. shearii.
Stolk & Samson (1983) described P. soppii as the anamorph of
E. shearii (= P. shearii) and as a consequence P. shearii was
synonymised with P. soppii. However, molecular data shows that P.
soppii is distinct (Fig. 1) and phylogenetically unrelated to P. shearii.
Furthermore, P. soppii does not grow at 37 °C and no ascospores
or asci are produced in the sclerotia of this species.
Penicillium sizovae Baghdadi, Nov. sist. Niz. Rast., 1968:
103. 1968. Fig. 38.
Typus: ex soil, Syria (CBS 413.69 – neotype, designated by Pitt et
al. 2000; cultures ex-type DTO 23A7 = FRR 518 = IMI 140344 =
VKM F-1073).
Description: Colony diam, 7 d, in mm: CYA 28–39; CYA15°C
8–15; CYA30°C 28–34; CYA37°C 0–4; MEA 27–35; YES 40–50;
DG18 23–32; ratio CYAS:CYA 0.95–1.2; creatine agar 15–23, poor
growth, weak acid production.
Good sporulation on CYA, velvety, conidia grey green, mycelium
inconspicuous, small clear exudate droplets, soluble pigments
absent, margin entire, reverse pale and occasionally pale crèmebrown. Moderate to good sporulation on YES, conidia dark green,
soluble pigments absent, reverse pale or pale yellow-crème. Most
isolates moderate to good sporulation on DG18, occasionally absent
or poor, conidia dull green or grey green, reverse pale and conidial
colour shining through the agar. Good sporulation on MEA, conidia
grey green, colony texture loccose. No reaction with Ehrlich reagent.
Sclerotia absent. Conidiophores from aerial hyphae and the mycelial
mat, predominantly symmetrically biverticillate, occasionally with
an additional branch; stipes smooth, 100–300 × 2.5–3.2 µm.
Metulae in whorls of 2–5, 11–16 × 2.5–3.2 µm, uniform in length.
Phialides ampulliform, 7.0–9.5 × 2.0–3.0 µm. Conidia globose to
subglobose, inely roughened, 2.0–2.5 µm diam.
Extrolites: Quinolactacin, tanzawaic acid E, verrucolone, “AFSI”,
“CHAE and “PNUF” (Houbraken et al. 2010).
Diagnostic characters: Fast growing on MEA and YES, pale reverse
on CYA, inely roughened conidia.
Similar species: Penicillium sizovae is phylogenetically related
to P. citrinum, P. hetheringtonii, P. steckii and P. gorlenkoanum. It
119
Houbraken et al.
Fig. 37. Penicillium shearii. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse, CREA
obverse. B. Sclerotia. C–D. Ascospores. E–G. Conidiophores. H. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
Fig. 38. Penicillium sizovae. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse, CREA
obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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Houbraken et al.
can be differentiated from these species by the formation of inely
roughened conidia and its high growth rate on MEA and YES.
Distribution and ecology: This species has been isolated from
soil, margarine, sea salt, salty water in saltern, glue and Papaver
somniferum in the Netherlands, Portugal, Syria, Italy, Slovenia.
Barcode & molecular based ID: GenBank no. GU944588. This
species has unique ITS, β-tubulin and calmodulin sequences.
Taxonomy and phylogeny: Pitt (1980) placed P. sizovae in
synonymy with P. fellutanum, but this species was later accepted
and reinstated by Pitt & Samson (1993). CBS 413.69NT is
degenerated and shows both conidiophores with terminal
metulae, as well as subterminal and intercalary metulae. These
features could explain the earlier proposed synonymy in P.
fellutanum (Houbraken et al. 2010).
Penicillium steckii Zaleski, Bull. Int. Acad. pol. Sci. Lett.,
Sér. B.: 469. 1927. Fig. 39.
= Penicillium corylophiloides S. Abe, J. gen. appl. Microbiol, Tokyo 2: 89. 1956
(nom. inval., Art. 36).
Typus: ex cotton fabric treated with copper naphthenate, Panama
(IMI 40583 – neotype, designated by Pitt et al. 2000; cultures extype CBS 260.55 = DTO 22G5 = ATCC 10499 = CECT 2268 = DSM
1252 = NRRL 2140 = QM 6413 = NDRC 52B4C).
Description: Colony diam, 7 d, in mm: CYA 24–32; CYA15°C 7–13;
CYA30°C 15–23; CYA37°C no growth; MEA 21–30; YES 29–40;
DG18 24–36; ratio CYAS:CYA 1.0–1.2; creatine agar 11–19, weak
to moderate growth, no or weak acid production.
Moderate or good sporulation on CYA, velvety, conidia grey green,
mycelium inconspicuous, small clear or weak yellow exudate
droplets, soluble pigments absent, reverse in shades of crème
(crème, pale crème, yellow-crème or brown crème). Moderate to
good sporulation on YES, conidia grey green, occasionally dull
green, soluble pigments absent, reverse in most isolates (pale)
yellow, sometimes orange. Good sporulation on DG18, conidia
grey green conidia, reverse variable, pale, cream, (bright) yellow
or yellow-orange. Good sporulation on MEA, conidia grey green or
dull green, colony texture velvety. Ehrlich reaction negative, with
the exception of CBS 122391.
Sclerotia absent. Conidiophores borne from surface hyphae,
predominantly symmetrically biverticillate, occasionally with
an additional branch; stipes smooth, 100–300 × 2.2–3.0 µm.
Metulae in whorls of 3–6, 13–18 × 2.5–3.3 µm, equal in length.
Phialides ampulliform, 7.0–10 × 2.2–3.0 µm. Conidia broadly
ellipsoidal, in some strains slightly fusiform, smooth, 2.3–3.0×
2.0–2.5 µm.
Extrolites: Isochromantoxins (Cox et al. 1979, Malmstrøm et al.
2000), quinolactacin, tanzawaic acid E, “ALTI”, “EXPO”, “FON”,
“FOS”, “GLOO”, “GYF”, “PHOE”, “RAI”, “STOK”, “SVUL”, and
“VERN” (Houbraken et al. 2010).
Diagnostic characters: No growth at 37 °C, moderate growth at
33 °C; reverse colours on CYA in shades of crème, broadly
ellipsoidal conidia.
122
Similar species: Penicillium steckii is phylogenetically related to P.
sizovae, P. citrinum, P. hetheringtonii and P. gorlenkoanum. This
species is characterised by the formation of broadly ellipsoidal
conidia, which are not formed by any of the other species mentioned.
Penicillium tropicoides and P. tropicum also form broadly ellipsoidal
conidia, but also produce cleistothecia and ascospores.
Distribution and ecology: This species has a worldwide distribution
and has been isolated in Japan, the Netherlands, Panama,
Venezuela, Bermuda, Egypt, Venezuela, Indonesia and Slovenia.
Penicillium steckii is isolated from cotton fabric treated with copper
naphthenate, (potting) soil, hypersaline water, blue runner ish,
baled coastal grass hay, artichokes, Ascidie (tunicate, urochordata),
and as an endophyte of root of coffee plant (Posada et al. 2007).
Barcode & molecular based ID: GenBank no. GU944597. This
species has a unique ITS sequence. A subgroup in the P. steckii
clade was observed. This subgroup, characterised by a single
basepair difference on position 164 of the ITS2 region, included the
type strain of P. corylophiloides nom. inval. (CBS 325.59).
Taxonomy and phylogeny: Abe (1956) described P. corylophiloides
without a Latin diagnosis and designation of a holotype. According
to Abe (1956), P. corylophiloides could be differentiated from
P. citrinum and P. steckii by the formation of ellipsoidal conidia.
Houbraken et al. (2010) showed that P. steckii also formed broadly
ellipsoidal conidia and both species were placed in synonymy.
Following the phylogenetic species concept, P. steckii and P.
corylophiloides are separate species; however, no differences in
morphology, physiology or extrolites patterns could be observed
and are therefore they are placed in synonymy (Houbraken et al.
2010).
Penicillium sumatrense von Szilvinyi, Archiv. Hydrobiol. 14,
Suppl 6: 533. 1936. Fig. 40.
= Penicillium baradicum Baghdadi, Novosti Sistematiki Nizshikh Rastenii 5:
107. 1968.
= Penicillium meleagrinum var. viridilavum Abe, J. Gen. Appl. Microbiol.,
Tokyo 2: 92. 1956 (nom. inval.).
Typus: ex soil, Toba Heath, Sumatra, Indonesia (CBS 281.36 –
lectotype, designated here; cultures ex-type DTO 22F1 = NRRL
779 = FRR 779 = ATCC 48669 = IBT 29658 = IBT 4978).
Description: Colony diam, 7 d, in mm: CYA 33–42; CYA15°C 10–
16; CYA30°C (10–) 15–25; CYA37°C no growth; MEA 27–36; YES
(26–) 32–42 (–47); DG18 (20–) 25–34; ratio CYAS:CYA 0.9–1.1;
creatine agar 15–23, weak growth and acid production absent.
Moderate or good sporulation on CYA, occasionally absent,
velvety, conidia dull-green or dark-green, mycelium inconspicuous,
exudate absent or present as small or large (pale)-yellow droplets,
occasionally clear or light brown, soluble pigments in most
strains absent, in some isolates weakly produced and light brown
coloured, margin entire, reverse in shades of beige, beige-brown
or brown. Good sporulation on YES, conidia dull-green, mycelium
inconspicuous, soluble pigments absent, reverse yellow. Good
sporulation on DG18; conidia grey-green or dull-green, reverse pale
or pale yellow. Sporulation on MEA variable, conidia blue-green,
light green or grayish-green, mycelium inconspicuous, loccose
colony texture in fresh isolates, velvety in strains maintained for
longer periods in the collection. Ehrlich reaction negative.
taxonoMy of Penicillium Section citrina
Fig. 39. Penicillium steckii. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse, CREA
obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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123
Houbraken et al.
