Polyphasic taxonomy of the heat resistant ascomycete ... - Persoonia

Persoonia 22, 2009: 14–27 

www.persoonia.org 

RESEARCH ARTICLE 

doi:10.3767/003158509X418925 

Polyphasic taxonomy of the heat resistant ascomycete genus 

Byssochlamys and its Paecilomyces anamorphs 

R.A. Samson 1 , J. Houbraken 1 , J. Varga 1,2 , J.C. Frisvad 3 

Key words 

Byssochlamys 

emodin 

Eurotiales 

extrolites 

heat resistance 

mycophenolic acid 

Paecilomyces 

patulin 

Abstract Byssochlamys and related Paecilomyces strains are often heat resistant and may produce mycotoxins 

in contaminated pasteurised foodstuffs. A comparative study of all Byssochlamys species was carried out using a 

polyphasic approach to find characters that differentiate species and to establish accurate data on potential mycotoxin 

production by each species. Phylogenetic analysis of the ITS region, parts of the β-tubulin and calmodulin 

genes, macro- and micromorphological examinations and analysis of extrolite profiles were applied. Phylogenetic 

analyses revealed that the genus Byssochlamys includes nine species, five of which form a teleomorph, i.e. B. fulva, 

B. lagunculariae, B. nivea, B. spectabilis and B. zollerniae, while four are asexual, namely P. brunneolus, P. divaricatus, 

P. formosus and P. saturatus. Among these, B. nivea produces the mycotoxins patulin and byssochlamic 

acid and the immunosuppressant mycophenolic acid. Byssochlamys lagunculariae produces byssochlamic acid 

and mycophenolic acid and thus chemically resembles B. nivea. Some strains of P. saturatus produce patulin and 

brefeldin A, while B. spectabilis (anamorph P. variotii s.s.) produces viriditoxin. Some micro- and macromorphological 

characters are valuable for identification purposes, including the shape and size of conidia and ascospores, 

presence and ornamentation of chlamydospores, growth rates on MEA and CYA and acid production on CREA. 

A dichotomous key is provided for species identification based on phenotypical characters. 

Article info Received: 4 October 2008; Accepted: 21 January 2009; Published: 10 February 2009. 

Introduction 

Byssochlamys species produce ascospores which are heatresistant, 

and survive considerable periods of heat above 85 °C 

(Beuchat & Rice 1979, Splittstoesser 1987). In addition to their 

heat resistance, Byssochlamys species can grow under very 

low oxygen tensions (Taniwaki 1995) and can form pectinolytic 

enzymes. The combination of these three physiological 

characteristics makes Byssochlamys species very important 

spoilage fungi in pasteurised and canned fruit. Byssochlamys 

has a Paecilomyces anamorph and the genus was revised by 

Stolk & Samson (1971). Samson (1974) accepted three Byssochlamys 

species: B. fulva, B. nivea and B. zollerniae with similar 

Paecilomyces anamorphs. Since then only B. verrucosa has 

been added to this genus (Samson & Tansey 1975). 

Paecilomyces was erected by Bainier (1907) to accommodate 

a single species, P. variotii, but many species were added 

(Brown & Smith 1957, Samson 1974). Luangsa-ard et al. 

(2004) presented a phylogenetic analysis of the 18S rDNA, 

demonstrating that Paecilomyces is polyphyletic across the 

Sordariomycetidae and Eurotiomycetidae. The type species 

P. variotii is a morphologically variable taxon, and has been redescribed 

under a variety of names broadening its circumscription. 

Thom (1930) and Samson (1974) mentioned the diversity 

in conidial shape and size, and Thom made a tentative division 

based on conidial size. 

Paecilomyces variotii and anamorphs of Byssochlamys species 

share several micromorphological characters, including 

phialides with cylindrical bases that taper abruptly into long 

1 

CBS Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD, Utrecht, The 

Netherlands; corresponding author e-mail: r.samson@cbs.knaw.nl. 

2 

Department of Microbiology, Faculty of Science and Informatics, University 

of Szeged, 6726 Szeged, Közép fasor 52, Hungary. 

3 

Centre for Microbial Biotechnology, Department of Systems Biology, Technical 

University of Denmark, 2800 Kgs. Lyngby, Denmark. 

cylindrical necks and produce catenate conidia. Some characters 

are constant at the species level, but vary among species. 

Houbraken et al. (2006) demonstrated that Byssochlamys and 

its associated anamorph species can be separated into at 

least nine taxa by investigating the micro- and macroscopical 

characteristics of Byssochlamys and Paecilomyces variotii-like 

isolates. In this study, we have extended this to a polyphasic 

approach by adding molecular and extrolite data and present a 

revised taxonomy and nomenclature of the accepted taxa. 

MaterialS and Methods 

Strains of Byssochlamys and Paecilomyces used in this study 

are listed in Table 1, and are preserved in the Fungal Biodiversity 

Centre (CBS), Utrecht, the Netherlands. 

DNA extraction, sequencing and analysis 

Total fungal genomic DNA was isolated using FastDNA ® Kit (Bio 

101, Carlsbad, USA) according to the manufacturer’s instructions. 

Amplification and sequencing of the ITS region (including 

internal transcribed spacer regions 1 and 2, and the 5.8S rRNA 

regions of the nuclear ribosomal RNA gene cluster), and parts 

of the β-tubulin and calmodulin genes were performed as described 

by Houbraken et al. (2007). Contigs were assembled 

from the forward and reverse sequences with the software 

package SeqMan from the Lasergene package (DNASTAR Inc., 

Madison, WI). The alignments of the sequence datasets were 

performed using Clustal W in MEGA 3.1 (Thompson et al. 1994, 

Kumar et al. 2004) and were, when necessary, adjusted by eye. 

Phylogenetic analyses of alignments were done using PAUP v. 

4.0b10 (Swofford 2000). Alignment gaps were treated as fifth 

character state, missing data were identified by ‘?’, uninformative 

characters were excluded and all characters were unordered 

and of equal weight. Maximum parsimony analysis was 

performed for all datasets using the heuristic search option. The 

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R.A. Samson et al.: Polyphasic taxonomy of Byssochlamys 

15 

Table 1 Byssochlamys and Paecilomyces isolates examined in this study. 

