Fungal Diversity (2020) 103:47–85
https://doi.org/10.1007/s13225-020-00452-8
A re‑evaluation of the Chaetothyriales using criteria of comparative
biology
Yu Quan1,2,3 · Lucia Muggia4 · Leandro F. Moreno5 · Meizhu Wang1,2 · Abdullah M. S. Al‑Hatmi1,6,7
Nickolas da Silva Menezes14 · Dongmei Shi9 · Shuwen Deng10 · Sarah Ahmed1,6 · Kevin D. Hyde11 ·
Vania A. Vicente8,14 · Yingqian Kang2,13 · J. Benjamin Stielow1,12 · Sybren de Hoog1,6,8,10
·
Received: 30 April 2020 / Accepted: 26 June 2020 / Published online: 4 August 2020
© The Author(s) 2020
Abstract
Chaetothyriales is an ascomycetous order within Eurotiomycetes. The order is particularly known through the black yeasts
and filamentous relatives that cause opportunistic infections in humans. All species in the order are consistently melanized.
Ecology and habitats of species are highly diverse, and often rather extreme in terms of exposition and toxicity. Families
are defined on the basis of evolutionary history, which is reconstructed by time of divergence and concepts of comparative
biology using stochastical character mapping and a multi-rate Brownian motion model to reconstruct ecological ancestral
character states. Ancestry is hypothesized to be with a rock-inhabiting life style. Ecological disparity increased significantly
in late Jurassic, probably due to expansion of cytochromes followed by colonization of vacant ecospaces. Dramatic diversification took place subsequently, but at a low level of innovation resulting in strong niche conservatism for extant taxa.
Families are ecologically different in degrees of specialization. One of the clades has adapted ant domatia, which are rich
in hydrocarbons. In derived families, similar processes have enabled survival in domesticated environments rich in creosote
and toxic hydrocarbons, and this ability might also explain the pronounced infectious ability of vertebrate hosts observed in
these families. Conventional systems of morphological classification poorly correspond with recent phylogenetic data. Species are hypothesized to have low competitive ability against neighboring microbes, which interferes with their laboratory
isolation on routine media. The dataset is unbalanced in that a large part of the extant biodiversity has not been analyzed by
molecular methods, novel taxonomic entities being introduced at a regular pace. Our study comprises all available species
sequenced to date for LSU and ITS, and a nomenclatural overview is provided. A limited number of species could not be
assigned to any extant family.
Keywords Black yeasts · Phylogeny · Ecology · Ancestral reconstruction · Evolution · Nomenclature
Introduction
Chaetothyriales is an ascomycetous order within Eurotiomycetes of the subphylum Pezizomycotina (Gueidan et al.
2014; Wijayawardene et al. 2020). The order is renowned
for containing so-called black yeasts and their filamentous relatives, among which are numerous opportunistic
* Dongmei Shi
shidongmei28@163.com
* Yingqian Kang
kangyingqian@gmc.edu.cn
* Sybren de Hoog
sybren.dehoog@radboudumc.nl
Extended author information available on the last page of the article
agents of disease in humans and cold-blooded vertebrates.
Well-known genera are Cladophialophora, Exophiala,
Fonsecaea and Phialophora (Herpotrichiellaceae), but the
order is much more diverse, in the literature of the last decades containing about 42 genera (with frequent additions)
arranged in six families as summarized in the taxonomic
browser of NCBI and 56 genera belonging to 11 families
by Wijayawardene et al. (2020). A family that has been
linked to Chaetothyriales, viz. Coccodiniaceae, contains
four genera with few epilithic and epiphytic species having
nondescript morphology and which are difficult to cultivate and sequence. Most researchers hypothesize an affinity to Capnodiales in Dothideomycetes (Hyde et al. 2013;
Réblová et al. 2013; Kirk et al. 2001; Winka et al. 1998).
Other families included in the order by Barr (1987a, b), i.e.
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48
Metacapnodiaceae, Microtheliopsidaceae, Strigulaceae and
Trichopeltidaceae, have also been suggested to belong to
Dothideomycetes or are incertae sedis (Reynolds 1985).
Pyrenotrichaceae (Herrera-Campos et al. 2005) has been
suggested to belong to Chaetothyriales Wijayawardene et al.
(2020) but no sequence data are available to support this.
Also for family Lyrommataceae, containing the single genus
Lyromma producing ascomata with antler-shaped appendages and pycnidia with filiform conidia (Flakus and Farkas
2013) no sequence data is available. Some other described
families will be discussed below. The five remaining families
that are currently accepted in the order are Chaetothyriaceae,
Cyphellophoraceae, Epibryaceae, Herpotrichiellaceae, and
Trichomeriaceae (Réblová et al. 2013; Gueidan et al. 2014;
Chomnunti et al. 2012a; Barr 1976; Barr and Makkai 1987).
A major problem in Chaetothyriales is that only a fraction of the extant species is likely to be known, as shown
for other groups of fungi in Hyde et al. (2018). Members of
Herpotrichiellaceae have limited morphological features and
should be distinguished by molecular parameters observed
on asexual states in culture. Conversely, species in the large
family Chaetothyriaceae have classically been distinguished
by the morphology of their sexual state in nature, and for
most no sequence data are available. Further, new monophyletic lineages of lichen-inhabiting fungi have been reported
for fungi close to Chaetothyriales (Muggia et al. 2015, 2016,
2017, 2020), for which the exact taxonomic position still
needs to be determined. Therefore, taxonomic boundaries
at lower and higher levels are likely to appear unstable in
the future when more extant biodiversity will be added and
adequately described.
In summary, the taxonomy in Chaetothyriales is unsettled, for three reasons: (1) fragmentary representation of
extant species, (2) limited availability of sequence data, and
(3) conflicting concepts between traditional and modern taxonomic methods. As a consequence, the order is in need of
detailed taxonomic revision. In view of taxonomic stability,
the present paper aims to develop a polyphasic approach to
classification, at least at the family level, since strict phylogenetic taxonomy may be subject to change as soon as new
aspects of biodiversity of the order are revealed.