Fig. 40. Penicillium sumatrense. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
Sclerotia absent. Conidiophores predominantly biverticillate,
occasionally with an additional branch, stipes up to 200 µm long
with smooth or inely rough walls, 2.0–3.0 µm wide. vMetulae
in terminal verticils and fairly compact, 3–6, uneven in length,
vesiculate and rather long (10–) 12–16 × 2.0–3.0 µm. Phialides
ampulliform, 8.0–10 × 2–3.5 µm. Conidia subglobose or broadly
ellipsoidal, inely roughened, occasionally smooth, 2.0–2.5 µm
diam.
Extrolites: Curvularin (Vesonder et al. 1976, Malmstrøm et al. 2000),
dehydrocurvularin, “POTO”, “SAAT”, “TERRIT”, “TIDL”, “VOX”.
Diagnostic characters: Growth on CYA incubated at 33 °C (cultures,
which are maintained for long periods in culture collections, have
a lower maximum growth temperature), beige-brown reverse on
CYA, high growth rate on YES with yellow reverse.
Similar species: Penicillium sumatrense is phylogenetically distinct
and differs from P. citrinum and P. hetheringtonii by its inability
to grow at 37 °C. Penicillium paxilli has a pale reverse on CYA,
appressed whorls of metulae and roughened stipes; P. steckii and
P. sizovae lack a distinct yellow reverse on YES.
Distribution and ecology: This species has a worldwide distribution,
but has a preference for (sub)tropical regions. Its main habitat
is soil, but it has also been isolated from marine environments
(Malmstrøm et al. 2000), as an endophyte of Vitis vinifera (Z. Wang
& X. Qian, unpublished, GenBank no. EU030367), cork (Serra
et al. 2008), packaging material imported into the Netherlands,
pomegranates and bromeliad leaf tissue.
Barcode & molecular based ID: GenBank no. GU944578. This
species has unique ITS, tubulin and calmodulin sequences.
Taxonomy and phylogeny: Penicillium sumatrense was formally
considered a synonym of P. corylophilum (Pitt 1980), but Peterson
(2000) and Houbraken & Samson (2011) showed that these
two species are phylogenetically unrelated. The former species
belongs to section Citrina (Peterson’s group 1), and the latter to
section Exilicaulis (Peterson’s group 4). Penicillium meleagrinum
var. viridilavum was described without a Latin diagnosis, making
the description invalid (Art. 36). Pitt et al. (2000) synonymised this
species with P. janthinellum; however, Serra et al. (2008) showed
that P. meleagrinum var. viridilavum is genetically close to the
type strain of P. sumatrense. The congruence of the phylograms
from four different loci indicated that this could be a separate
species (Serra et al. 2008). Our data (Fig. 4) also shows sequence
variation among the analysed P. sumatrense strains. However,
no differences in phenotype and extrolite patterns were detected
among these strains and therefore they are maintained as one
species. More research is needed to clarify the population structure
of this species.
Penicillium terrigenum Seifert, Houbraken, Frisvad &
Samson, sp. nov. MycoBank MB563204. Fig. 41.
Etymology: Referring to soil, the substrate from where the type
strain was isolated.
Differt ab omnibus speciebus afinibus coloniis in agaro CYA bene crescentibus ad
33 °C, conidiis ellipsoideis, laevibus, conidiophoris biverticillatis.
www.studiesinmycology.org
Typus: ex soil, Hawaii, USA, R. A. Samson (CBS H-20667 –
holotypus, cultures ex-type CBS 127354 = DTO 9D4 = IBT 30769).
Description: Colony diam, 7 d, in mm: CYA 28–36; CYA15°C 7–15;
CYA30°C 18–23; CYA37°C no growth; MEA 25–32; YES 34–41;
DG18 28–34; ratio CYAS:CYA 1.0–1.3; creatine agar 15–22, weak
growth and no acid production.
Sporulation on CYA variable, velvety and loccose at the centre,
conidia dull-grey green, mycelium white, exudate produced as
minute clear droplets, soluble pigments absent, margin entire
to slightly irregular, reverse pale or crème. Weak to moderate
sporulation on YES, mycelium white, soluble pigment absent,
reverse creme-yellow, occasionally with a green shade. Good
sporulation on DG18, conidia dull green, reverse pale. Moderate
to good sporulation on MEA, conidia dull or dull-grey green, colony
texture loccose. Ehrlich reaction negative.
Sclerotia absent. Conidiophores predominantly symmetrically
biverticillate, occasionally with an additional branch, stipes long, up
to 500 µm, smooth to inely rough walled or distinctly rough walled
(CBS 117967), 2.5–3.5 µm wide; metulae in a compact terminal
whorls of 3–7, slightly vesiculate, equal in length, (10–) 12–16 ×
2.0–3.5 µm; phialides ampulliform to cylindrical, 7.5–9 × 2.5–3.5
µm. Conidia broadly ellipsoidal, smooth, 2.0–3.0 × 2.0–2.5 µm.
Extrolites: “HAEN”, “ISOC”, “PRS”, “VERSI”.
Diagnostic characters: Good on CYA incubated at 33 °C, broadly
ellipsoidal smooth walled conidia, biverticillate conidiophores.
Similar species: This species is phylogenetically related to P.
copticola, but can be distinguished by its poor growth on CREA.
Morphologically, this species is similar to P. steckii, which also
forms broadly ellipsoidal conidia and is also able to grow at 33
°C. Penicillium steckii sporulates better on CYA and YES and has
velvety colonies.
Distribution and ecology: This species is isolated from Hawaiian
soil, a leaf surface, USA, a mushroom fairy ring in Oshawa, Ontario,
Canada and soil in Portugal. A BLAST analysis showed that this
species was also isolated from a French pastry product (brioche)
(GenBank FJ471589, ITS).
Barcode & molecular based ID: GenBank no. JN617684. This species
can be identiied with ITS, β-tubulin and calmodulin sequences.
Taxonomy and phylogeny: CBS 127357 has an intermediate
position between P. copticola and P. terrigenum (Fig. 4) and
represents a new species. This strain resembles P. terrigenum
in many aspects such as poor grow on CREA and the formation
of broadly ellipsoidal conidia. However, it differs from P. copticola
and P. terrigenum in its inability to grow at 33 °C. A more in-depth
study with more P. copticola and P. terrigenum strains is needed to
elucidate the taxonomy of this clade.
Penicillium tropicoides Houbraken, Frisvad & Samson,
Fung. Divers. 44: 127. 2010. Fig. 42.
Typus: ex rainforest soil, near Hua-Hin, Thailand (CBS 122410 –
holotypus, cultures ex-type DTO 10C4 = IBT 29043).
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Houbraken et al.
Fig. 41. Penicillium terrigenum. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
Description: Colony diam, 7 d, in mm: CYA 24–30; CYA15°C 5–11;
CYA30°C 15–25; CYA37°C no growth; MEA 18–23; YES 36–43;
DG18 16–23; ratio CYAS:CYA 1.1–1.4; creatine agar 13–16, poor
to moderate growth and weak acid production (under colony).
Sporulation on CYA inconspicuous or sparsely produced in fresh
isolated strains, becoming more conidial after several transfers,
conidia blue grey green, cleistothecia abundantly produced and
determining colony colour, drab grey, mycelium inconspicuously,
colonies typical with large hyaline exudate droplets, soluble
pigments absent, margin slightly irregular, reverse crème-brown.
Weak sporulation on YES, cleistothecia abundant present, drabgrey, soluble pigment absent, mycelium inconspicuously, reverse
yellow. Weak to good sporulation on DG18, reverse yellow.
Colonies on MEA ascomatal and sporulation absent or sparse,
cleistothecia darb grey. Ehrlich reaction negative.
Cleistothecia sclerotioid, 200–300 µm diam, ripening slowly and
mature after 3 mo on MEA and OA. Ascospores ellipsoidal, 2.5–3.5
× 1.5–2.5 µm, with two narrow, closely appressed equatorial ridges,
valves smooth by light microscopy, warted with anastomosing ribs
by SEM. Conidiophores arising from the mycelial mat, symmetrically
biverticillate, stipes smooth, 100–250 µm long, 2.5–3.5 µm wide.
Metulae in whorls of 2–5, 13–17 × 3.0–4.0 µm, uniform in length.
Phialides ampulliform, 8.5–10.5 x 2.0–3.0 µm. Conidia broadly
ellipsoidal, smooth, 2.0–3.0 × 2.0–2.5 µm.
Extrolites: Isochromantoxins, several apolar indol-alkaloids, “CITY”,
“HOLOX”, “PR1-x”, “RAIMO” (Houbraken et al. 2010).
Sporulation on CYA sparse, conidia blue grey green, cleistothecia
abundantly produced, orange-tan, becoming warm shades of grey
(brownish-grey) in age, mycelium inconspicuous; exudate copious
produced in large, hyaline droplets, soluble pigments absent,
reverse crème coloured. Weak sporulation on YES, cleistothecia
abundantly produced, deep dull grey, mycelium inconspicuous,
soluble pigment absent, reverse crème-yellow. Good sporulation
on DG18, conidia blue-grey green, reverse pale or very pale yellow.
Colonies on MEA ascomatal, in shades of grey, sporulation absent
or inconspicuous. Ehrlich reaction negative.
Cleistothecia sclerotioid, 200–300 µm diam, ripening within 3–6 wk
on MEA and OA. Ascospores ellipsoidal, 2.5–3 × 2–2.5 µm, with two
narrow, closely appressed equatorial langes and inely roughened
valves. Conidiophores arising from the mycelial mat, symmetrically
biverticillate, stipes smooth, 2.5–3.5 µm wide; metulae in whorls of
2–5 (–8), 12–16 × 2.5–3.5 µm. Phialides ampulliform, 8.0–10.5 ×
2.0–3.0 µm. Conidia broadly ellipsoidal, smooth, 2.3–3.0 × 2.0–2.5
µm.