Species Accession No. Source and notes 

B. fulva CBS 132.33 Bottled fruit, UK; ex-type of Paecilomyces fulvus 

CBS 146.48 T 

Bottled fruit, UK 

CBS 135.62 

Fruit juice, Switzerland; ex-type of Paecilomyces todicus 

CBS 604.71 

Unknown source 

CBS 113954 Unknown source, patulin producer acc. to Rice et al. (1977) 

B. lagunculariae CBS 373.70 T Wood of Laguncularia racemosa (Mangue), Brazil 

CBS 696.95 

Pasteurized strawberries, the Netherlands 

CBS 110378 

Unknown source, France 

B. nivea CBS 100.11 T Unknown source 

CBS 133.37 

Milk of cow, USA; ex-type of Arachniotus trisporus 

CBS 271.95 

Mushroom bed, China 

CBS 102192 

Pasteurized drink yoghurt, Belgium 

CBS 113245 

Pasteurized fruit juice, Switzerland 

B. spectabilis CBS 338.51 Fruit juice, Switzerland 

CBS 102.74 

Unknown source; ex-type of Paecilomyces variotii 

CBS 101075 T 

Heat processed fruit beverage, Japan 

CBS 121581 

Spoiled sweetened tea, USA 

B. verrucosa CBS 605.74 T Nesting material of Leipoa ocellata, Australia 

B. zollerniae CBS 374.70 T Wood of Zollernia ilicifolia and Protium heptaphyllum, Brazil 

P. brunneolus CBS 370.70 T Non fat dry milk, Canada 

P. divaricatus CBS 284.48 T Mucilage bottle with library paste, USA 

CBS 110429 

Pectin, Mexico 

P. formosus CBS 628.66 Quebracho-tanned sheep leather, France 

CBS 371.70 

Annona squamosa, Brazil; ex-type of Paecilomyces maximus 

CBS 990.73B T 

Unknown source 

CBS 296.93 

Man, bone marrow of patient, Uzbekistan 

CBS 113247 

Soil, Thailand 

CBS 372.70 

Lecythis unsitata (Lecythidaceae), wood, Brazil; ex-type strain of P. lecythidis 

P. saturatus CBS 323.34 T Unknown source; ex-type of Paecilomyces mandshuricus var. saturatus 

CBS 368.70 

Medicine containing quinine, UK 

CBS 251.55 T 

Acetic acid, Brazil; ex-type of P. dactylomorphys 

CBS 990.73A 

Unknown source; ex-type of Penicillium viniferum 

CBS 492.84 

Lepidium sativum, Denmark 

Talaromyces byssochlamydoides CBS 413.71 T Dry soil under Pseudotsuga menziesii, USA 

Talaromyces emersonii CBS 393.64 T Compost, Italy 

Thermoascus crustaceus CBS 181.67 T Parthenium argentatum (Compositae), decaying plant, USA 

robustness of the most parsimonious trees was evaluated with 

1 000 bootstrap replications (Hillis & Bull 1993). Other statistics, 

including tree length, consistency index, retention index and 

rescaled consistency index (CI, RI and RC) were calculated. 

Monascus pilosus (GenBank accession AY629427) was used 

as an outgroup in the analyses of the ITS dataset; Thermoascus 

crustaceus was used as an outgroup for the β-tubulin and calmodulin 

data. Newly generated sequences were deposited in 

GenBank with accession numbers FJ389920–FJ390009. The 

alignments generated and the most parsimonious trees were 

deposited in TreeBase under accession numbers S2199 and 

M4168–M4170. 

Morphological characterisation 

The media used for macro-morphological examination included 

Czapek yeast autolysate (CYA) agar, malt extract autolysate 

(MEA) agar, yeast extract sucrose (YES) agar and creatinesucrose 

(CREA) agar (media compositions were according to 

Samson et al. 2004). Isolates were incubated at 25, 30 and 

37 °C. Micromorphological characterisation of the asexual 

Paecilomyces state was carried out on MEA, hay agar (HAY) 

and YES agars. The latter was exclusively used to determine 

the presence of chlamydospores. For the analyses of the features 

of the sexual Byssochlamys state, the media oatmeal 

agar (OA) and potato-dextrose agar (PDA) were used (for 

media formulations, see Samson et al. 2004). The surfaces 

of conidia, chlamydospores and ascospores were examined 

after prolonged incubation (up to 70 d). Conditions and media 

for measuring the microaerophily, growth on 0.5 % acetic acid 

and the resistance to propionic acid are described by Frisvad 

& Samson (2004). 

Extrolite analysis 

Strains studied (Table 1) were three-point inoculated on MEA, 

YES, PDA, OA and CYA agars. All isolates were analysed for 

extrolite metabolites after 2 wk growth at 30 °C. The cultures 

were extracted according the method of Smedsgaard (1997) 

and analysed with high performance liquid chromatography 

(HPLC) with diode array detection (DAD) (Frisvad & Thrane 

1987, 1993). The metabolites found were compared with a 

spectral UV library derived from authentic standards, including 

patulin, viriditoxin, mycophenolic acid, byssochlamic acid and 

physcion, using the same conditions (the maximum similarity 

is a match of 1 000). The retention indices were compared with 

those of standards. 

Results 

DNA sequencing 

The trees constructed by maximum parsimony analysis of the 

datasets of the protein coding genes β-tubulin and calmodulin 

and the ITS region exhibited similar topologies (Fig. 1–3). 

Molecular analyses revealed that in the genus Byssochlamys 

nine taxa can be recognised. Five taxa form a teleomorph, 

namely B. fulva, B. lagunculariae, B. nivea, B. spectabilis and 

B. zollerniae, while four are strictly anamorphic, i.e. P. brunneolus, 

P. divaricatus, P. formosus and P. saturatus. Analyses 

of the ITS showed that B. verrucosa is not a member of the 

genus Byssochlamys and is related to Thermoascus (Fig. 1). 

This was also confirmed by analyses of the partial β-tubulin 

and calmodulin sequence data (data not shown). 