Materials and methods
Strains and sequences
Sequences of strains used in this study were retrieved from
an in-house black yeast database maintained for research
purposes at Westerdijk Fungal Biodiversity Institute, supplemented with data from GenBank (Table 1). In view of
optimal resolution of phylogenetic relationships, all species
sequenced to date were included with a single sequence per
13
Fungal Diversity (2020) 103:47–85
species. Up to now (April 2020), GenBank records at NCBI
list the order Chaetothyriales with 6 families, 42 genera and
273 species. Sequences in the present study comprise of 8
described families, 33 genera, 209 species, 45 undescribed
species and two outgroup species. Species not included are
either missing sequences for the LSU or ITS or both, or
these sequences are obvious errors in NCBI. Undescribed
species are mainly inhabitants of ant nests (carton-building
ants or domatia) (Voglmayr et al. 2011; Nepel et al. 2014), or
rock-inhabiting species of which a significant share belong
to Chaetothyriales (Ruibal et al. 2018; Muggia et al. 2020);
only a selection of these has been included.
Phylogeny
To assess the phylogenetic position of Chaetothyriales, phylogenetic analyses of the ITS and LSU loci were performed
for 254 sequences representing this order. Multiple sequence
alignments were made by MAFFT v7 (http://mafft.cbrc.jp/)
and optimized manually using MEGA v7.2 (Kumar et al.
2012) and BIOEDIT v7.2 (Hall 1999). Missing data for part
of the sequences for some taxa were coded as ‘missing’, but
still could be used in the final matrix (Wiens 2006, 2008).
Models of DNA sequence evolution for each locus partition were selected with jModelTest v.2.0 (Darriba et al.
2012), using the Akaike information criterion (AIC, Akaike
1974). To detect possible topological conflicts among
loci, the CADM test (Campbell et al. 2011; Legendre and
Lapointe 2004) was performed using the function ‘CADM.
global’ implemented in the package ‘ape’ of R (Paradis et al.
2004). With congruence, three alignments, ITS, LSU and
ITS combined with LSU were used to run the tree. Three
algorithms, i.e. maximum likelihood (ML), Bayesian inference (BI) and Neighbor-Joining (NJ) were employed on
phylogenetic analyses. Capnodium coffeae, CBS 147.52 and
Capnodium salicinum, CBS 131.34 were taken as outgroups
in most of the trees.
ML trees were obtained using RaxML-VI-HPC as implemented on the CIPRES portal web server (http://www.phylo
.org/). Neighbor Joining (NJ) was performed by MEGA v6
(Tamura et al. 2013) with Kimura 2-parameter model and
statistical bootstrapping procedure involving 1000 replicates.
Bayesian command files were prepared using MESQUITE
v2.75 (Maddison and Maddison 2007), and the analysis was
done in MRBAYES v3.1.2 implemented in the CIPRES web
server (http://www.phylo.org/). Two parallel runs with four
Markov chain Monte Carlo (MCMC) simulations for each
run were set for 10,000,000 generations and the result was
checked using TRACER v1.5 (Rambaut and Drummond
2009) for effective sample size (ESS). The run was then
extended for another 10,000,000 generations with a sample
frequency of 1,000 per generation.
Fungal Diversity (2020) 103:47–85
49
Table 1 Strain GenBank data with proximate ecology per species
Clade
Species
Accession number Ecology
ITS
LSU
References
Clade 1
Herpotrichiellaceae
Exophiala spinifera
D22I
Opportunistic
MH010942.1
MH012097.1
Rhinocladiella similis
PW3041
Opportunistic
LC158611.1
LC158635.1
Exophiala exophialae
Exophiala nigra
CBS 668.76 (T)
CBS 535.94 (T)
Other
Other
AY156973.1
KY115191.1
NG059252.1
NG059253.1
Opportunistic
Opportunistic
Epiphytic
MH864631.1
KP070763.1
KY496744.1
MH876068.1
NG059237.1
KY496723.1
Other
Other
MG922572.1
MH862572.1
MG922576.1
MH874198.1
Other
MH863226.1
EU552107.1
Nascimento et al.
(2017)
de Hoog et al.
(2003)
CBS
Moussa et al.
(2017a)
Zeng et al. (2007)
Yong et al. (2015)
Tibpromma et al.
(2017)
Dong et al. (2018)
Pratibha and Prabhugaonkar (2015)
Marincowitz et al.
(2008)
de Hoog (1977)
Exophiala oligosperma CBS 127587
Exophiala polymorpha CBS 138920 (T)
Exophiala italica
MFLUCC
16-0245
Thysanorea aquatica
MFLCC 15-0966
Thysanorea papuana
CBS 212.96 (T)
Capronia kleinmonCBS 122671 (T)
densis
Rhinocladiella atroCBS 264.49 (T)
virens
Exophiala dermatitidis CBS 207.35 (T)
Epiphytic
MH856518.1
EU041869.1
Opportunistic
MH855649.1
NG059225.1
Sudhadham et al.