Extrolites: Several apolar indol-alkaloids, “CITY”,”EMON”, ”HOLOX”
and “RAIMO” (Tuthill & Frisvad 2004, Houbraken et al. 2010).
Diagnostic characters: No growth at 37 °C, abundant production
of cleistothecia in warm shades of grey (brownish grey), maturing
within 2–5 wk, colonies on CYA incubated at 30 °C reaching a
diameter of 25–30 mm.
Similar species: See P. tropicoides.
Diagnostic characters: Slow growth at 30 °C, no growth at 37 °C,
abundant production of drab-grey cleistothecia, maturing after
prolonged incubation, over 3 months.
Distribution and ecology: Penicillium tropicum has been isolated
from (sub)tropical soils (e.g. India, Costa Rica, Ecuador and
Galapagos Islands).
Similar species: Penicillium tropicoides morphologically resembles
P. tropicum. The difference between P. tropicoides and P. tropicum
is the slower maturation of the cleistothecia, slower growth rate at
30 °C and the production of isochromantoxins by P. tropicoides.
Penicillium shearii is related, but can be differentiated by a higher
maximum growth temperature than P. tropicoides and P. tropicum.
Barcode & molecular based ID: GenBank no. GU944582.
Penicillium tropicum and P. tropicoides have no differences in their
ITS regions, but these species can be differentiated with β-tubulin
and calmodulin sequences.
Distribution and ecology: Penicillium tropicoides is isolated form
rainforest soil in Thailand.
Penicillium ubiquetum Houbraken, Frisvad & Samson, sp.
nov. MycoBank MB563201. Fig. 44.
Barcode & molecular based ID: GenBank no. GU944584.
Penicillium tropicoides and P. tropicum have no differences in their
ITS regions, but these species can be differentiated with β-tubulin
and calmodulin sequences.
Taxonomy and phylogeny: None.
Penicillium tropicum Houbraken, Frisvad & Samson, Fung.
Divers. 44: 129. 2010. Fig. 43.
= Eupenicillium tropicum Tuthill & Frisvad Mycological Progress 3: 14. 2004.
Typus: ex soil beneath Coffea arabica, Karnataka, India (SC42-1 –
holotype, cultures ex-type DTO 31B1 = CBS 112584 = IBT 24580).
Description: Colony diam, 7 d, in mm: CYA 24–31; CYA15°C 9–13;
CYA30°C 25–30; CYA37°C no growth; MEA 23–27; YES 33–37;
DG18 20–25; ratio CYAS:CYA 1.0–1.1; creatine agar 16–20, poor
growth and weak acid production.
www.studiesinmycology.org
Taxonomy and phylogeny: None.
Etymology: Named after the worldwide distribution of this species.
Differt ab omnibus speciebus afinibus conidiis subtiliter exasperatis, coloniis ad 30
°C haud crescentibus, coloniis in agaro MEA ad 25 °C post hebdomatem usque ad
18–26 mm, reverso plus minusve aurantiaco vel roseo-rubro in agaro YES.
Typus: ex soil, Wilson Botanical Garden, Costa Rica, M. Christensen
(CBS H-20659 – holotypus, cultures ex-type CBS 126437 = DTO
78B5 = IBT 22226).
Description: Colony diam, 7 d, in mm: CYA 24–34; CYA15°C 14–
18; CYA30°C and CYA37°C no growth; MEA 18–26; YES 30–36;
DG18 18–27; ratio CYAS:CYA 1–1.3; creatine agar 13–18, weak to
moderate growth and no acid production.
Good sporulation on CYA, velvety, conidia dull-green to dark
green, mycelium inconspicuous, exudates clear, soluble
pigments absent, margin entire, reverse flesh coloured,
127
Houbraken et al.
Fig. 42. Penicillium tropicoides. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B. Ascomata. C–D. Ascospores. E–G. Conidiophores. H. Conidia. Scale bars = 10 µm.
128
taxonoMy of Penicillium Section citrina
Fig. 43. Penicillium tropicum. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse, CREA
obverse. B. Sclerotia. C. Ascospores. D–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
www.studiesinmycology.org
129
Houbraken et al.
Fig. 44. Penicillium ubiquetum. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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taxonoMy of Penicillium Section citrina
pinkish-brown with orange centre, often with orange pigmented
sulcations. Good sporulation on YES, mycelium white, soluble
pigments absent, reverse in shades of orange to pinkish-red.
Good sporulation on DG18, conidia in shades of dull green,
reverse pale, pale with yellow centre or bright yellow. Moderate
to good sporulation MEA, conidial colour variable: blue-green or
bluish-grey green or dark-blue green, colony texture floccose.
Ehrlich reaction negative.
Sclerotia absent. Conidiophores symmetrically biverticillate,
occasionally with an divergent branch that is shorter than the main axis;
stipes shorter than most related species, up to 300 µm, smooth, 2.5–
4.0 µm wide; metulae in a compact terminal verticil, 3–7 (–9), unequal
in length, vesiculate, (8–) 10–15 × 2.0–3.5 µm. Phialides ampulliform,
stout, 6.0–8.0 × 1.5–3.0 µm. Conidia globose to subglobose, inely
roughened, strongly pigmented cell wall, 1.8–2.5 µm diam.
Extrolites: Citrinin, terrein, “ALK”, “GLYF”, “RAI”, “TRIP”,
“XANTHOC”, isolates in one subclade, CBS 126438 & CBS
126436 produce anthraquinone bisanthrons, citrinin, okaramins,
and “SENGA”.
Diagnostic characters: Finely roughened conidia, no growth at 30
°C, colonies on MEA attaining a diameter of 18–26 mm in 7 d at 25
°C, reverse on YES in shades of orange to pinkish-red.
Similar species: See P. pancosmium.
Distribution and ecology: Soil appears to be the primary habitat,
but this species is also isolated from cork bark (GenBank no.v
EF198586, as P. decaturense). Worldwide distribution: Queensland,
Australia, Wisconsin, USA, Madagascar, Costa Rica, Italy, Portugal.
Barcode & molecular based ID: GenBank no. JN617680 (1)
and JN617677 (2). Penicillium ubiquetum can be divided in
two groups based on ITS sequences. ITS sequences of group
1 are unique (incl. CBS 126437T); group 2 ITS sequences of
P. ubiquetum are identical with P. waksmanii (CBS 126438,
CBS 126436 and NRRL 35636). Figure 3 shows that the latter
isolates also form a subgroup based on partial β-tubulin and
calmodulin sequences.
Taxonomy and phylogeny: CBS 126438 and CBS 126436 have a
distinct extrolite pattern and differ in their ITS sequence with other
P. ubiquetum strains. However, no phenotypic or physiological
differences were observed among these and other P. ubiquetum
strains, and therefore these strains are all regarded as one species.
Penicillium vancouverense Houbraken, Frisvad & Samson,
sp. nov. MycoBank MB563207. Fig. 45.
Etymology: Named after the location of the type strain, Vancouver
(Canada).
Differt ab omnibus speciebus afinibus mycelio lavido (vulgo in CYA15°C et/
vel YES), conidiis glaucoviridibus in agaro MEA et conidiis subtiliter exasperatis,
crassitunicatis.
Typus: ex soil under Maple tree, Vancouver, BC, Canada, J.C.
Frisvad (CBS H-20646 – holotypus, cultures ex-type. CBS 126323
= DTO 82B8 = IBT 20700).
www.studiesinmycology.org
Description: Colony diam, 7 d, in mm: CYA 20–30; CYA15°C 17–
25; CYA30°C and CYA37°C: no growth; MEA 16–23; YES 23–33;
DG18 17–25; ratio CYAS:CYA 1.0–1.3; creatine agar 8–17, weak
growth and no acid production.
Weak to moderate sporulation on CYA, velvety to loccose, conidia
grey-green, mycelium light-yellow, often with minute clear or yellow
exudates droplets, soluble pigment production variable, if produced
yellow coloured, margin entire, reverse in shades of orange-brown
or brown. Moderate to good sporulation on YES, conidia dull green,
occasionally dull-blue green, mycelium in shades of yellow, soluble
pigments absent, reverse beige or beige-brown. Good sporulation
on DG18, conidia dull-green, reverse pale or yellow. Moderate
to good sporulation on MEA, conidia blue green, colony texture
velvety to loccose. Ehrlich reaction negative, with exception of
CBS 126324.
Sclerotia absent. Conidiophores predominantly symmetrically
biverticillate and, depending on the isolate, additional branches
occur; stipes 200–400 µm long, smooth or inely rough walled,
width variable, 2.0–4.0 µm; metulae in a compact terminal whorls
of 3–6 (–7), unequal in length, often vesiculate, 10–14 × 2.5–3.5
µm. Phialides ampulliform, 7–9 × 2.0–3.5 µm. Conidia subglobose,
inely roughened and with a distinct thick and pigmented cell wall,
2.0–3.0 µm diam.
Extrolites: The extrolite patterns of P. vancouverense isolates are
somewhat diverse. All strains produce citrinin, citreoviridin, “MIF”,
“PAS” and “met OE”. Some strains also produce “CANOT”, “MIM”,
“PHOE” and “XANTHOC”.
Diagnostic characters: Light yellow mycelium (especially on
CYA15°C and/or YES), blue green conidia on MEA and inely
roughened, thick walled conidia.
Similar species: Penicillium vancouverense is phylogentically
related to P. pasqualense, but the latter species does not have
yellow mycelium and has a dark-brown reverse on CYA. Penicillium
manginii and some strains of P. miczynskii and related species also
form yellow mycelium; P. manginii can be differentiated by the
faster growth rate on CYA and the red soluble on YES; P. miczynskii
and related species have smooth walled, subglobose to broadly
ellipsoidal conidia.