The basal nodes were also similar for all three parsimony 

trees (Fig. 1–3). Byssochlamys nivea and B. fulva were sister

16 Persoonia – Volume 22, 2009 

1 

ITS 

CBS 289.34 Monascus pilosus AY629427 

CBS 374.70 B. zollerniae 

90 CBS 371.70 P. formosus 

79 CBS 113247 P. formosus 


99 

CBS 628.66 P. formosus 


86 

CBS 990.73B P. formosus 

CBS 370.70 P. brunneolus 

100 

CBS 121581 B. spectabilis/ P. variotii 

99 

CBS 338.51 B. spectabilis / P. variotii 

73 CBS 102.74 B. spectabilis / P. variotii 

CBS 101075 B. spectabilis / P. variotii 

CBS 100.11 B. nivea 


CBS 113245 B. nivea 


74 CBS 606.71 B. nivea 

CBS 132.33 B. fulva 



80 NRRL 32567 B. fulva 

100 

CBS 135 62 B. fulva 

CBS 373.70 B. lagunculariae 


89 CBS 110378 B. lagunculariae 

CBS 251.55 P. saturatus 


67 



CBS 990.73A P. saturatus 

100 CBS 284.48 P. divaricatus 

CBS 110429 P. divaricatus 

99 CBS 393.64 Talaromyces emersonii 

71 

CBS 413.71 Talaromyces byssochlamydoides 

100 CBS 605.74 Byssochlamys verrucosa 

CBS 181.67 Thermoascus crustaceus 

100 

99 



100 CBS 606.71 B. nivea 



94 



NRRL 32567 B. fulva 



Calmodulin 



100 



99 CBS 323.34 P. saturatus 


99 CBS 696.95 B. lagunculariae 

CBS 110378 B. lagunculariae 


100CBS 296.93 P. formosus 


88 


98 

100 

CBS 113247 P. formosus 


100 




96 CBS 121581 B. spectabilis / P. variotii 

99 CBS 101075 B. spectabilis / P. variotii 

Fig. 1 One of three equally parsimonious trees of the analysed ITS region 

(55 of the 629 characters were parsimony informative; tree length = 294, 

CI = 0.738, RI = 0.855, RC = 0.631, HI = 0.262). 

100 


CBS 284.48 P. divaricatus 


10 


species, as were B. lagunculariae and P. saturatus. These 

four species form a distinct clade (group I). Byssochlamys 

spectabilis and P. brunneolus also clustered together and form, 

together with P. formosus, another distinct clade in Byssochlamys 

(group II). Paecilomyces divaricatus was basal to 

these groups in all analyses, while the position of the single 

strain of B. zollerniae varied. Partial β-tubulin data showed that 

B. zollerniae is related to group I with a high bootstrap support 

(92 %; Fig. 3). The partial calmodulin data also showed that 

B. zollerniae is related to group I (Fig. 2), while analyses of the 

ITS regions revealed that it is more related to group II (Fig. 1), 

but its placement was supported only by low bootstrap values 

on these trees (Fig. 1, 2). 

Morphological characterisation 

The genus Byssochlamys is morphologically well-defined and 

characterised by almost naked ascomata in which croziers 

and globose asci are formed with ellipsoidal ascospores. The 

ascomatal initials consist of swollen antheridia and coiled 

ascogonia. All Byssochlamys species have a Paecilomyces 

anamorph. The Byssochlamys anamorphs belong to Paecilomyces 

sect. Paecilomyces, containing mesophilic, thermotolerant 

and thermophilic species (Samson 1974). As discussed by 

Fig. 2 One of eight equally parsimonious trees of the analysed partial 

calmodulin gene sequences (204 of the 607 characters were parsimony informative; 

tree length = 328, CI = 0.708, RI = 0.889, RC = 0.630, HI = 0.292). 

Luangsa-ard et al. (2005), other species previously classified in 

Paecilomyces sect. Isarioidea are now mainly accommodated 

in Isaria or newly described genera. 

Various microscopic characters are valuable for identification 

purposes, including the shape and sizes of conidia and ascospores, 

and presence and ornamentation of chlamydospores. 

Useful macroscopical features are growth rates on MEA and 

CYA, and acid production on CREA. An overview of various 

macro- and microscopical features is presented in Table 2. The 

ratio between the colony diameters on MEA incubated at 30 °C 

or 37 °C is also diagnostic. 

Extrolite analysis 

The extrolite profiles of the taxa are listed in Table 3. Most 

strains of B. fulva produced byssochlamic acid, but B. fulva 

could be subdivided into two chemically different groups: one 

group of isolates produced meriditin (a compound produced by 

Eupenicillium meridianum) and a peptide with a cycloaspeptide


17 

10 

100 

100 

99 

100 

83 

92 

100 

100 









CBS 113954 B. fulva 





100 




98 


92 

78 CBS 113247 P. formosus 


100 







100 



CBS 284.48 P. divaricatus 


98 CBS 251.55 P. saturatus 


100 

CBS 110378 B. lagunculariae 


β-tubulin 

Fig. 3 One of 36 equally parsimonious trees of the analysed partial β-tubulin 

gene sequences (156 of the 494 characters were parsimony informative; tree 

length = 304, CI = 0.704, RI = 0.913, RC = 0.643, HI = 0.296). 

chromophore (CBS 132.33, CBS 135.62 and CBS 604.71), 

while the other group produced a series of alkaloids, some 

with UV spectra similar to that of paspaline (named ‘OLK’ in 

Table 2) and some with verrucologen-like UV spectra (called 

‘URT’ in Table 2) (CBS 113225, CBS 113246, CBS 113954 and 

TM 03.048). The ex-type culture of B. fulva was deteriorated 

and only produced byssochlamic acid, and none of the other 

mentioned extrolites. 

Some strains of B. nivea produced the full profile of extrolites: 

patulin, mycophenolic acid, byssochlamic acid and metabolite 

‘OLK’ (CBS 900.70, CBS 271.95 and CBS 102192). Mycophenolic 

acid, patulin and byssochlamic acid and some of their 

precursors were also found by Puel et al. (2005). Byssochlamys 

lagunculariae produces the same overall extrolite profile as 

B. nivea, except that patulin has not been detected in the 

former species. Byssochlamys spectabilis and isolates with 

only anamorphs (P. variotii) consistently produced viriditoxin, 

which was earlier reported from an isolate identified as Spicaria 

divaricata (Jiu & Mizuba 1974). Other unique extrolites were 

also produced but the structures of these have not yet been 

elucidated. 