(2008)
CBS
CBS
Woo et al. (2013)
Capronia mansonii
Capronia munkii
Exophiala hongkongensis
Capronia dactylotricha
Capronia pilosella
Veronaea compacta
Exophiala brunnea
Exophiala jeanselmei
Exophiala moniliae
Exophiala bergeri
Exophiala sideris
CBS 101.67 (T)
CBS 615.96 (T)
HKU 32 (T)
Epiphytic
Epiphytic
Opportunistic
AF050247.1
MH862601.1
JN625231.2
AY004338.1
EF413604.1
NG059264.1
CBS 604.96 (T)
AFTOL-ID 657
CBS 268.75 (T)
CBS 587.66 (T)
CBS 507.90 (T)
CBS 520.76 (T)
CBS 353.52 (T)
D88
Other
Other
Epiphytic
Epiphytic
Opportunistic
Epiphytic
Opportunistic
Other
AF050243.1
DQ826737.1
EU041819.1
MH858890.1
AY156963.1
KF881967.1
MH857080.1
KC315801.1
KX712343.1
DQ823099.1
NG057790.1
KX712342.1
KJ930161.1
KJ930162.1
NG059199.1
HM627072.1
Exophiala capensis
CBS 128771 (T)
Epiphytic
NR_121493.1 NG_059207.1
Capronia fungicola
Capronia nigerrima
Phaeoannellomyces
elegans
Exophiala psychrophila
Exophiala lignicola
Exophiala nidicola
Exophiala nishimurae
CBS 614.96 (T)
CBS 513.69
CBS 101597
Other
Other
Opportunistic
KY484990.1 NG058761.1
MH859363.1 AY605075.1
NR_155687.1 KY115194.1
CBS 191.87 (T)
Opportunistic
NR_145371.1 MH873750.1
CBS 144622 (T)
FMR 3889 (T)
CBS 101538 (T)
Epiphytic
Other
Epiphytic
NR_163358.1 NG_066324.1
NR_161045.1 MG701056.1
NR_137092.1 KX712351.1
Exophiala palmae
UPCB 86822 (T)
Epiphytic
NR_158414.1 NG_064428.1
Exophiala heteromorpha
Exophiala eucalypticola
Exophiala eucalypti
CBS 232.33 (T)
Epiphytic
NR_111184.1 NG_063975.1
CBS 143412 (T)
Epiphytic
MH107891.1
NG_063955.1
CBS
Müller et al. (1987)
Papendorf (1976)
Papendorf (1969)
Zeng et al. (2007)
de Hoog (1977)
Zeng et al. (2007)
Seyedmousavi et al.
(2011)
Crous and Groenewald (2011)
Müller et al. (1987)
Barr (1991)
Moussa et al.
(2017a, b)
de Hoog et al.
(2011)
Crous et al. (2019)
Crous et al. (2018)
de Hoog et al.
(2003)
Nascimento et al.
(2017)
de Hoog et al.
(2003)
Crous et al. (2018)
CPC 27630
Epiphytic
KY173411.1
KY173502.1
Crous et al. (2013)
13
50
Fungal Diversity (2020) 103:47–85
Table 1 (continued)
Clade
Species
Accession number Ecology
ITS
Capronia camelliaeyunnanensis
Capronia leucadendri
CGMCC 3.19061 Epiphytic
(T)
CBS 122672 (T) Epiphytic
Capronia parasitica
CBS 123.88
References
F10685 123.33
CBS 123.33 (T)
CBS 158.58 (T)
CBS 402.95
T210
CBS 496.78 (T)
Opportunistic
Opportunistic
Opportunistic
Other
Carton
Other
CBS 122635
Opportunistic
NR_164589.1 NG_066425.1 Phookamsak et al.
(2019)
NR_156212.1 MH874754.1 Marincowitz et al.
(2008)
AF050252.1 FJ358225.1
Gueidan et al.
(2008)
KX306769.1 NG059698.1 HernándezRestrepo et al.
(2016)
KT013095.1 KT013094.1 Overy et al. (2015)
MH855383.1 NG059200.1 Zeng et al. (2007)
MH857734.1 KF928522.1 CBS
MH862536.1 KX712349.1 Zeng et al. (2007)
KF614880
KF614880
Nepel et al. (2014)
EU041811.1 NG057785.1 Veerkamp et al.
(1983)
GU017732.1 KX822357.1 Badali et al. (2010)
RA776
Opportunistic
KU854928.1
CBS 132.86 (T)
Epiphytic
CBS 101460 (T)
Opportunistic
CBS 157.67 (T)
Opportunistic
Exophiala radicis
Exophiala equina
P2854 (T)
CBS 116009 (T)
Epiphytic
Opportunistic
Exophiala pisciphila
CBS 537.73 (T)
Opportunistic
Exophiala bonariae
CCFEE 5792 (T)
Exophiala opportunisticica
Exophiala cancerae
CBS 122268
Epilithic/lichenicolous
Opportunistic
NR_145356.1 NG_057784.1 Arzanlou et al.
(2007)
AY163561.1 NG057783.1 de Hoog et al.
(2019)
JF747137.1
AY213702.1 de Hoog et al.
(2011)
KT099204.1 KT723448.1 Madrid et al. (2016)
KF928433.1 KF928497.1 de Hoog et al.
(2011)
DQ826739.1 NR121269
de Hoog et al.
(2011)
JX681046.1
KR781083.1 Isola et al. (2016)
CBS 115142
Opportunistic
Exophiala abietophila
CBS 145038 (T)
Epiphytic
Veronaea constricta
CBS 572.90
Other
Veronaea japonica
CBS 776.83 (T)
Epiphytic
Veronaea botryosa
CBS 254.57 (T)
Opportunistic
Chaetothyriales sp.
CBS 128956
Carton
Exophiala crusticola
Minimelanolocus
obscurus
Minimelanolocus
melanicus
Minimelanolocus
asiaticus
CBS 119970 (T)
MFLUCC
15-0416
MFLUCC
15-0415 (T)
MFLUCC
15-0237 (T)
Rhinocladiella quercus CPC 26621 (T)
13
LSU
Exophiala attenuata
Exophiala lecanii-comi
Exophiala castellanii
Exophiala mesophila
Chaetothyriales sp.
Rhinocladiella phaeophora
Rhinocladiella
aquaspersa
Rhinocladiella tropicalis
Rhinocladiella fasciculata
Rhinocladiella basitona
Exophiala salmonis
Epiphytic
Epilithic/lichenicolous
KX356663.1
Gomes et al. (2016)
KF928436.1
KF928500.1
Other
Other
de Hoog et al.
(2011)
MH862980.1 MH874540.1 de Hoog et al.
(2011)
NR_163357.1 NG_066323.1 Crous and Groenewald (2011)
MH862237.1 MH873920.1 Moustafa and
Abdul-Wahid
(1990)
MH861692.1 NG057789.1 Arzanlou et al.