Distribution and ecology: Penicillium vancouverense has a
worldwide distribution (the Netherlands, Costa Rica, Chile,
California, USA, Queensland, Australia, Madagascar, BC and
Ontario, Canada). Soil appears to be the primary habitat, but this
species is also isolated from indoor air of a house and a nut of
Juglans cinerea (butternut).
Barcode & molecular based ID: GenBank no. JN617675. With the
exception of isolate CBS 126321, all investigated strains have the
same unique ITS sequence. Isolate CBS 126321 has one base
pair difference in the ITS region compared with the type isolate
CBS 126324T.
Taxonomy and phylogeny: Penicillium miczynskii is characterised
by the production of yellow pigmented mycelium, exudates and
reverses (Pitt 1980, Christensen et al. 1999). These features are
also characteristic for P. vancouverense and it is therefore likely
that P. vancouversense isolates were previously identiied as
131
Houbraken et al.
Fig. 45. Penicillium vancouverense. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
132
taxonoMy of Penicillium Section citrina
P. miczynskii. This study shows that P. miczynskii forms smooth
walled conidia and stipes. There is some variation in extrolite
proiles and sequences detected among the P. vancouverense
isolates. The different extrolite proiles do not correlate with the
clustering observed in the phylogenetic study.
Penicillium waksmanii Zaleski, Bull. Int. Acad. pol. Sci.
Lett., Sér. B.: 468. 1927. Fig. 46.
= Penicillium rivolii Zaleski, Bull. Int. Acad. pol. Sci. Lett., Sér. B: 471. 1927.
indicates a close relationship with P. godlewskii. Peterson (2000)
suggested that P. rivolii was a distinct species, because 2 nucleotide
differences were observed between the ITS2 region of P. waksmanii
and P. rivolii. However, this observation could not be conirmed and
our data suggests that the names are conspeciic. Zaleski (1927)
described the production of orange pigment in this species. This is
not observed in our ex-type strain and recent isolated strains of P.
waksmanii. CBS 126426 produces, as the only isolate in this species,
an anthraquinone, which may be the orange pigment.
Typus: ex woodland soil, Purczcza Bialowieska Forest, Poland
(Herb. IMI 39746i – lectotype, Pitt 1980; cultures ex-type CBS
230.28 = DTO 22E6 = ATCC 10516 = FRR 777 = IFO 7737 = IMI
039746 = MUCL 29120 = NRRL 777 = QM 7681 = IBT 5003 = IBT
6994).
Penicillium wellingtonense AJL Cole, Houbraken, Frisvad
& Samson, sp. nov. MycoBank MB563208. Fig. 47.
Description: Colony diam, 7 d, in mm: CYA (20–) 25–32; CYA15°C
10–19; CYA30°C and CYA37°C no growth; MEA 18–24(–30); YES
25–33; DG18 16–27; ratio CYAS:CYA 1.0–1.2; creatine agar 10–
18, weak growth and no acid production.
Differt ab omnibus speciebus afinibus, coloniis in agaro CYA, MEA et YES constricte
crescentibus, ratione incrementi meliore ad 15 °C quam 25 °C.
Moderate sporulation on CYA, velvety, conidia dull green, mycelium
inconspicuous, exudate absent or as very small clear droplets,
soluble pigment absent, entire margins, reverse beige or beigebrown. Sporulation on YES moderate, mycelium white, conidia dull
green, soluble pigments absent, reverse beige or beige-brown.
Grey green conidia on DG18, reverse pale. Colonies on MEA dullgrey green, colony texture velvety with loccose centre. Ehrlich
reaction negative.
Sclerotia absent. Conidiophores symmetrically biverticillate and
often with a divergent branch, stipes up to 200–500 µm long,
smooth, 2.5–3.5 µm wide; metulae in a compact terminal verticil,
5–6 (–8), unequal in length, vesiculate, 10–14 × 2.5–3.5 µm;
phialides ampulliform, 7.0–9.0 × 2–3 µm. Conidia globose to
subglobose, inely roughened, 2.0–2.5 µm diam.
Extrolites: Citrinin, cyclopiamin, meleagrin (only produced by one
isolate), “GLYF”, “PAS”, “SENGA”.
Diagnostic characters: Finely roughened conidia, no growth at
30 °C, reverse on CYA in shades of brown and a pale reverse on
DG18.
Similar species: See P. chrzaszczii.
Distribution and ecology: Soil appears to be primary habitat, but
this species was also isolated from a dead polypore; strains have
been isolated from Poland, New Mexico, USA and New Zeeland.
Etymology: Named after location of the type strain, Wellington
(New Zealand).
Typus: ex soil, Wellington, New Zealand, A.J.L. Cole (CBS H-20657
– holotypus, cultures ex-type CBS 130375 = DTO 76C6 = IBT
23557).
Description: Colony diam, 7 d, in mm: CYA 10–15; CYA15°C 18–
23; CYA30°C and CYA37°C no growth; MEA 8–13; YES 20–25;
DG18 13–17; ratio CYAS:CYA 1.2–1.4; creatine agar 8–12, weak
growth and no acid production.
Moderate sporulation on CYA, velvety, conidia grey-green,
mycelium inconspicuous, exudate absent, soluble pigment absent,
reverse orange. Good sporulation on YES, conidia grey-green,
soluble pigments absent, reverse beige-brown. Dull-green colonies
on DG18, soluble pigments yellow, reverse reverse bright yellow.
Colonies on MEA blue-green, colony texture velvety and wrinkled
surface. Ehrlich reaction negative.
Sclerotia absent. Conidiophores predominantly symmetrically
biverticillate and occasionally with a branch; stipes rather long,
200–400 µm, smooth, 2.5–3.5 µm wide; metulae in a compact
terminal vertical, 3–7, unequal in length, short and stout, 9–12 ×
3.0–4.0 µm; phialides ampulliform, 7.5–9.5 × 2.5–3.5 µm. Conidia
subglobose to broadly ellipsoidal, smooth to inely roughened,
variable in size, 2.5–3.0 × 2.5–3.0 µm.
Extrolites: Citrinin, decaturin, “MIF”, “met Q”, “POF”, “RAI”, “TRIP”,
“XANTHOC”.
Diagnostic characters: Restricted growth on CYA, MEA and YES
and a higher growth rate at 15 °C than at 25 °C.
Barcode & molecular based ID: GenBank no. GU944602. Some
strains of P. ubiquetum (NRRL 35636 and CBS 126436) share
ITS sequences with P. waksmanii. Partial β-tubulin and calmodulin
sequences can be used for identiication.
Similar species: This species is unique in its slow growth rate.
Penicillium nothofagi is phenotypically similar. This species has a
pale-beige reverse on CYA and P. wellingtonense has an orange
reverse on CYA.
Taxonomy and phylogeny: Pitt (1980) accommodated P. waksmanii
in the series Fellutana of the subgenus Furcatum based on the
production of irregular conidiophores, while members of the series
Citrina produce regular, terminal penicilli. Microscopical analysis
of freshly isolated P. waksmanii strains from Polish soil show that
this species also forms regularly biverticillate structures, often with
an additional branch. Furthermore, phylogenetical analysis clearly
Distribution and ecology: This species is only known from its type
culture, isolated from soil, New Zealand.
www.studiesinmycology.org
Barcode & molecular based ID: GenBank no. JN617713. This
species has a unique β-tubulin, calmodulin and ITS sequence.
Taxonomy
and
phylogeny:
Penicillium
wellingtonense
is
133
Houbraken et al.
Fig. 46. Penicillium waksmanii. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
134
taxonoMy of Penicillium Section citrina
Fig. 47. Penicillium wellingtonense. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse,
CREA obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
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135
Houbraken et al.
Fig. 48. Penicillium westlingii. A. 7 d old cultures, 25 °C, left to right; irst row, all obverse, CYA, YES, DG18, MEA; second row, CYA reverse, YES reverse, DG18 reverse, CREA
obverse. B–F. Conidiophores. G. Conidia. Scale bars = 10 µm.
136
taxonoMy of Penicillium Section citrina
phylogenetically basal to P. vancouverense.
Penicillium westlingii Zaleski, Bull. Int. Acad. pol. Sci. Lett.,
Sér. B.: 473. 1927. Fig. 48.
= P. citrinum var. pseudopaxilli Martínez & Ramírez, nomen nudum.
Typus: ex soil under conifer, Denga Goolina, Poznan, Poland (IMI
92272 – neotype, designated by Pitt et al. 2000; cultures ex-type
CBS 231.28 = DTO 22E7 = IBT 15088).
Description: Colony diam, 7 d, in mm: CYA (25–) 30–36; CYA15°C
15–22; CYA30°C no growth or germination (0–3); CYA37°C no
growth; MEA 25–34; YES 33–40; DG18 16–28; ratio CYAS:CYA
0.9–1.1; creatine agar 10–17, weak or moderate growth and no
acid production.
No or sparse sporulation on CYA, white mycelium, exudate absent,
soluble pigments absent, margin polygonal, reverse pale, palebeige or pinkish beige. Sporulation on YES absent, mycelium
white, soluble pigments absent, reverse pale yellow (cream) to
cream-buff. Variable sporulation on DG18, conidia dull green or
grey green, reverse pale or pale-cream. Colonies on MEA poorly
sporulating, conidia blueish-dark green, colony texture loccose.
Ehrlich reaction negative.
Sclerotia absent. Conidiophores symmetrically biverticillate,
often with a divergent branch that is shorter than the main axis,
occasionally quaterverticillate, stipes up to 500 µm long, smooth,
2.5–4.0 µm wide; metulae in a compact terminal verticil, 3–6 (–8),
mostly uniform in length, both vesiculate and non-vesiculate,
8–14 (–16) × 2.0–3.5 µm. Phialides ampulliform, 6.5–8.5 × 2–3
µm. Conidia globose, inely or distinct roughened, 1.8–2.5 µm
diam.