Table 2 Production of extrolites by Byssochlamys and Paecilomyces 

species 1 . 

Species 

All strains of P. divaricatus produced anthraquinones including 

emodin. However CBS 110429 only produced another type of 

anthraquinone, CBS 110428 and CBS 110430 produced ascofuranone. 

Only the ex-type culture of B. zollerniae was available 

for study and some unique unknown extrolites were found in this 

isolate. In this study, we could not confirm viriditoxin production 

in P. divaricatus and assume that the strain studied by Jiu & 

Mizuba (1974) was probably a B. spectabilis isolate. 

Our phylogenetic analysis showed that B. verrucosa is related to 

Thermoascus. Byssochlamys verrucosa produced cornexistin 

and/or byssochlamic acid, and also some specific unidentified 

extrolites only seen in this species. Thermoascus aurantiacus 

also produces compounds with chromophores (UV spectra) 

consistent with cornexistin, byssochlamic acid or similar tropolones 

(Frisvad unpubl. data). The production of cornexistin and 

byssochlamic acid demonstrates that the species chemically resemble 

B. fulva, B. laguncularia, B. nivea and P. divaricatus. 

Paecilomyces saturatus is chemically somewhat diverse. Group I 

produced at least one of the following extrolites: patulin, mycophenolic 

acid and a compound which chemically resembles 

aspergillic acid (CBS 251.55 T , CBS 223.52, CBS 492.84 and 

IBT 21716), while group II produced brefeldin A (CBS 323.34 T 

and CBS 990.73A) and may fit with P. mandshuricus var. saturatus. 

Paecilomyces formosus consistently produced variotin 

and related compounds, except CBS 296.93, which may be 

chemically close to P. saturatus (group I). 

Discussion 

Extrolites 

B. fulva Group I: byssochlamic acid, meriditin, ‘cycloaspeptide-like 

compound’ 

Group II: byssochlamic acid, ‘OLK’, ‘URT’ 

B. lagunculariae Byssochlamic acid, mycophenolic acid, ‘OLK’ 

B. nivea Byssochlamic acid, mycophenolic acid, patulin, ‘OLK’ 

B. spectabilis Viriditoxin and other compounds with characteristic UV 

spectra 

B. verrucosa Cornexistin and/or byssochlamic acid 

B. zollerniae No known extrolites, though several compounds characterized 

by a characteristic UV spectrum are present 

P. brunneolus ‘Ascofuranone-like compound’, ‘tetracycline-like compounds’ 

P. divaricatus Cornexistin and/or byssochlamic acid, ascofuranone, emodin 

and other anthraquinones 

P. formosus Variotin 

P. saturatus Group I: patulin, mycophenolic acid or ‘aspergillic acid-like 

compound’ 

Group II: brefeldin A 

1 

Byssochlamic acid, mycophenolic acid, patulin, and viriditoxin were available as authentic 

standards. Evidence for production of ascofuranone, cornexistin, meriditin and variotin is 

based on similar UV spectra as those reported in the literature, and their occurrence in 

species already known to produce them. Metabolites in inverted commas have UV spectra 

that indicate a chemical relationship to the compounds mentioned. For example the ‘tetracycline-like 

compounds’ in P. brunneolus have UV spectra similar to those of tetracycline and 

viridicatumtoxin. ‘OLK’ and ‘URT’ are apolar indole-terpene compounds, but the chemical 

structure is as yet unknown. ‘OLK’ has a paspaline UV spectrum. 

Byssochlamys isolates were included in this study to verify the 

connection between the anamorphic P. variotii complex and 

holomorphic Byssochlamys species. The genus Paecilomyces 

was monographed by Samson (1974) who recognised 31 species 

divided into two sections, Paecilomyces and Isarioidea. 

However, the phylogenetic analysis of the 18S rDNA demonstrates 

that Paecilomyces is polyphyletic across two subclasses, 

Sordariomycetidae and Eurotiomycetidae (Luangsa-ard et al. 

2004).


Table 3 Macro-and microscopical features of Byssochlamys and Paecilomyces isolates. 

Species Conidial length (µm) Conidial shape (predominant) Chlamydospores Ascospore length (µm) Ascospore Colony diam. Degree of Acid proornamentation 

(mm) on CYA growth on CYA duction 

7 d, 30 °C 7 d, 30 °C on CREA 

7 d, 30 °C 

B. fulva 3.7–7.5 × 1.4–2.5 Cylindrical with truncate ends Absent; in some isolates after prolonged 5.3–7.1 × 3.3–4.3 Smooth 50–90 Good + 

incubation present (40 d) 

B. lagunculariae 2.7–4.5 × 2.2–3.3 Globose with flattened base Present, smooth 3.8–5 × 3–3.9 Smooth 45–55 Good – 

B. nivea 3–4.7 × 2.3–4 Globose to ellipsoidal with flattened base Present, smooth to finely rough 4.1–5.5 × 2.9–3.9 Smooth (8–)28–50 Weak – (+) 

B. spectabilis 3.3–6.1 × 1.5–4.4 Predominantly ellipsoidal and ellipsoidal Present, smooth to finely rough 5.2–6.8 × 3.5–4.5 Almost smooth, 30 – 45(– 55) Good – 

with truncate ends slightly roughened 

B. verrucosa 6.3–13.1 × 1.6–4.7 Cylindrical with truncate ends Absent 6.6–8.4 × 4–6.1 Rough 25–40 Good – 

B. zollerniae 2.5–4 × 1.5–3 Globose to ellipsoidal, apiculate Present, warted 3–4.5 × 2.5–3 Smooth 30–35 Weak – 

P. brunneolus 3.7–5.5 × 1.8–3.4 Ellipsoid to broadly cylindrical with truncate ends Present, smooth No ascospores detected Not relevant 20–30 Good – 

P. divaricatus 3.2–4.6 × 1.6–2.5 Ellipsoidal to cylindrical with truncate ends Absent; in some isolates after prolonged 5.3–7 × 3.8–4.9, smooth 10–17 Moderate – 

incubation present (40 d) rarely produced 

P. formosus 3–10 × 1.8–3.5 Ellipsoidal to cylindrical with truncate ends Present, smooth and often pigmented No ascospores detected Not relevant 18–90 Good + 

P. saturatus 2.3–7 × 1.7–3.4 Predominantly cylindrical and ellipsoidal Present, smooth No ascospores detected No ascospores 22–55 Good – 

without truncate ends detected 

Therefore, Paecilomyces is only monophyletic within the order 

Eurotiales and characterised by a Byssochlamys teleomorph. 