(2007)
MH857711.1 MH869255.1 de Hoog et al.
(2019)
KX822529
KX822529
Voglmayr et al.
(2011)
MH863070.1 NG059220.1 Döğen et al. (2013)
KR215606.1 KR215611.1 Liu et al. (2015)
Other
KR215608.1
KR215613.1
Liu et al. (2015)
Other
NR_154179.1 KR215610.1
Liu et al. (2015)
Fungal Diversity (2020) 103:47–85
51
Table 1 (continued)
Clade
Species
Accession number Ecology
ITS
LSU
References
Minimelanolocus
curvatus
Minimelanolocus
aquaticus
Capronia acutiseta
Chaetothyriales sp.
Rhinocladiella anceps
Melanoctona tectonae
MFLUCC
15-0259 (T)
MFLUCC
15-0414 (T)
CBS 618.96 (T)
CBS 129051
AFTOL ID 659
MFLUCC
12-0389 (T)
CBS 129050
ATCC 56201 (T)
CBS 482.92 (T)
Other
KR215605.1
KR215609.1
Liu et al. (2015)
Other
KR215607.1
KR215612.1
Liu et al. (2015)
Epiphytic
Carton
Other
Epiphytic
NR_154744.1
KX822540
DQ826740.1
KX258778.1
NG058859.1
KX822540
DQ823102.1
KX258779.1
Müller et al. (1987)
Nepel et al. (2014)
CBS
Tian et al. (2016)
Carton
Other
Opportunistic
KX822532.1 KX822532
NR_154745.1 AF050242.1
MH862370.1 KF155190.1
Chaetothyriales sp.
Capronia coronata
Exophiala angulospora
Rhinocladiella mackenziei
Rhinocladiella coryli
CBS 368.92
Opportunistic
MH862361.1
EU041866.1
CPC 26654 (T)
Epiphytic
KX306768.1
KX306793.1
Chaetothyriales sp.
Chaetothyriales sp.
Exophiala alcalophila
Fonsecaea minima
T171
T22
CBS 520.82 (T)
CBS 125757 (T)
Carton
Carton
Other
Epiphytic
KF614875
KF614881
MH861524.1
MH863743.1
KF614875
KF614881
NG059189.1
KF928520.1
Fonsecaea pugnacius
CBS 139214 (T)
Opportunistic
NR_155089.1 NG058177.1
Fonsecaea pedrosoi
Fonsecaea erecta
CBS 271.37 (T)
CBS 125763
Opportunistic
Epiphytic
AB114127.1
KC886414.1
KJ930166.1
KF155186.1
Opportunistic
KJ701015.1
KJ930163.1
CBS 147.84 (T)
Opportunistic
EU103985.1
KC809989.1
Nepel et al. (2014)
Müller et al. (1987)
Gjessing et al.
(2011)
Moreno et al.
(2018)
HernándezRestrepo et al.
(2016)
Nepel et al. (2014)
Nepel et al. (2014)
CBS
Vicente et al.
(2014)
de Azevedo et al.
(2015)
Sutton et al. (2009)
Vicente et al.
(2014)
Vicente et al.
(2012)
Badali et al. (2008)
CBS 834.96 (T)
Opportunistic
MH862619.1
KC809990.1
Badali et al. (2008)
T367
CBS 306.94 (T)
Carton
Opportunistic
KF614894
EU103986.1
KF614894
NG058959.1
Nepel et al. (2014)
Badali et al. (2008)
CBS 556.83 (T)
Epiphytic
AY251087.1
NG058763.1
Badali et al. (2008)
CBS 110553 (T)
Other
AY857517.1
NG058955.1
Badali et al. (2008)
CBS 114772
Other
EU035410.1
EU035410.1
Crous et al. (2007)
CBS 112793
Other
EU137331.1
EU035402.1
Crous et al. (2007)
MFC1-P384 (T)
Epiphytic
FN549916.1
FN400758.1
Koukol (2010)
KNU 16032 (T)
Other
LC387460.1
LC387461.1
Das et al. (2019)
CBS 640.96
Opportunistic
EU103995.1
KC809995.1
CBS 128948
Carton
KX822492
KX822492
van den Ende and
De Hoog (1999)
Voglmayr et al.
(2011)
Fonsecaea brasiliensis BMU 07620
Cladophialophora
devriesii
Cladophialophora
immunda
Chaetothyriales sp.
Cladophialophora
arxii
Cladophialophora
minourae
Cladophialophora
psammophila
Cladophialophora
potulentorum
Cladophialophora
australiensis
Cladophialophora
matsushimae
Cladophialophora
lanosa
Cladophialophora
emmonsii
Chaetothyriales sp.
13
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Fungal Diversity (2020) 103:47–85
Table 1 (continued)
Clade
Species
Accession number Ecology
ITS
LSU
References
Chaetothyriales sp.
CBS 128935
Carton
KX822479
KX822479
Chaetothyriales sp.
CBS 128945
Carton
KX822487
KX822487
Cladophialophora
mycetomatis
Cladophialophora
tumulicola
Cladophialophora
parmeliae
Chaetothyriales sp.
CBS 122637 (T)
Opportunistic
FJ385276.1
NG058960.1
Voglmayr et al.
(2011)
Voglmayr et al.
(2011)
Badali et al. (2008)
JCM 28768
LC192127.1
LC192092.1
Kiyuna et al. (2018)
CBS 129337
Epilithic/lichenicolous
Other
JQ342180.2
JQ342182.1
CBS 129044
Carton
KX822488
KX822488
CBS 114747
Epiphytic
EU035403.1
KF928514.1
Diederich et al.
(2013)
Voglmayr et al.
(2011)
Koukol (2010)
CBS 126.86 (T)
Opportunistic
MH861932.1
NG058762.1
CBS 114405 (T)
Epiphytic
EU137322.1
NG058855.1
CBS 122642 (T)
Opportunistic
FJ385273.1
NG058961.1
de Hoog et al.