Extrolites: Citrinin, curvularin, dehydrocurvularin,”PHOE”, “TRIP”,
“XANTHOC”.
Diagnostic characters: Finely roughened conidia, no (or at most
very restricted) growth at 30 °C, reverse on CYA pale or pale-beige
or pinkish beige, YES pale yellow to cream, no sporulation on CYA
and YES.
Similar species: Penicillium westlingii is phylogenetically related
to P. nothofagi and P. cosmopolitanum. It differs from P. nothofagi
by its faster growth rate on CYA, YES and MEA. Penicillium
cosmopolitanum generally has warmer reverse colours on CYA (with
orange coloured sulcations) and larger conidia (2.5–3.0 µm diam).
Penicillium westlingii is morphologically similar to P. pancosmium
and P. ubiquetum, but the latter two species sporulate well on CYA.
Penicillium waksmanii is also similar, but P. westlingii has a lighter
reverse on CYA and a faster growth rate on CYA and YES.
Distribution and ecology: This species commonly occurs in soils
in temperature regions, but is also isolated from a nut of Juglans
nigra (black walnut), acorns of Quercus, moose dung and indoor
environments.
Barcode & molecular based ID: GenBank no. GU944601. The
majority of the investigated P. westlingii isolates have the same
and unique ITS sequence, though several P. westlingii isolates
(CBS 124312, CBS 124313, CBS 127003, CBS 127040) share
sequences with certain isolates of P. cosmopolitanum. These
strains also appear in separate subclades in Fig. 4.
www.studiesinmycology.org
Taxonomy and phylogeny: Raper & Thom (1949) and Pitt (1980)
placed P. westlingii in synonymy of P. waksmanii. Pitt (1980) noted
that P. westlingii grows faster than P. waksmanii, but decided that
this was insuficient to describe P. westlingii as a separate species.
Peterson (2000) showed that P. westlingii and P. waksmanii are
genetically distinct and numerous (99 total) nucleotide differences
were detected. Re-examination of these sequences shows that
the deposited sequence of P. westlingii NRRL 800T (GenBank no.
AF033423) is not the same as CBS 231.28T. Comparison of the
sequence of NRRL 800 shows that P. westlingii is the same or very
closely related to P. citrinum, while the sequence obtained in this
study indicates a relation with P. waksmanii.
AcKNowledgeMeNTS
Barbara Byskal is thanked for collecting soil samples of Polish soil and Martin Meijer
and Edith de Rijk are thanked for the isolation and sequencing of Penicillium species
from those samples. Jelle Bos is acknowledged for performing the temperature growth
experiments and Ellen Kirstine Lyhne for her technical support. We are also grateful to
Gerry Louis-Seize for generating sequences, Keith Seifert, Dorothy Tuthill and Martha
Christensen for sharing strains and sequences, and Marjan Vermaas for preparing
the photographic plates. Uwe Braun is acknowledged for providing Latin diagnoses.
Research grants from Natural Sciences and Engineering Research Council of Canada
(NSERC) supported David Malloch, who shared Penicillium strains used in this study.
reFereNceS
Abe S (1956). Studies on the classiication of the Penicillia. Journal of General and
Applied Microbiology 2: 1–193.
Baghdadi VC (1968). De speciebus novis Penicilli Fr. et Aspergilli Fr. E terries Syriae
isolatis notula. Novitates Systematicae Plantarum non Vascularium 7: 96–114.
Belofsky GN, Gloer JB, Wicklow DT, Dowd PF (1995). Anti-insectan alkaloids.
Shearinines A-C and a new paxilline derivative from the ascostromata of
Eupenicillium shearii. Tetrahedron 51: 3959–3968.
Beyma Thoe Kingma FH van (1940). Beschreibung einiger neuer Pilzarten aus dem
Centraalbureau voor Schimmelcultures, Baarn (Nederland) VI. Antonie van
Leeuwenhoek 6: 263–290.
Brefeld O (1874). Botanische Untersuchungen über Schimmelpilze. Heft 2. “Die
Entwicklungsgeschichte von Penicillium”. Leipzig: A. Felix.
Christensen M, Frisvad JC, Tuthill D (1999). Penicillium miczynskii and related
species. Mycological Research 103: 527–541.
Cox RH, Hernandez O, Dorner JW, Cole RJ, Fennell DI (1979) A new isochroman
mycotoxin isolated from Penicillium steckii. Journal of Agricultural and Food
Chemistry 5: 999–1001.
Frisvad JC (1985). Creatine-sucrose agar, a differential medium for mycotoxin
producing terverticillate Penicillium species. Letters in Applied Microbiology 1:
109–113.
Frisvad JC (1989). The connection between the penicillia and aspergilla and
mycotoxins with special emphasis on misidentiied isolates. Archives of
Environmental Contamination and Toxicology 18: 452–467.
Frisvad JC, Filtenborg O (1990). Revision of Penicillium subgenus Furcatum based
on secondary metabolites and conventional characters. In: Modern Concepts
in Penicillium and Aspergillus Classiication (Samson RA, Pitt JI, eds) Plenum
Press, New York: 159–172.
Frisvad JC, Samson RA (2004). Polyphasic taxonomy of Penicillium subgenus
Penicillium. A guide to identiication of the food and air-borne terverticillate
Penicillia and their mycotoxins. Studies in Mycology 49: 1–173.
Frisvad JC, Samson RA, Stolk AC (1990). Notes on the typiication of some species
of Penicillium. Persoonia 14: 193–202.
Frisvad JC, Samson RA, Stolk AC (1990). Disposition of recently described species
of Penicillium. Persoonia 14: 209–232.
Frisvad JC, Thrane U (1987). Standardized high-performance liquid chromatography
of 182 mycotoxins and other fungal metabolites based on alkylphenone
retention indices and UV-VIS spectra (diode array detection). Journal of
Chromatography 404: 195–214.
Frisvad JC, Thrane U, Samson RA, Pitt JI (2006). Important mycotoxins and the
fungi which produce them. Advances in Experimental Medicine and Biology
571: 3–31.
137
Houbraken et al.
Gazis R, Chaverria P (2010). Diversity of fungal endophytes in leaves and stems
of wild rubber trees (Hevea brasiliensis) in Peru. Fungal Ecology 3: 240–254.
Houbraken J, Due M, Varga J, Meijer M, Frisvad JC, Samson RA (2007). Polyphasic
taxonomy of Aspergillus section Usti. Studies in Mycology 59: 107–128.
Houbraken J, Frisvad JC, Samson RA (2010). Taxonomy of Penicillium citrinum and
related species. Fungal Diversity 44: 117–133.
Houbraken J, López Quintero CA, Frisvad JC, Boekhout T, Theelen B, et al. (2011a).
Five new Penicillium species, P. araracuarense, P. elleniae, P. penarojense, P.
vanderhammenii and P. wotroi, from Colombian leaf litter. International Journal
of Systematic and Evolutionary Microbiology 61: 1462–1475.
Houbraken J, Samson RA (2011). Phylogeny of Penicillium and the segregation of
Trichocomaceae into three families. Studies in Mycology 70: 1–51.
Houbraken J, Spierenburg H, Frisvad JC (2011b). Rasamsonia, a new genus
comprising thermotolerant and thermophilic Talaromyces and Geosmithia
species. Antonie van Leeuwenhoek. DOI: 10.1007/s10482-011-9647-1.
Khan SA, Hamayun M, Yoon H, Kim H-Y, Suh S-J, et al. (2008). Plant growth
promotion and Penicillium citrinum. BMC Microbiology 8: 231–241.
Kozlovskiĭ AG, Stefanmova-Avramova LR, Reshitilova TA (1981a). The effect
of culture age and medium composition on the biosynthesis of alkaloids in
Penicillium gorlenkoanum. Microbiologiya 50: 1046–1052.
Kozlovskiĭ AG, Stefanmova-Avramova LR, Reshitilova TA, Sakharovskiĭ VG, Adanin
VM (1981b). Clavine ergot alkaloids, metabolites of Penicillium gorlenkoanum.
Prikladnaia Biokhimiia i Mikrobiologiia 17: 806–812.
Lai S, Matsunaga K, Shizuri Y, Yamamura S (1990). Biomimetic synthesis of
citreoviridin-type compounds and isolation of epicitreoviridinol, a new
metabolite of Penicillium pedemontanum IFO 9583. Tetrahedron Letters 31:
5503–5506.
Lund F (1995). Differentiating Penicillium species by detection of indole metabolites
using a ilter paper method. Letters in Applied Microbiology 20: 228–231.
Malmstrøm J, Christophersen C, Frisvad JC (2000). Secondary metabolites
characteristic of Penicillium citrinum, Penicillium steckii and related species.
Phytochemistry 54: 301–309.
McMillan LK, Carr RL, Young CA, Astin JW, Lowe RG, et al. (2003). Molecular
analysis of two cytochrome P450 monooxygenase genes required for paxilline
biosynthesis in Penicillium paxilli, and effects of paxilline intermediates on
mammalian maxi-K ion channels. Molecular Genetics and Genomics 270:
9–23.
Nagel DW, Steyn PS, Scott DB (1972). Production of citreoviridin by Penicillium
pulvillorum. Phytochemistry 11: 627–630.
Nielsen KF, Månsson M, Rank C, Frisvad JC, Larsen TO (2011). Dereplication of
microbial natural products by LC-DAD-TOFMS. Journal of Natural Products.
Doi: 10.1021/np200254t. In press.
Page RDM (1996). TREEVIEW: an application to display phylogenetic trees on
personal computers. Computer Applications in the Biosciences 12: 357–358.
Peterson SW (2000a). Phylogenetic analysis of Penicillium species based on ITS
and LSU-rDNA nucleotide sequences. In: Integration of modern taxonomic
methods for Penicillium and Aspergillus classiication (Samson RA, Pitt JI, eds)
Plenum Press, New York: 163–178.