In the present study the P. variotii complex could be divided 

into four species, P. divaricatus, P. formosus, P. saturatus and 

P. variotii. 

Udagawa & Suzuki (1994) described Talaromyces spectabilis, 

but phylogenetic analysis of the 18S rDNA clarified that this species 

belongs to the genus Byssochlamys (Luangsa-ard et al. 

2004). Recently, Houbraken et al. (2008) showed that this 

species is heterothallic and that it is linked to the anamorphic 

species P. variotii. This was confirmed in the present study by 

morphological features and extrolite data. The presence of a 

teleomorph with heat-resistant ascospores for P. variotii explains 

the ability of this fungus to spoil heat treated fruit juices 

(Piecková & Samson 2000). 

Short descriptions of B. lagunculariae, B. spectabilis, P. brunneolus, 

P. divaricatus, P. formosus and P. saturatus are presented. 

The concepts of B. fulva, B. nivea and B. zollerniae are 

unchanged since the descriptions by Stolk & Samson (1971), 

with the remark that B. nivea var. langunculariae is elevated to 

species level. Byssochlamys verrucosa is not discussed here, 

because the taxon probably belongs to Thermoascus; it was 

fully described by Samson & Tansey (1975). Microscopic dimensions 

and cultural characters are summarised in Table 3. 

Discussion of accepted taxa 

Byssochlamys lagunculariae (C. Ram) Samson, Houbraken 

& Frisvad, comb. nov. — MycoBank MB512557; Fig. 4a–f 

Basionym. Byssochlamys nivea Westling var. lagunculariae C. Ram, 

Nova Hedwigia 16: 311. 1968. 

Byssochlamys lagunculariae strains grow fast on MEA, covering 

the dish within 7 d at 30 °C. Depending on the isolate, it 

predominantly forms conidia (CBS 373.70 T ) or ascomata (CBS 

696.95). Colonies 25–55 mm on MEA at 37 °C after 7 d of 

incubation. Growth occurs under microaerophilic conditions, in 

the presence of 0.5 % acetic acid or 1 000 ppm propionic acid 

(pH 3.8). No growth is observed on CYA with 5 % NaCl. Poor 

growth and no acid production on CREA. 

Morphologically, B. lagunculariae is similar to B. nivea and 

shares various characters such as fast growth rate on MEA at 

30 °C and globose (to ellipsoidal) conidia with a flattened base. 

Chlamydospores are present, uncoloured and smooth-walled. 

Though similar in shape to those of B. nivea, the conidia and 

ascospores of B. lagunculariae are generally smaller in size. 

Another difference is that B. lagunculariae grows well on CYA 

while B. nivea grows rather poorly. 

Our molecular studies and morphological examinations both 

revealed that B. lagunculariae is clearly distinct from B. nivea. 

In the original description by Ram (1968), B. lagunculariae was 

described as a variety of B. nivea, distinguished by its smaller 

conidia and ascospores. Stolk & Samson (1971) synonymised 

it with B. nivea, but the present study showed that the growth 

rate on CYA, and smaller conidial and ascospore sizes are 

constant characters that can be used to differentiate between 

these species. 

This species produces a similar range of extrolites to B. nivea, 

but patulin has not been detected in B. lagunculariae. Differentiation 

between B. nivea and B. lagunculariae, based on 

extrolite profiles, is not possible. 

The ex-type culture was isolated from wood of Laguncularia 

racemosa (mangue) in Brazil and other strains identified as 

this species were found in soil, and pasteurised strawberries 

and aloe juice. The occurrence of this species in heat treated 

products makes it an important food spoilage organism.


19 

a 

b 

c 

d 

e 

f 

i 

g 

h 

Fig. 4 Byssochlamys lagunculariae. a–d. Conidiophores; e. conidia; f. asci and ascospores. — Byssochlamys zollerniae. g, h. Phialides; i. chlamydospores; 

j. conidia. — Scale bars = 10 µm. 

j


a 

b 

c 

d 

e 

f 

g h i 

Fig. 5 Byssochlamys spectabilis. a–e. Conidiophores; f. conidia; g. ascomata; h, i. asci and ascospores. — Scale bars = 10 µm.


21 

Byssochlamys spectabilis (Udagawa & Shoji Suzuki) Houbraken 

& Samson, Appl. Environm. Microbiol. 74: 1618. 

2008. — Fig. 5 

Basionym. Talaromyces spectabilis Udagawa & Shoji Suzuki, Mycotaxon 

50: 82. 1994. 

Anamorph. Paecilomyces variotii Bainier, Bull. Trimestriel Soc. Mycol. 

France 23: 26. 1907. 

≡ Penicillium variotii (Bainier) Sacc., Syll. Fung. 22: 1273. 1913. 

Colonies spreading rapidly on MEA at 30 °C and covering the 

Petri dish within 7 d. Similar or higher growth rate at 37 °C 

than at 30 °C. Good growth under microaerophilic conditions, 

on MEA with 0.5 % acetic acid and on CYA with 1 000 ppm 

propionic acid (pH 3.8). No or weak growth on CYA with 5 % 

NaCl (0–10 mm). Since B. spectabilis forms its ascospores in 

a heterothallic manner, only the anamorph is usually produced. 

The conidiophores are irregularly branched and ellipsoidal 

and/or cylindrical; truncate conidia are formed, which are often 

pale yellow brown. Chlamydospores present, smooth-walled, 

in some isolates finely roughened. Often broad, thick-walled 

hyphae are present in fresh isolates. Ascospores are formed 

when strains of opposite mating types are grown together. 