(2019)
de Hoog et al.
(2007)
Badali et al. (2008)
CBS 126736
Epiphytic
KC776592.1
KC812100.1
Feng et al. (2014)
CBS 259.83 (T)
Opportunistic
MH861581.1
NG058854.1
Badali et al. (2008)
CBS 400.67
Opportunistic
MH859007.1
MH859007.1
CBS 286.47
CBS 98096 (T)
Opportunistic
Opportunistic
KF928455.1 KF928519.1
NR_111612.1 NG057983.1
Untereiner et al.
(1999)
Li et al. (2017)
CBS
FMR 3995
Other
KU705830.1
KU705847.1
JCM 28746 (T)
LC192125.1
LC192090.1
MFLUCC
15-0971
CBS 126086
Epilithic/lichenicolous
Other
de Hoog et al.
(2011)
Kiyuna et al. (2018)
MG922573.1
MG922577.1
Dong et al. (2018)
Epiphytic
MH863784.1
MH875246.1
Ruiz et al. (2001)
HMAS245592
Epiphytic
KP337330.1
KP337329.1
YMF 1.04133
MFLUCC
16-1449(T)
MFLUCC
11-0529
CBS 124764 (T)
Epiphytic
Epiphytic
KU173860.1 KX131164.1
NR_164246.1 KY305176.1
Ying-Rui Ma et al.
(2015)
Yang et al. (2011)
Li et al. (2018)
Epiphytic
MG922571.1
MG922575.1
Dong et al. (2018)
Epiphytic
KC455238.1
GQ303305.1
CBS 129342 (T)
Epiphytic
MH865228.1
MH876666.1
CHCJHBJBLM
(T)
GLZJSJ41 (T)
CBS 122.74 (T)
Epiphytic
KP010367.1
KP122930.1
Cheewangkoon
et al. (2009)
Decock et al.
(2003)
Gao et al. (2015)
Epiphytic
Other
KP010370.1
KC455247.1
KP122932.1
KC455260.1
HLHNZWYZZ08 Epiphytic
(T)
KP010371.1
KP122933.1
Cladophialophora
chaetospira
Cladophialophora
boppii
Cladophialophora
yegresii
Cladophialophora
subtilis
Cladophialophora
abundans
Cladophialophora
samoensis
Phialophora americana
Phialophora verrucosa
Fonsecaea multimorphosa
Exophiala lacus
Cladophialophora
tumbae
Minimelanolocus
thailandensis
Minimelanolocus rousselianus
Atrokylindriopsis
setulosa
Uncispora sp.
Marinophialophora
garethjonesii
Aculeata aquatica
Clade 2 Cyphellophoraceae
13
Cyphellophora eucalypti
Cyphellophora guyanensis
Cyphellophora artocarpi
Cyphellophora musae
Cyphellophora olivacea
Cyphellophora phyllostachydis
Gao et al. (2015)
Réblová et al.
(2013)
Gao et al. (2015)
Fungal Diversity (2020) 103:47–85
53
Table 1 (continued)
Clade
Clade 3 Phaeosaccardinulaceae
Clade 4
Domatia
Species
Accession number Ecology
ITS
LSU
References
Cyphellophora gamsii
Cyphellophora oxyspora
Cyphellophora jingdongensis
Cyphellophora livistonae
Phialophora intermedia
Cyphellophora pluriseptata
Cyphellophora laciniata
Cyphellophora suttonii
Cyphellophora fusarioides
Cyphellophora pauciseptata
Cyphellophora sessilis
Cyphellophora europaea
Cyphellophora vermispora
Cyphellophora reptans
Chaetothyriales sp.
CPC 25867 (T)
CBS 698.73 (T)
Epiphytic
Other
KX228255.1
MH860790.1
KX228307.1
KC455262.1
Crous et al. (2016)
CBS
IFRDCC 2659
Epiphytic
MF285234.1
MF285236.1
Yang et al. (2018)
CPC 19433 (T)
Epiphytic
KC005774.1
NG042752.1
Madrid et al. (2016)
CBS 235.93
Opportunistic
JQ766431.1
JQ766480.1
Iwatsu et al. (1988)
CBS 286.85 (T)
Opportunistic
MH861881.1
KC455255.1
Feng et al. (2014)
CBS 190.61 (T)
Opportunistic
EU035416.1
KF928547.1
Feng et al. (2014)
CBS 449.91 (T)
CBS 130291 (T)
Opportunistic
Opportunistic
KC455243.1
MH865596.1
KC455256.1
JQ766486.1
Feng et al. (2014)
Feng et al. (2014)
CBS 284.85 (T)
Opportunistic
JQ766438.1
JQ766519.1
Feng et al. (2014)
CBS 243.85 (T)
CBS 101466 (T)
Epiphytic
Opportunistic
AY857542.1
KF928473.1
EU514700.1
KC455259.1
CBS 228.86 (T)
Other
MH861947.1
KC455257.1
CBS
Lian and De Hoog
(2010)
Feng et al. (2014)
CBS 113.85 (T)
CBS 128959
Other
Carton
EU514699.1
KX822542
EU514699.1
KX822542
CBS 131954
Carton
KF928465.1
KF928529.1
Phialophora
capiguarae
Cyphellophora clematidis
Cyphellophora filicis
CBS 144983
Epiphytic
MK442577.1
MK442519.1
DP002B
Epiphytic
MK404057.1
MK404053.1
Phialophora attae
CBS 132767
Carton
Anthopsis deltoidea
CBS 263.77(T)
Other
Paracladophialophora CPC 27596 (T)
carceris
P. cyperacearum
CPC 33046 (T)
Chaetothyriales sp.
MACrb1
Gao et al. (2015)
Voglmayr et al.
(2011)
Attili-Angelis et al.
(2014)
Crous et al. (2019)
Epiphytic
Phookamsak et al.
(2019)
KF928464.1 KF928528.1 Attili-Angelis et al.