Peterson SW, Horn BW (2009). Penicillium parvulum and Penicillium georgiense,
sp. nov., isolated from the conidial heads of Aspergillus species. Mycologia
101: 71–83.
Peterson SW, Bayer EM, Wicklow DT (2004). Penicillium thiersii, Penicillium
angulare and Penicillium decaturense, new species isolated from wood-decay
fungi in North America and their phylogenetic placement from multilocus DNA
sequence analysis. Mycologia 96: 1280–1293.
Pitt JI (1980). The genus Penicillium and its teleomorphic states Eupenicillium and
Talaromyces. Academic Press, London.
138
Pitt JI, Hocking AD (2009). Fungi and food spoilage. New York: Springer.
Pitt JI, Samson RA (1993). Species names in current use in the Trichocomaceae
(Fungi, Eurotiales). Koeltz Scientiic Books, Königstein.
Pitt JI, Samson RA, Frisvad JC (2000). List of accepted species and their synonyms
in the family Trichocomaceae. In: Integration of modern methods for Penicillium
and Aspergillus classiication (Samson RA, Pitt JI, eds). Harwood Academic
Publishers: Amsterdam: 9–49.
Pollock AV (1947). Production of citrinin by ive species of Penicillium. Nature 160:
331–332.
Posada F, Aime M, Peterson SW, Rehner SA, Vega F (2007). Inoculation of coffee
plants with the fungal entomopathogen Beauveria bassiana (Ascomycota:
Hypocreales). Mycological Research 111: 748–757.
Raper KB, Thom C (1949). Manual of the Penicillia, Williams & Wilkins.
Ramírez C (1982). Manual and atlas of the Penicillia. Amsterdam: Elsevier
Biomedical Press.
Ramírez C, Martínez AT (1981). Seven new species of Penicillium and a new variety
of Penicillium novae-caledoniae Smith. Mycopathologia 74: 35–49.
Rebuffat S, Davoust D, Molho L, Molho D (1980). La citréomontanine, nouvelle
α-pyrone polyéthylénique isolée de Penicillium pedemontanum. Phytochemistry
19: 427–431.
Rebuffat S, Molho D, Dizabo P (1984). Mass spectra of citreoviridin A and related
mycotoxins. Organic Mass Spectrometry 19: 349–351.
Samson RA, Houbraken J, Thrane U, Frisvad JC, Andersen B (2010). Food and
Indoor Fungi, CBS laboratory manual series 2, CBS-Fungal Biodiversity
Centre, Utrecht.
Shear CL (1934). Penicillium glaucum of Brefeld (Carpenteles of Langeron) refound.
Mycologia 26: 104–107.
Serra R, Peterson SW, CTCOR, Venâncio A (2008). Multilocus sequence
identiication of Penicillium species in cork bark during plank preparation for the
manufacture of stoppers. Research in Microbiology 159: 178–186.
Stamatakis A, Hoover P, Rougemont J (2008). A rapid bootstrap algorithm for the
RAxML Web-Servers. Systematic Biology 75: 758–771.
Stolk AC, Samson RA (1983). The ascomycete genus Eupenicillium and related
Penicillium anamorphs. Studies in Mycology 23: 1–149.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011). MEGA5:
Molecular Evolutionary Genetics Analysis using Maximum Likelihood,
Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology
and Evolution 28: 2731–2739.
Thom C (1930). The Penicillia. Williams & Wilkins, Baltimore: 1–644.
Tuthill DE, Frisvad JC (2004). A new species from tropical soils, Eupenicillium
tropicum. Mycological Progress 3: 13–18.
Vega FE, Posada F, Peterson SW, Gianfagna TJ, Chaves F (2006). Penicillium
species endophytic in coffee plants and ochratoxin A production. Mycologia
98: 31–42.
Young C, McMillan L, Telfer E, Scott B (2001). Molecular cloning and genetic
analysis of an indole-diterpene gene cluster from Penicillium paxilli. Molecular
Microbiology 39: 754–764.
Zaleski KM (1927). Über die in Polen gefundenen Arten der Gruppe Penicillium
Link. I, II and III Teil. Bulletin de l’Académie Polonaise des Sciences et des
Lettres, Classe des Sciences Mathématiques et Naturelles – Série B: Sciences
Naturelles: 417–563, pls 36–44 (printed in 1928).
Zhang Y, Li C, Swenson DC, Gloer JB, Wicklow DT, Dowd PF (2003). Novel
antiinsectan oxalicine alkaloids from two undescribed fungicolous Penicillium
spp. Organic Letters 5: 773–776.
Suppl. Fig. 1
Supplementary
InFormatIon
Citrina ‐ Tubuline
Taxonomy of Penicillium secTion citrina
CBS 241.85 P. citrinum
CBS 252.55 P. citrinum
CBS 232.38 P. citrinum
CBS 139.45 P. citrinum
CBS 122419 P. citrinum
CBS 122397 P. citrinum
CBS 122396 P. citrinum
CBS 122395 P. citrinum
CBS 122394 P. citrinum
CBS 115992 P. citrinum
CSB 122726 P. citrinum
DTO 78B9 P. citrinum
CBS 122452 P. citrinum
DTO 78C3 P. citrinum
79
CBS 122451 P. citrinum
100
CBS 117.64 P. citrinum
CBS 865.97 P. citrinum
70
CBS 101275 P. citrinum
DTO 30H7 P.
P hetheringtonii
100
CBS 124287 P. hetheringtonii
CBS 122392T P. hetheringtonii
73
CBS 117184 P. sizovae
CBS 413.69NT P. sizovae
CBS 115968 P. sizovae
98
CBS 139.65 P. sizovae
99
CBS 122387 P. sizovae
100 CBS 122410T P. tropicoides
p
CBS 122436 P. tropicoides
CBS 112584T P. tropicum
100 CBS 408.69T P. gorlenkoanum
CBS 411.69 P. gorlenkoanum
CBS 122390 P. steckii
CBS 260.55NT P. steckii
73
CBS 122389 P. steckii
94
CBS 122388 P. steckii
96 DTO 49G1 P.
P steckii
t kii
CBS 325.59 P. steckii
NRRL 35625 P. steckii
CBS 789.70 P. steckii
90
CBS 122391 P. steckii
CBS 335.59 P. sumatrense
CBS 130380 P. sumatrense
CBS 127363 P. sumatrense
CBS 117185 P.
P sumatrense
CBS 127362 P. sumatrense
CBS 127365 P. sumatrense
CBS 130377 P. sumatrense
CBS 130378 P. sumatrense
CBS 416.69 P. sumatrense
100
CBS 281.36T P. sumatrense
CBS 127364 P. sumatrense
CBS 115708 P. sumatrense
82 CBS 127366 P. sumatrense
CBS 330.79 P. corylophilum
0.1
Fig. S1. Maximum Likelihood tree based on a partial β-tubulin sequence data of the P. citrinum-clade. Numbers above branches are bootstrap values. Only values above 70 %
are shown and branches with more than 95 % bootstrap support are thickened. The phylogram is rooted with P. corylophilum (CBS 330.79).
www.studiesinmycology.org
138-S1
Houbraken et al.
Supplementary InFormatIon
98
0.1
DTO 78B9 P. citrinum
DTO 78C3 P. citrinum
CBS 122726 P. citrinum
CBS 252.55 P. citrinum
CBS
C
S 241.85
85 P. ccitrinum
t u
CBS 232.38 P. citrinum
CBS 139.45 P. citrinum
CBS 122452 P. citrinum
CBS 122451 P. citrinum
CBS 122419 P. citrinum
CBS 122397 P. citrinum
CBS 122396 P. citrinum
CBS 122395 P. citrinum
CBS 122394 P. citrinum
CBS 117.64 P. citrinum
100 CBS 115992 P. citrinum
CBS 101275 P. citrinum
73
CBS 865.97 P. citrinum
DTO 30H7 P. hetheringtonii
CBS 124287 P. hetheringtonii
94 CBS 122392T P. hetheringtonii
CBS 139.65
139 65 P.
P sizovae
CBS 413.69NT P. sizovae
100 CBS 122387 P. sizovae
CBS 117184 P. sizovae
CBS 115968 P. sizovae
CBS 112584T P. tropicum
100 CBS 122410T P. tropicoides
CBS 122436 P. tropicoides
CBS 260.55NT P. steckii
DTO 49G1 P. steckii
CBS 122390 P. steckii
CBS 122389 P. steckii
CBS 122388 P. steckii
98
CBS 789.70 P. steckii
NRRL 35625 P. steckii
CBS 122391 P. steckii
CBS 325.59 P. steckii
100 CBS 408.69
408 69T P.
P gorlenkoanum
l k
CBS 411.69 P. gorlenkoanum
CBS 127363 P. sumatrense
CBS 335.59 P. sumatrense
CBS 117185 P. sumatrense
CBS 127365 P. sumatrense
77
CBS 130377 P. sumatrense
CBS 130378 P. sumatrense
CBS 127362 P.
P sumatrense
CBS 130380 P. sumatrense
CBS 281.36T P. sumatrense
100 CBS 115708 P. sumatrense
100
CBS 127366 P. sumatrense
CBS 416.69 P. sumatrense
CBS 127364 P. sumatrense
CBS 330.79 P. corylophilum
Fig. S2. Maximum Likelihood tree based on a partial calmodulin sequence data of the P. citrinum-clade. Numbers above branches are bootstrap values. Only values above 70
% are shown and branches with more than 95 % bootstrap support are thickened. The phylogram is rooted with P. corylophilum (CBS 330.79).