Our recent study (Houbraken et al. 2008) showed that strains 

originating from heat treated products are mostly frequently 

capable of producing fertile progeny. The ascospores are ellipsoidal, 

smooth to finely roughened, 5.5–6.5 × 3.5–4.5 µm. 

Colonies on MEA agar growing rapidly, attaining a diameter of 

7 cm within 7 d at 30 °C. Poor growth and no acid production 

on CREA. 

The extrolite viriditoxin was produced by all investigated isolates. 

Whether this extrolite is also produced in foodstuffs is 

unknown. 

Byssochlamys spectabilis commonly occurs in air, compost, 

infected humans and various foodstuffs (including pasteurised 

fruit juices, rye bread). It is frequently found in heat treated products, 

although after isolation only the anamorph is produced. 

Paecilomyces brunneolus (N. Inagaki) Samson & Houbraken, 

comb. nov. — MycoBank MB512559; Fig. 6g–i 

Basionym. Paecilomyces variotii Bainier var. brunneolus N. Inagaki, Trans. 

Mycol. Soc. Japan 4: 4. 1962. 

The type strain of P. brunneolus on MEA in 7 d forms colonies 

of 35–45 mm diam (30 °C) with well-defined margins. Colonies 

on MEA 20–30 mm diam in 7 d at 37 °C. Growth occurs 

under microaerophilic conditions and in the presence of 0.5 % 

acetic acid or 1 000 ppm propionic acid (pH 3.8). No growth 

is observed on CYA with 5 % NaCl. Poor growth and no acid 

production on CREA. Microscopical examination showed 

short, irregular branched conidiophores (2–3 × 15–25 µm). 

Conidia ellipsoidal to broadly cylindrical with truncate ends 

(1.5–)2–3(–3.5) × (3.5–)4–5(–5.5) µm. Chlamydospores 

present, smooth and hyaline. 

Paecilomyces brunneolus is only known from its type culture, 

CBS 370.70. Analyses of a part of the β-tubulin, calmodulin 

gene and the ITS regions showed that this strain is closely 

related to B. spectabilis (P. variotii). However, extrolites and 

morphological data support that this is a distinct species. Viriditoxin 

is consistently produced by B. spectabilis, while P. brunneolus 

produces an ascofuranone like compound and tetracyclic 

compounds. Paecilomyces brunneolus colonies are more 

restricted than strains of B. spectabilis (P. variotii) on MEA. 

Another difference is that the growth rate of P. brunneolus at 

37 °C is slower than at 30 °C, while this is the opposite for 

B. spectabilis. 

This species has only been isolated from non-fat, dry milk from 

Canada in the 1960s. 

Paecilomyces divaricatus (Thom) Samson, Houbraken & 

Frisvad, comb. nov. — MycoBank MB512561; Fig. 6a–f 

Basiomym. Penicillium divaricatum Thom, Bull. Bur. Anim. Ind. U.S. Dep. 

Agric. 118: 92. 1910. 

≡ Spicaria divaricata (Thom) J.C. Gilman & E.C. Abbott, Iowa State Coll. 

J. Sci. 1: 301. 1929. 

≡ Spicaria divaricata (Thom) R.M. Ma, Lingnan Sci. J. (Suppl.) 12: 115. 

1933. 

The growth rate of P. divaricatus on MEA is restricted, compared 

with other members of the investigated Byssochlamys clade, 

and colonies of 30–40 mm are attained after 7 d of incubation at 

30 °C. Only P. brunneolus has colony diameters of comparable 

size. Grows at 37 °C, although slower at 30 °C. Weak growth 

and no acid production on CREA. Paecilomyces divaricatus is 

characterised by its ellipsoidal to cylindrical, truncate conidia, 

measuring 3.5–4.5 × 1.5–2 µm and the absence of chlamydospores. 

Ascomata absent on agar media, though ascomatal 

initials, arising as coils, can be observed. Smooth ellipsoidal 

ascospores were once observed in a fresh isolate (5.3–7 × 

3.8–4.9 µm) but have not been seen since. 

Anthraquinones including emodin are produced by all investigated 

isolates. The production and presence of emodin, a 

genotoxic and diarrheagenic mycotoxin, in foods and feeds 

is unknown. 

Thom (1910) described the species Penicillium divaricatum 

but placed this species later in synonymy with P. variotii (Thom 

1930). We examined the ex-type isolate and conclude that 

P. divaricatus is a distinct species. Microscopical analyses of 

the original type isolate (CBS 284.48) showed a few structures 

resembling ascoma initials. Using a heat treatment, strains of 

P. divaricatus could be isolated from various food products. The 

survival of a heat treatment suggests the presence of a Byssochlamys 

teleomorph (ascospores), and many Byssochlamys 

initials were present (croziers) in these strains; however, no 

ascomata were detected even after prolonged incubation. 

This species was isolated from a bottle with mucilage library 

paste, heat treated pectin and fruit concentrates. Its presence 

in heat treated products and the absence of thick-walled 

chlamydospores, suggests that this species is able to form heat 

resistant ascospores. 

Paecilomyces formosus (Sakag., May. Inoue & Tada) Houbraken 

& Samson, comb. nov. — MycoBank MB512562; 

Fig. 7g–i 

Basionym. Monilia formosa Sakag., May. Inoue & Tada, Zentralbl. Bakteriol., 

2. Abt. 100: 302. 1939. 

= Paecilomyces maximus C. Ram, Nova Hedwigia 16: 306. 1968. 

= Paecilomyces lecythidis C. Ram (as lecythisii), Nova Hedwigia 16: 307. 

1968. 

Fast growth on MEA at 30 °C and covering the dish within 7 d. 

Ratio between growth rates at 30 and 37 °C variable; most 

strains have slower or similar growth rates (< 1), though CBS 

371.70 (ex-type strain of P. maximus) and CBS 113247 are 

exceptions and have a faster growth rate at 37 °C. Growth on 

MEA with 0.5 % acetic acid varying from absence of growth to 

more than 80 mm after 1 wk of incubation. Variable growth patterns 

on CYA with 5 % NaCl, 0–25 mm. All investigated strains 

have poor growth on CREA and acid production under colonies. 