(2014)
NR_153555.1 NG_057113.1 Moussa et al.
(2017a, b)
NR_154360.1 KY173395.1 Crous et al. (2018)
Epiphytic
Domatium
NR_160625.1 MH327844.1
HQ634654.1 HQ634654.1
Chaetothyriales sp.
CBS 135085
Domatium
KX822349
KX822349
Chaetothyriales sp.
CBS 132039
Domatium
KX822342
KX822342
Chaetothyriales sp.
CBS 129057
Domatium
KX822346
KX822346
Chaetothyriales sp.
CBS 132003
Domatium
KX822477
KX822477
Chaetothyriales sp.
CR13Ceci2
Domatium
KX120978.1
KX120978.1
Chaetothyriales sp.
Cecr4
Domatium
KX822476
KX822476
Chaetothyriales sp.
CBS 135086
Domatium
KX822336
KX822336
Crous et al. (2018)
Wang et al. (unpublished)
Wang et al. (unpublished)
Wang et al. (unpublished)
Wang et al. (unpublished)
Wang et al. (unpublished)
Wang et al. (unpublished)
Wang et al. (unpublished)
Wang et al. (unpublished)
13
54
Fungal Diversity (2020) 103:47–85
Table 1 (continued)
Clade
Clade 5
Melanina
Species
Accession number Ecology
ITS
LSU
References
Chaetothyriales sp.
Trii4
Domatium
KX822551
KX822551
Chaetothyriales sp.
CBS 134920
Domatium
KX822324
KX822324
Chaetothyriales sp.
CBS 134916
Domatium
KX822344
KX822344
Chaetothyriales sp.
CBS 128963
Domatium
KX822328
KX822328
Chaetothyriales sp.
CBS 128966
Domatium
KX822331
KX822331
Chaetothyriales sp.
CBS 128973
Domatium
KX822354
KX822354
Chaetothyriales sp.
CBS 134923
Domatium
KX822319
KX822319
Chaetothyriales sp.
A581
MT193582
KT263163.1
Wang et al. (unpublished)
Wang et al. (unpublished)
Wang et al. (unpublished)
Wang et al. (unpublished)
Wang et al. (unpublished)
Wang et al. (unpublished)
Wang et al. (unpublished)
Muggia et al (2020)
MT193581
KT270641
Muggia et al (2020)
MT193584
KT270601
Muggia et al (2020)
MT193583
KT270659
Muggia et al (2020)
KP174843.1
KP174924.1
Su (2015)
KP174846.1
KP174922.1
Su (2015)
MH862564.1
NG042586.1
MH862556.1
NG042775.1
Tsuneda et al.
(2011)
Nai et al. (2013)
KP791780.1
KR781068.1
Isola et al. (2016)
KP791790.1
KR781077.1
Isola et al. (2016)
KP791784.1
KR781072.1
Isola et al. (2016)
NR_111330.1 NG042475.1
Tsuneda et al.
(2011)
Tsuneda et al.
(2011)
Isola et al. (2016)
Chaetothyriales sp.
Chaetothyriales sp.
Chaetothyriales sp.
Clade 6 Trichomeriaceae Anthracinomyces
petraeus
Anthracinomyces
ramosus
Knufia perforans
Knufia petricola
Knufia vaticanii
Knufia marmoricola
Knufia karalitana
Knufia epidermidis
Knufia cryptophialidica
Knufia mediterranea
Chaetothyriales sp.
Arthrocladium tropicale
Arthrocladium tardum
13
Epilithic/lichenicolous
A933
Epilithic/lichenicolous
A872
Epilithic/lichenicolous
A957
Epilithic/lichenicolous
CGMCC 3.17315 Epilithic/lichenicolous
CGMCC 3.16367 Epilithic/lichenicolous
CBS 885.95 (T)
Epilithic/lichenicolous
CBS 726.95 (T)
Epilithic/lichenicolous
CCFEE 5939 (T) Epilithic/lichenicolous
CCFEE 6201
Epilithic/lichenicolous
CCFEE 5921
Epilithic/lichenicolous
CBS 120353 (T) Epilithic/lichenicolous
DAOM 216555
Epiphytic
(T)
CBS 139721 (T) Epilithic/lichenicolous
T261
Carton
CBS 134926 (T) Domatium
CBS 127021 (T)
JN040501.1
JN040500.1
KP791794.1
KR781081.1
KF614886.1
KX822543.1
KF614886
NG057119.1
Epiphytic
KT337440.1
NG057089.1
CBS 457.67 (T)
Epiphytic
MH859032.1
NG_057084
Arthrocladium caudatum
Arthrocladium fulminans
Chaetothyriales sp.
CBS 136243 (T)
Opportunistic
KT337439.1
NG057088.1
CBS 128958
Carton
KX822541
KX822541
Chaetothyriales sp.
CBS 129049
Carton
KX822531
KX822531
Nepel et al. (2014)
Nascimento et al.
(2016)
Nascimento et al.
(2016)
Nascimento et al.
(2016)
Nascimento et al.
(2016)
Voglmayr et al.
(2011)
Voglmayr et al.
(2011)
Fungal Diversity (2020) 103:47–85
55
Table 1 (continued)
Clade
Species
Accession number Ecology
ITS
LSU
References
Chaetothyriales sp.
CBS 129047
Carton
KX822533.1
KX822533
Exophiala placitae
Chaetothyriales sp.
Cladophialophora
eucalypti
Cladophialophora
pucciniophila
Cladophialophora
proteae
Strelitziana albiziae
Strelitziana eucalypti
Strelitziana australiensis
Strelitziana cliviae
Bradymyces alpinus
CBS 121716 (T)
T179
CBS 145551 (T)
Epiphytic
Carton
Epiphytic
MH863143.1
KF614876.1
MK876380.1
MH874694.1
KF614876.1
MK876419.1
Voglmayr et al.