138-S2
Taxonomy of Penicillium secTion citrina
Supplementary InFormatIon
CBS 122435 P. cosmopolitanum
CBS 251.70 P. cosmopolitanum
CBS 122406 P. cosmopolitanum
CBS 124315 P. cosmopolitanum
CBS 126990 P. cosmopolitanum
CBS 126992 P. cosmopolitanum
CBS 63
637.70
0 P.
P cosmopolitanum
li
CBS 126994 P. cosmopolitanum
CBS 200.86 P. cosmopolitanum
86 CBS 126993 P. cosmopolitanum
CBS 124316 P. cosmopolitanum
CBS 126995T P. cosmopolitanum
CBS 126991 P. cosmopolitanum
CBS 126997 P. cosmopolitanum
CBS 126998 P. cosmopolitanum
CBS 127038 P. cosmopolitanum
CBS 126996 P. cosmopolitanum
83
DTO 42G4 P. cosmopolitanum
DTO 82C8 P.
P cosmopolitanum
lit
CBS 586.70 P. cosmopolitanum
CBS 552.86 P. cosmopolitanum
CBS 127002 P. cosmopolitanum
CBS 126999 P. cosmopolitanum
CBS 127000 P. cosmopolitanum
CBS 127001 P. cosmopolitanum
CBS 127007 P. westlingii
CBS 688.77 P. westlingii
CBS 118051 P. westlingii
CBS 118166 P. westlingii
CBS 127005 P. westlingii
87
CBS 122407 P.
P westlingii
tli ii
CBS 122408 P. westlingii
CBS 122409 P. westlingii
CBS 127039 P. westlingii
CBS 124311 P. westlingii
CBS 127037 P. westlingii
CBS 231.28T P. westlingii
CBS 1270088 P. westlingii
CBS 118037 P. westlingii
73
CBS 127040 P. westlingii
CBS 127040 P. westlingii
CBS 127006 P. westlingii
CBS 124313 P.
P westlingii
tli ii
91
CBS 124312 P. westlingii
CBS 127003 P. westlingii
CBS 127004 P. nothofagi
CBS 130383T P. nothofagi
100 CBS 126237 P. christenseniae
CBS 126236T P. christenseniae
CBS 119390 P. decaturense
CBS 117510 P. decaturense
CBS 117509T P. decaturense
CBS 117506 P. decaturense
71
CBS 117504 P. decaturense
100
CBS 117507 P.
P decaturense
CBS 117505 P. decaturense
CBS 117508 P. decaturense
CBS 126423 P. godlewskii
CBS 126424 P. godlewskii
CBS 126422 P. godlewskii
CBS 218.28 P. godlewskii
CBS 215.28T P. godlewskii
CBS 117273 P. godlewskii
CBS 126421 P. godlewskii
DTO 42E9 P. godlewskii
CBS 124319 P. godlewskii
CBS 126419 P.
P godlewskii
CBS 126420 P. godlewskii
CBS 126430 P. chrzaszczii
CBS 124320 P. chrzaszczii
83
CBS 176.81 P. chrzaszczii
CBS 217.28T P. chrzaszczii
CBS 117525 P. waksmanii
CBS 117502 P. waksmanii
97
CBS 126429 P. waksmanii
71
DTO 78C1 P. waksmanii
CBS 230.28T P. waksmanii
CBS 126426 P. waksmanii
CBS 126428 P.
P waksmanii
90 CBS 124295 P. waksmanii
CBS 124322 P. waksmanii
CBS 124321 P. waksmanii
CBS 126427 P. waksmanii
CBS 126425 P. waksmanii
Fig. S3. Maximum Likelihood tree based on a partial β-tubulin
sequence data of the P. westlingii-clade. Numbers above branches are
bootstrap values. Only values above 70 % are shown and branches
with more than 95 % bootstrap support are thickened. The phylogram
is rooted with P. corylophilum (CBS 330.79).
www.studiesinmycology.org
70
73
DTO 82D1 P. pancosmium
CBS 126433 P. pancosmium
CBS 276.75T P. pancosmium
KAS 2126 P. pancosmium
CBS 118018 P. pancosmium
KAS 2138 P. pancosmium
CBS 126432 P. pancosmium
95
CBS 126435 P. pancosmium
CBS
124293 P. pancosmium
73
CBS 126434 P. pancosmium
CBS 126431 P. pancosmium
CBS 118007 P. pancosmium
CBS 126436 P. ubiquetum
86
NRRL 35636 P. ubiquetum
CBS 126438 P. ubiquetum
CBS 126439 P. ubiquetum
CBS 124317 P. ubiquetum
q
92 CBS 124318 P. ubiquetum
CBS 117212 P. ubiquetum
CBS 126437T P. ubiquetum
CBS 124450 P. ubiquetum
CBS 126327 P. vancouverense
CBS 117962 P. vancouverense
CBS 122400 P. vancouverense
CBS 124329 P. vancouverense
CBS 126326 P. vancouverense
CBS 122401 P. vancouverense
CBS 126325 P. vancouverense
CBS 124328 P. vancouverense
CBS 126321 P. vancouverense
CBS 126328 P. vancouverense
100
CBS 126324 P. vancouverense
CBS
130376 P. vancouverense
70
CBS 126323T P. vancouverense
CBS 126322 P. vancouverense
83
CBS 130375 P. wellingtonense
CBS 126329 P. pasqualense
96
CBS 124327 P. pasqualense
95
CBS 126330T P. pasqualense
CBS 122402 P. pasqualense
CBS 261.64 P. atrofulvum
T
100 CBS 109.66 P. atrofulvum
CBS 126332 P. atrofulvum
CBS 126331 P. atrofulvum
CBS 126234T P. raphiae
CBS 126235 P. raphiae
CBS 118028 P. cairnsense
CBS 126226 P. cairnsense
CBS 117982 P. cairnsense
KAS 2103 P. cairnsense
KAS 2102 P. cairnsense
CBS 117962 P. cairnsense
DTO 87B9 P. cairnsense
CBS 124326 P. cairnsense
95
CBS 124325T P. cairnsense
CBS 126225 P. cairnsense
71
DTO 82B7 P. cairnsense
CBS 124324 P. cairnsense
CBS 101623T P. quebecense
CBS 126277 P. aurantiacobrunneum
CBS 126230 P. aurantiacobrunneum
CBS 126228T P. aurantiacobrunneum
CBS 126229 P. aurantiacobrunneum
CBS 126224 P. miczynskii
CBS 126222 P. miczynskii
CBS 124323 P. miczynskii
CBS 126223 P. miczynskii
CBS 220.28T P. miczynskii
CBS 126231T P. neomiczynskii
CBS 409.65 P. manginii
CBS 327.79 P. manginii
CBS 408.65 P. manginii
CBS 343.52 P. manginii
CBS 253.31NT P. manginii
CBS 122403 P. manginii
93 CBS 407.65 P. manginii
CBS 126232 P. manginii
CBS 265.65 P. manginii
100
CBS 126233 P.
P manginii
i ii
CBS 108.66 P. manginii
CBS 378.65 P. manginii
CBS 330.79 P. corylophilum
0.1
Fig. S3. (Continued).
138-S3
Houbraken et al.
Supplementary InFormatIon
89
CBS 552.86 P. cosmopolitanum
CBS 251.70 P. cosmopolitanum
CBS 586.70 P. cosmopolitanum
CBS 637.70 P. cosmopolitanum
CBS 122435 P. cosmopolitanum
CBS 122406 P. cosmopolitanum
CBS 124315 P. cosmopolitanum
CBS 200.86 P. cosmopolitanum
CBS 126993 P. cosmopolitanum
CBS 126990 P. cosmopolitanum
DTO 42G4 P. cosmopolitanum
CBS 127001 P. cosmopolitanum
CBS 127002 P. cosmopolitanum
CBS 126991 P. cosmopolitanum
CBS 126995T P. cosmopolitanum
CBS 126994 P. cosmopolitanum
p
CBS 126999 P. cosmopolitanum
CBS 127000 P. cosmopolitanum
CBS 126992 P. cosmopolitanum
CBS 127038 P. cosmopolitanum
CBS 126996 P. cosmopolitanum
CBS 126997 P. cosmopolitanum
CBS 126998 P. cosmopolitanum
CBS 124316 P. cosmopolitanum
CBS 122408 P. westlingii
CBS 127007 P. westlingii
CBS 122407 P. westlingii
CBS 688.77 P. westlingii
CBS 122409 P. westlingii
g
CBS 124311 P. westlingii
T P. westlingii
CBS
231.28
98
CBS 127005 P. westlingii
CBS 127006 P. westlingii
CBS 127008 P. westlingii
CBS 127040 P. westlingii
CBS 118051 P. westlingii
CBS 127037 P. westlingii
88
CBS 127039 P. westlingii
CBS 118166 P. westlingii
CBS 118037 P. westlingii
CBS 124313 P. westlingii
CBS 127003 P. westlingii
g
CBS 124312 P. westlingii
CBS 127040 P. westlingii
CBS 130383T P. nothofagi
CBS 127004 P. nothofagi
DTO 82D1 P. pancosmium
CBS 126435 P. pancosmium
89
KAS 2126 P. pancosmium
KAS 2138 P. pancosmium
CBS 276.75T P. pancosmium
CBS 118018 P. pancosmium
CBS 126432 P. pancosmium
99 CBS 126434 P. pancosmium
CBS 124293 P. p
pancosmium
81
CBS 126433 P. pancosmium
96 CBS 118007 P. pancosmium
CBS 126431 P. pancosmium
CBS 117510 P. decaturense
75
CBS 119390 P. decaturense
CBS 117508 P. decaturense
CBS 117504 P. decaturense
T
94 CBS 117509 P. decaturense
CBS 117506 P. decaturense
100
CBS 117505 P. decaturense
CBS 117507 P. decaturense
CBS
124317
P.