Conidiophores irregularly branched, with olive-brown conidia. 

Chlamydospores present (often on small stalks), smooth walled, 

globose and (weakly) pigmented. The conidia of this species 

are variable, varying from ellipsoidal to cylindrical; all with 

truncate ends. In some isolates conidial shape might vary from 

ellipsoidal to cylindrical.


a 

b 

c 

d 

e 

f 

g h i 

Fig. 6 Paecilomyces divaricatus. a–c. Conidiophores; d. conidia; e. ascoma initials; f. ascospores. — Paecilomyces brunneolus. g, h. Conidiophores; 

i. conidia. — Scale bars = 10 µm.


23 

a 

b 

c 

d 

e 

f 

g h i 

Fig. 7 Paecilomyces saturatus. a–e. Conidiophores; f. conidia. — Paecilomyces formosus. g, h. Conidiophores; i. conidia. — Scale bars = 10 µm.


Ram (1968) described two Paecilomyces species, P. lecythidis 

and P. maximus, based on their cultural characters and their 

large-sized conidia. 

The results of the sequencing of the ITS region, and parts of 

the protein coding genes β-tubulin and calmodulin, showed that 

P. formosus may consist of three taxa, P. formosus, P. lecythidis 

and P. maximus. However, the three species could not be 

distinguished by microscopical examination. One difference 

between strains belonging to the ‘P. maximus-clade’ and the 

other members of this diverse group, is the faster growth rate 

of this species at 37 °C than at 30 °C. The sequence and morphological 

diversity was not detected by the extrolite analyses: 

the ex-type cultures of P. lecythidis and P. maximus produced 

similar extrolite profiles, while the ex-type culture of P. formosus 

is degenerated and is a weak producer of extrolites. 

For a more detailed conclusion and delimitation of these three 

groups more strains should be studied, particularly emphasising 

conidial shape and extrolites production. For the time being 

we propose to place P. lecythidis and P. maximus in synonymy 

with P. formosus. 

This species is morphologically similar to P. variotii and the main 

difference is the consistent acid production on CREA. 

Paecilomyces formosus has been isolated from tropical and 

subtropical soils, wood, sponge, man (bone marrow, blood), 

air in a bedroom (Denmark) and pot plant soil of Senseviera 

trifasciata (Denmark). 

Paecilomyces saturatus (Nakaz., Y. Takeda & Suematsu) 

Samson & Houbraken, comb. nov. — MycoBank MB512560; 

Fig. 7a–f 

Basionym. Paecilomyces mandshuricus (Saito) Thom var. saturatus 

Nakaz., Y. Takeda & Suematsu, J. Agric. Chem. Soc. Japan 10: 102. 1934. 

= Penicillium viniferum Sakag., May. Inoue & Tada, Zentralbl. Bakteriol., 

2. Abt. 100: 303. 1939. 

= Paecilomyces dactylethromorphus Bat. & H. Maia, Anais Soc. Biol. 

Pernambuco 15: 152. 1957. 

The oldest basionym available for this taxon is P. mandshuricus 

var. saturatus and therefore the name of this taxon is derived 

from this varietal name. 

Isolates growing on MEA at 30 °C cover the Petri dish within 

7 d, with strong olive-brown sporulation. Good growth at 37 °C, 

though slower at 30 °C. Good growth on MEA with 0.5 % acetic 

acid and CYA with 1 000 ppm propionic acid (pH 3.8). No 

growth observed on CYA with 5 % NaCl. Poor growth and no 

acid production on CREA. 

Morphological examination of various strains showed that this 

species forms fairly regularly branched, penicillium-like conidiophores, 

with ellipsoidal and/or cylindrical conidia without a distinct 

truncation. Chlamydospores present, hyaline and smooth 

walled. No teleomorph observed. 

The production of extrolites depends very much on the growth 

medium; patulin or brefeldin A can be produced. 

Paecilomyces saturatus is an easily recognisable species 

with its ellipsoidal and/or cylindrical conidia and its fairy regularly 

branched, penicillium-like conidiophores. Sakaguchi et al. 

(1939) described Penicillium viniferum and this species was 

subsequently placed in Paecilomyces by Raper & Thom (1949). 

In retrospect, the placement in Paecilomyces was correct, although 

this species could be interpreted, with its penicillium-like 

conidiophores and the presence of chlamydospores, as an intermediate 

form between Penicillium and Paecilomyces. Molecular 

studies now show that this species belongs to the Byssochlamys 

clade and is different from other olive-brown coloured species 

such as Hamigera avellanea (Luangsa-ard et al. 2004), Penicillium 

digitatum and P. cylindrosporum (unpubl. data). 

This species has been isolated from a variety of substrates, e.g. 

acetic acid, leather, medicine containing quinine, a dispersion 

of fenylacetate and dibutylmaleinate and Lepidium sativum. 

Notes on the ecology and extrolites production 

Byssochlamys and Paecilomyces species are often found 

in acidic habitats such as silage (Scurti et al. 1973, Escoula 

1975a, b, Anderson et al. 1979), and in common with Penicillium 

series Roqueforti species (Frisvad & Samson 2004) can also 

tolerate microaerophilic conditions (Escoula 1975a, b, Taniwaki 

1995). Byssochlamys nivea was initially reported to produce 

patulin under the name Gymnoascus sp. (Karow & Forster 

1944, Kuehn 1958), later confirmed by Kis et al. (1969), Scurti 

et al. (1973), Rice et al. (1977) and Draughon & Ayres (1980). 

Byssochlamys fulva was also reported to produce patulin, albeit 

by few strains (Escoula 1975a, b, Percebois et al. 1975, Rice et 

al. 1977). Besides their presence in pasteurised fruit, B. fulva 

and B. nivea also form toxic extrolites, such as byssotoxin A 

and byssochlamic acid (Kramer et al. 1976, Rice et al. 1977). 

Besides mycotoxins, also an antitumor metabolite, byssochlamysol, 

a steroid against IGF-1 dependent cancer cells, is 

produced by B. nivea (Mori et al. 2003). 