(2011)
Crous et al. (2007)
Nepel et al. (2014)
Crous et al. (2019)
KUS F23645
Other
JF263533.1
JF263534.1
CBS 111667 (T)
Opportunistic
EU035411.1
EU035411.1
CBS 126497 (T)
CBS 128214
CBS 124778 (T)
Epiphytic
Epiphytic
Epiphytic
MH864122.1
HQ599596.1
GQ303295.1
HQ599585.1
HQ599597.1
GQ303326.2
CPC 19822 (T)
CCFEE 5493 (T)
Epiphytic
Epilithic/lichenicolous
Epilithic/lichenicolous
Opportunistic
KC005772.1
HG793052.1
NG042750.1
GU250396.1
KX179910.1
KX179912.1
NR_132843.1 NG058643.1
Carton
Epiphytic
KF614873.1
JX313655.1
KF614873.1
JX313661.1
Epiphytic
JX313656.1
JX313662.1
Epiphytic
NR_137946.1 NG058126.1
Bradymyces graniticola
Bradymyces oncorhynchi
Chaetothyriales sp.
Trichomerium foliicola
F6A
CCF 4369 (T)
T333
MFLUCC
10-0078 (T)
MFLUCC
10-0087 (T)
CBS 138870 (T)
Park and Shin
(2011)
Crous et al. (2007)
Crous et al. (2010)
Crous et al. (2010)
Cheewangkoon
et al. (2009)
Crous et al. (2012)
Hubka et al. (2014)
Réblová et al.
(2016)
Hubka et al. (2014)
Nepel et al. (2014)
Chomnunti et al
(2011)
Hongsanan et al.
(2016a)
Crous et al. (2014)
Trichomerium gloeosporum
Trichomerium
dioscoreae
Trichomerium
deniquelatum
Trichomerium eucalypti
Chaetothyriales sp.
Chaetothyriales sp.
Chaetothyriales sp.
MFLUCC
10-0884 (T)
CBS 143443 (T)
Epiphytic
JX313654.1
Epiphytic
NR_156672.1 NG058525.1
T13
T9
CBS 128943
Carton
Carton
Carton
KF614778
KF614780.1
KX822485.1
KF614778
KF614780.1
KX822485
Chaetothyriales sp.
CBS 129046
Carton
KX822526.1
KX822526
Knufia peltigerae
CGMCC 3.17283 Epilithic/lichenicolous
FMR 10621 (T)
Other
CBS 110960 (T) Epiphytic
KP174864.1
KP174935.1
NR_132842.1 HG003672.1
MH862870.1 DQ008153.1
CBS 124104 (T)
Epiphytic
NR_132828.1 NG_058633.1 Crous et al. (2009)
CBS 128210
Epiphytic
HQ599588.1
CPC 19837 (T)
Epiphytic
NR_111822.1 NG_042749.1 Crous et al. (2012)
CBS 139903(T)
Epiphytic
NR_137987.1 NG_058165.1 Crous et al. (2015)
CBS 120037
Epiphytic
DQ885895.1
Knufia tsunedae
Metulocladosporiella
musicola
Brycekendrickomyces
acaciae
Exophiala encephalarti
Ceramothyrium melastoma
Neostrelitziana acaciigena
Strelitziana africana
JX313660.1
HQ599589.1
DQ885895.1
Chomnunti et al.
(2012c)
Crous et al. (2017)
Nepel et al. (2014)
Nepel et al. (2014)
Voglmayr et al.
(2011)
Voglmayr et al.
(2011)
Réblová et al.
(2013)
Crous et al. (2013)
Crous et al. (2006)
Crous et al. (2010)
Arzanlou and Crous
(2006)
13
56
Fungal Diversity (2020) 103:47–85
Table 1 (continued)
Clade
Clade 7
Chaetothyrialceae
Species
Accession number Ecology
ITS
LSU
References
Arthrophiala arthrospora
Lithohypha aloicola
Ceramothyrium
exiguum
Nullicamyces eucalypti
Ceramothyrium
aquaticum
Ceramothyrium
phuquocense
Camptophora schimae
Camptophora hylomeconis
Aphanophora eugeniae
COAD 658
KY173473.1
KX447143.1
Crous et al. (2016)
CPC 35996(T)
Epiphytic
VTCCF-1209 (T) Other
NR_166313.1 MN567611.1
LC360297.1 LC360295.1
CPC 32942 (T)
Epiphytic
VTCCF-1210 (T) Other
MH327807.1
LC360299.1
NG064546.1
LC360296.1
VTCCF-1206 (T) Epiphytic
LC360298.1
LC360294.1
IFRDCC 2664
CBS 113311 (T)
Epiphytic
Epiphytic
MF285231.1
EU035415.1
MF285233.1
EU035415.1
Crous et al. (2019)
Tsurumi et al.
(2018)
Crous et al. (2018)
Tsurumi et al.
(2018)
Tsurumi et al.
(2018)
Yang et al. (2018)
Yang et al. (2018)
CBS 124105 (T)
Epiphytic
FJ839617.1
NG056965.1
Phaeosaccardinula
dendrocalami
Phaeosaccardinula
multiseptata
Phaeosaccardinula
ficus
Ceramothyrium menglunense
Chaetothyrium
brischoficola
Vonarxia vagans
Clade 8
Epibryaceae
Clade 9
13
Epiphytic
IFRDCC 2649 (T) Epiphytic
NR_137820.1 NG060116.1
Réblová et al.
(2013)
Yang et al. (2014)
IFRDCC 2639 (T) Epiphytic
NR_132894.1 KF667244.1
Yang et al. (2014)
MFLUCC
10-0009 (T)
MFLUCC
16-1874 (T)
MFLUCC
10-0083 (T)
CBS 123533 (T)
Epiphytic
HQ895840.1
NG059455.1
Epiphytic
KX524148.1
KX524146.1
Chomnunti et al.
(2014)
Hyde et al. (2016)
Epiphytic
HQ895839.1
HQ895836.
Epiphytic
FJ839636.1
NG057821.1
Epiphytic
KP744437.1
KP744480.1
Chomnunti et al.