ubiquetum
86
q
CBS 124318 P. ubiquetum
CBS 126439 P. ubiquetum
NRRL 35636 P. ubiquetum
CBS 126438 P. ubiquetum
CBS 126436 P. ubiquetum
CBS 126437T P. ubiquetum
CBS 124450 P. ubiquetum
CBS 117212 P. ubiquetum
CBS 124295 P. waksmanii
CBS 126427 P. waksmanii
CBS 126425 P. waksmanii
CBS 124321 P. waksmanii
CBS 126428 P. waksmanii
CBS 126426 P. waksmanii
CBS 124322 P. waksmanii
CBS 117525 P. waksmanii
CBS 117502 P. waksmanii
CBS 230.28T P. waksmanii
CBS 126429 P. waksmanii
DTO 78C1 P. waksmanii
CBS
215.28T P. godlewskii
97
CBS 126423 P. godlewskii
CBS 126424 P. godlewskii
CBS 124319 P. godlewskii
CBS 126421 P. godlewskii
DTO 42E9 P. godlewskii
CBS 126419 P. g
godlewskii
CBS 117273 P. godlewskii
T
CBS 218.28 P. godlewskii
CBS 126420 P. godlewskii
CBS 126422 P. godlewskii
81 CBS 176.81 P. chrzaszczii
CBS 126430 P. chrzaszczii
78 CBS 124320 P. chrzaszczii
CBS 217.28T P. chrzaszczii
CBS 126326 P. vancouverense
CBS 117962 P. vancouverense
CBS 122400 P. vancouverense
80 CBS 122401 P. vancouverense
CBS 126327 P. vancouverense
CBS 124329 P. vancouverense
CBS 126328 P. vancouverense
CBS
126321 P. vancouverense
90
CBS 124328 P. vancouverense
93
CBS 126325 P. vancouverense
CBS 126324 P. vancouverense
CBS 126323T P. vancouverense
CBS 130376 P. vancouverense
CBS 126322 P. vancouverense
85
CBS 130375 P. wellingtonense
70 CBS 122402 P. pasqualense
CBS
126330T P. pasqualense
99
86
CBS 126329 P. p
pasqualense
q
CBS 124327 P. pasqualense
100 CBS 126331 P. atrofulvum
CBS 126332 P. atrofulvum
100
CBS 261.64 P. atrofulvum
CBS 109.66 P. atrofulvum
75
100
CBS 126236T P. christenseniae
CBS 126237 P. christenseniae
97
CBS 126234T P. raphiae
CBS 126235 P. raphiae
CBS 408.65 P. manginii
CBS 343.52 P. manginii
75 CBS 407.65 P. manginii
CBS 253.31T P. manginii
g
CBS 122403 P. manginii
CBS
126232
P.
manginii
78
CBS 409.65 P. manginii
77 CBS 265.65 P. manginii
CBS 327.79 P. manginii
87
CBS 378.65 P. manginii
100
CBS 108.66 P. manginii
CBS 126233 P. manginii
DTO 87B9 P. cairnsense
CBS 126226 P. cairnsense
CBS 118028 P. cairnsense
CBS 117982 P. cairnsense
CBS 117962 P. cairnsense
CBS 124326 P. cairnsense
KAS 2103 P. cairnsense
KAS 2102 P. cairnsense
T
100 CBS 124325 P. cairnsense
CBS 124324 P. cairnsense
100
82 CBS 126225 P. cairnsense
DTO 82B7 P. cairnsense
CBS 101623T P. quebecense
CBS 126222 P. miczynskii
CBS 126223 P. miczynskii
89
98 CBS 220.28 P. miczynskii
CBS 124323 P. miczynskii
CBS 126224 P. miczynskii
72
CBS 126229 P.
P aurantiacobrunneum
ti
b
78
100 CBS 126277 P. aurantiacobrunneum
CBS 126230 P. aurantiacobrunneum
CBS 126228T P. aurantiacobrunneum
CBS 126231T P. neomiczynskii
CBS 330.79 P. corylophilum
0.1
Fig. S4. Maximum Likelihood tree based on a partial calmodulin
sequence data of the P. westlingii -clade. Numbers above branches
are bootstrap values. Only values above 70 % are shown and
branches with more than 95 % bootstrap support are thickened. The
phylogram is rooted with P. corylophilum (CBS 330.79).
138-S4
Fig. S4. (Continued).
Taxonomy of Penicillium secTion citrina
Supplementary InFormatIon
CBS 300.67 P. sanguifluum
CBS 441.88 P. sanguifluum
CBS 118024 P. sanguifluum
CBS 127029 P. sanguifluum
CBS
643.73 P. sanguifluum
79
CBS 644.73
644 73 P.
P sanguifluum
CBS 118020 P. sanguifluum
CBS 685.85 P. sanguifluum
70
CBS 148.83 P. sanguifluum
CBS 110.64 P. sanguifluum
CBS 127034 P. sanguifluum
94
CBS 127031 P. sanguifluum
CBS 127033 P. sanguifluum
CBS 127035 P. sanguifluum
85
92 CBS 127036 P. sanguifluum
g
CBS 127032NT P. sanguifluum
CBS 127030 P. sanguifluum
CBS 127028 P. roseopurpureum
82
CBS 127025 P. roseopurpureum
99 CBS 127026 P. roseopurpureum
CBS 281.39 P. roseopurpureum
CBS 266.29NT P. roseopurpureum
CBS 127027 P. roseopurpureum
CBS 130381 P. argentinense
100
CBS 130373 P. argentinense
CBS 130371T P. argentinense
92 CBS 130372 P. euglaucum
CBS 323.71T P. euglaucum
100
CBS 308.89 P. anatolicum
99 CBS 478.66T P. anatolicum
CBS 479.66 P. anatolicum
70
CBS 467.67 P. anatolicum
CBS 130382 P. copticola
96
CBS 12
127355
3 T P.
P copticola
i l
CBS 127356 P. copticola
CBS 127357 P. cf. terrigenum
100
CBS 127354T P. terrigenum
CBS 117967 P. terrigenum
83 CBS 117993 P. terrigenum
CBS 118059 P. shearii
CBS 290.48T P. shearii
CBS 513.73 P. shearii
99 CBS 502.78
502 78 P.
P shearii
CBS 343.54 P. shearii
CBS 578.70 P. shearii
CBS 117190 P. paxilli
97 CBS 127360 P. paxilli
CBS 162.96 P. paxilli
CBS 360.48T P. paxilli
CBS 101273 P. paxilli
88
CBS 101274 P. paxilli
CBS 117191 P.
P paxilli
CBS 547.77 P. paxilli
100
CBS 127361 P. paxilli
KAS 2144 P. paxilli
CBS 167.81T P. gallaicum
100
CBS 418.69 P. gallaicum
CBS 164.81 P. gallaicum
CBS 330.79 P. corylophilum
Clade 1
Clade 2
0.1
Fig. S5. Maximum Likelihood tree based on a partial β-tubulin sequence data of selected members of section Citrina. Numbers above branches are bootstrap values. Only
values above 70 % are shown and branches with more than 95 % bootstrap support are thickened. The phylogram is rooted with P. corylophilum (CBS 330.79).
www.studiesinmycology.org
138-S5
Houbraken et al.
Supplementary InFormatIon
CBS 130381 P. argentinense
88 CBS 130373 P. argentinense
CBS 130371T P. argentinense
97 CBS 130372 P. euglaucum
CBS 323.71NT P. euglaucum
100
98 CBS 478.66
478 66T P.
P anatolicum
CBS 479.66 P. anatolicum
CBS 467.67 P. anatolicum
CBS 308.89 P. anatolicum
CBS 290.48T P. shearii
CBS 502.78 P. shearii
CBS 343.54 P. shearii
CBS
118059 P. shearii
100
CBS 513.73 P. shearii
CBS 578.70 P. shearii
CBS 127360 P. paxilli
CBS 547.77 P. paxilli
CBS 360.48T P. paxilli
CBS 162.96 P. paxilli
CBS 117191 P. paxilli
CBS 117190 P. paxilli
100
CBS 101274 P. paxilli
100
CBS 101273 P. paxilli
CBS 127361 P. paxilli
KAS 2144 P. paxilli
CBS 130382 P. copticola
100
CBS 127355T P. copticola
CBS 127356 P. copticola
CBS 127357 P. cf. terrigenum
100
CBS 127354T P. terrigenum
CBS 117967 P. terrigenum
93 CBS 117993 P. terrigenum
CBS 118020 P. sanguifluum
92 CBS 685.85 P. sanguifluum
CBS 643.73 P. sanguifluum
81
CBS 644.73 P. sanguifluum
CBS 118024 P. sanguifluum
CBS 300.67 P. sanguifluum
81
CBS 441.88 P. sanguifluum
86
CBS 127029 P. sanguifluum
CBS 110.64 P. sanguifluum
CBS 148.83 P. sanguifluum
CBS 127034 P.
P sanguifluum
ifl
100
CBS 127031 P. sanguifluum
CBS 127032NT P. sanguifluum
CBS 127035 P. sanguifluum
99
CBS 127036 P. sanguifluum
98
CBS 127030 P. sanguifluum
100
CBS 127033 P. sanguifluum
CBS 127025 P. roseopurpureum
CBS 127026 P. roseopurpureum
82 CBS 281.39
281 39 P.
P roseopurpureum
99
CBS 266.29NT P. roseopurpureum
CBS 127028 P. roseopurpureum
79
CBS 127027 P. roseopurpureum
CBS 164.81 P. gallaicum
100 CBS 418.69 P. gallaicum
CBS 167.81T P. gallaicum
CBS 330.79 P. corylophilum
Clade 1
Clade 2
0.1
Fig. S6. Maximum Likelihood tree based on a partial calmodulin sequence data of selected members of section Citrina. Numbers above branches are bootstrap values. Only
values above 70 % are shown and branches with more than 95 % bootstrap support are thickened. The phylogram is rooted with P. corylophilum (CBS 330.79).
138-S6