Paecilomyces variotii s.l. also produces mycotoxins (Scott 

1965), such as patulin (Escoula 1975a, b), sphingofungin E 

and F (Frommer et al. 1992) and viriditoxin, reported originally 

from an isolate named Spicaria divaricata (Jiu & Mizuba 1974). 

Apart from being reported as being a potential mycotoxin, 

viriditoxin has also been reported to be a candidate for treatment 

of antibiotic resistant bacteria (Wang et al. 2003). Among 

the known extrolites are the antifungal drug variotin (Takeuchi 

et al. 1959, 1964, Suzuki et al. 1990, Omolo et al. 2000), and 

other drug candidates such as cornexistins (Nakajima et al. 

1991, Fields et al. 1996), SCH 643432 (Hegde et al. 2003) 

and a penicillin-like compound (Burton 1949). The sideramins 

ferrirubrin and fusigen (Diekmann 1967, Domsch et al. 1980) 

and the organic acids 3-indole-acetic acid (Bakalinerov 1968, 

Voinova-Raikova et al. 1969), citric acid (Loesecke 1945), 

ethyleneoxide-α, β-dicarboxylic acid (Sakaguchi et al. 1939), 

(3Z,5E)-octa-3,5-diene -1,3,4-tricarboxylic acid 3,4-anhydride 

(Aldridge et al. 1980) have also been reported. The possible 

mycotoxins and/or potential drugs byssotoxin A, sphingofungin 

E and F, SCH 643432 and byssochlamysol were not available to 

us as standards. Given the taxonomic revision presented here, 

it remains to be seen which species produce these extrolites. 

Some connections between species and bioactive extrolites 

were confirmed or established here and several species had a 

high consistent extrolite profile. However, the chemotaxonomy 

of P. saturatus is unresolved, because there appear to be two 

chemotypes, which may or may not indicate that there are two 

species rather than one. Likewise, B. fulva appears to have 

two chemotypes, with only byssochlamic acid as a common 

extrolite in all isolates examined. 

Key to Byssochlamys and related 

PaecilomYces anamorphs* 

1. Conidia with conspicuously truncate ends or a flattened 

base . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 

1. Conidia ellipsoidal or cylindrical with inconspicuously truncate 

ends . . . . . . . . . . . . . . . . . . . . . . . . . . . . P. saturatus 

2. Conidia predominantly ellipsoidal and/or cylindrical chlamydospores 

absent or present; Byssochlamys teleomorph absent 

or present . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 

2. Conidia predominantly globose to subglobose, chlamydospores 

present; Byssochlamys teleomorph present . . . . 8


25 

a 

b 

c 

d 

e 

f 

g h i 

Fig. 8 Byssochlamys fulva. a. Conidiophores; b. conidia; c. asci and ascospores. — Byssochlamys nivea. d. Conidiophores; e. conidia; f. ascospores. — Byssochlamys 

verrucosa. g, h. Conidiophores and conidia; i. asci and ascospores. — Scale bars = 10 µm.


3. Conidia cylindrical and/or ellipsoidal; measuring 3.4–4.2 × 

1.7–2.1 µm, colonies on MEA restricted, attaining a diameter 

of less than 45 mm in 7 d at 30 °C . . . . . . . . . . . . . . . . . 4 

3. Conidia larger 2.3–8(–13) × 1.5–4.5 µm, cylindrical or ellipsoidal, 

colonies on MEA larger than 45 mm after 7 d at 

30 °C . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 

4. Chlamydospores present, ratio between diameters on MEA 

at 37:30 °C between 0.25 and 0.45, colonies with welldefined 

margins . . . . . . . . . . . . . . . . . . . . . . P. brunneolus 

4. Chlamydospores absent, ratio between diameters on MEA 

at 37:30 °C between 0.60 and 0.75, colonies with more or 

less feathery margins . . . . . . . . . . . . . . . . P. divaricatus** 

5. Conidia predominantly ellipsoidal with truncate ends, chlamydospores 

present . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 

5. Conidia predominantly cylindrical, chlamydospores absent 

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 

6. Conidia measuring 3.7–5.6 × 2.4–3.6 µm, no acid production 

on CREA; Byssochlamys teleomorph produced in a 

heterothallic manner . . . . . . . . . . . . . . . . . . B. spectabilis 

6. Conidia measuring 3.2–5.7(–10) × 2–2.9(–3.4) µm, acid 

production under colony on CREA; Byssochlamys teleomorph 

absent . . . . . . . . . . . . . . . . . . . . . . . . P. formosus 

7. Conidia measuring 4.5–6 × 1.7–2.2 µm; ascospores, smoothwalled, 

5.5–6.5 × 3.5–4.1 µm, acid production under colony 

on CREA . . . . . . . . . . . . . . . . . . . . . . B. fulva (Fig. 8a–c) 

7. Conidia measuring 9–11.8 × 2.5–4 µm; ascospores, verrucose 

and large, 7.1–8.1 × 5–5.7 µm, no acid production 

on CREA . . . . . . . . . . . . . . . . . . B. verrucosa (Fig. 8g–i)* 

8. Chlamydospores distinctly rough-walled . . . . . . . . . . . . . . 

. . . . . . . . . . . . . . . . . . . . . . . . . . . B. zollerniae (Fig. 4g–j) 

8. Chlamydospores smooth walled or finely roughened . . . 9 

9. Conidia measuring 3.1–3.8 × 2.5–3.2 µm, good growth on 

CYA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. lagunculariae 

9. Conidia measuring 3.1–4.3 × 2.6–3.4 µm, moderate growth 

on CYA . . . . . . . . . . . . . . . . . . . . . . . B. nivea (Fig. 8d–f) 

* Byssochlamys verrucosa is phylogenetically unrelated to the true Byssochlamys 

spp., but the taxon is included in the key because of its striking 

morphological similarity to other Byssochlamys species. 

** Smooth ellipsoidal ascospores once observed in a fresh isolate (5.3–7 × 

3.8–4.9 µm). 

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Polyphasic taxonomy of the heat resistant ascomycete ... - Persoonia

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