(2012c)
Réblová et al.
(2013)
Liu et al. (2015)
Epiphytic
KC005773.1
NG042751.1
Crous et al. (2012)
Epiphytic
Epiphytic
NR_161138.1 NG_066293.1 Crous et al. (2018)
MH863133.1 NG_060793.1 Crous et al. (2007)
Epiphytic
KC978733.1
KC455251.1
CBS
Epiphytic
HQ895838.1
NG058817.1
Zeng et al. (2016)
Epiphytic
KT588601.1
NG058927.1
Epiphytic
KP324929.1
NG058904.1
Hongsanan et al.
(2015a, b)
Zeng et al. (2016)
Epiphytic
EU035408.1
NG058850.1
Crous et al. (2007)
Bryophytic
MH863155.1
NG058851.1
Epiphytic
EU035413.1
EU035413.1
Davey and Currah
(2007)
Crous et al. (2007)
Bryophytic
Bryophytic
MH863955.1
MH863958.1
MH875414.1
MH875417.1
Bryophytic
Epilithic/lichenicolous
MH864165.1
KT263083.1
MH875627.1
KT263083.1
Chaetothyrium agathis MFLUCC
12-0113 (T)
Ceramothyrium podo- CPC 19826 (T)
carpi
Fumagopsis stellae
CBS 145078 (T)
Exophiala eucalypCBS 121638 (T)
torum
Ceramothyrium carni- CBS 175.95
olicum
Ceramothyrium thaiMFLUCC
landicum
10-0008 (T)
Ceramothyrium ficus
MFLUCC
15-0228 (T)
C. longivolcaniforme
MFLUCC
16-1306 (T)
Cladophialophora
CBS 117536 (T)
humicola
Cladophialophora
CBS 121758 (T)
minutissima
Cladophialophora
CBS 350.83 (T)
sylvestris
Epibryon bryophilum CBS 126278
Epibryon interlamelCBS 126286
lare
Epibryon turfosorum
CBS 126587
Chaetothyriales sp.
L1992
Dobbeler (1978)
Dobbeler et al.
(1979)
Dobbeler (1978)
Muggia et al.
(2015)
Fungal Diversity (2020) 103:47–85
57
Table 1 (continued)
Clade
Incertae sedis
Outgroup
Species
Accession number Ecology
ITS
LSU
References
Chaetothyriales sp.
L1993
KT263084.1
KT263084.1
Chaetothyriales sp.
L1994
KT263085.1
KT263085.1
Lichenodiplis lecanorae
Cladophialophora
modesta
Cladophialophora
scillae
Bacillicladium clematidis
Cladophialophora
hostae
Coccodinium bartschii
Capronia villosa
L
Muggia et al.
(2015)
Muggia et al.
(2015)
Muggia et al.
(2015)
Stielow and de
Hoog (2014)
Crous et al. (2007)
–
KT285909.1
CBS 985.96
Epilithic/lichenicolous
Epilithic/lichenicolous
Epilithic/lichenicolous
Opportunistic
KF928421.1
KF928485.1
CBS 116461
Epiphytic
EU035412.1
EU035412.1
CBS 145035(T)
Epiphytic
NR_163355.1 NG_066322.1 Crous et al. (2019)
CBS 121637
Epiphytic
KX822478.1
KX822478.1
Crous et al. (2007)
CPC 13861
ATCC 56206
Epiphytic
Epiphytic
EU019265.1
AF050261
EU019265.1
AF050261
Epibryon hepaticola
M10 (T)
Bryophytic
EU725690.1
EU940091.1
Capnodium coffeae
CBS 147.52
Epiphytic
MH856967.1
MH868489.1
Capnodium salicinum
CBS 131.34
Epiphytic
MH855469.1
MH866941.1
Crous et al. (2007)
Untereiner et al.
(1999)
Stenroos et al.
(2010a, b)
Hongsanan (2015a,
b)
Mont (1849)
Of the 209 described species, four species were not
recorded in the NCBI Taxonomy browser, but were
described as incertae sedis by Wijayawardene et al. (2020),
who listed ten genera as incertae sedis. We tested these as
possible out- or in-groups by comparing the resulting bootstrap values. Similarly, species with long branches were reanalyzed as outgroup in ML trees that were run accordingly.
All branches with bootstrap values ≥ 70 % were collapsed,
starting with the first group containing >1 members. The
absolute and relative numbers of collapsed clades were
taken as a parameter of confidence, the ratios (supported/
unsupported clades) were calculated (Table 2), criteria of
quality of trees being a low number of unsupported trees, as
well as a low number of collapsed trees indicating high support of branches of the backbone. Phylogenetic trees were
edited using TREEVIEW v1.6.6 and completed with Adobe
ILLUSTRATOR CS v5. The alignment was deposited in
TREEBASE under accession number 26209.
estimation was executed with a strict clock and birth-death
models. Fossil data of the taxonomic group closest to Eurotiomycetes, i.e. the class Sordariomycetes studied e.g. by
Pérez-Ortega et al. (2016), Liu et al. (2017) and Samarakoon et al. (2019) was used as calibration point (mean: 136
Mya; sigma: 0.5; credibility interval: 95 %). Tree sequences
from Sordariomycetes were included: Meliola centellae,
Cordyceps agriota, and Colletotrichum agaves caricis forcing the monophyletic mode. Similarly, a calibration point
of 100 Mya to the order Capnodiales was included. Default
MCMC options were used. The results were analyzed using
TRACER v1.7.1 and to generate a maximum confidence
of clades in the tree, TREEANNOTATOR v2.6.0 (burn-in
option of 10%) and BEASTv.2.6.1. The tree was visualized
by FIGTREE v1.4.4 and the geological axis was added using
the GEOSCALEPHYLO function from the STRAP R package (https://cran.r-project.org/web/packages/strap) (Fig. 1).
Ecology
Divergence time and evolutionary rate estimation
Fossil-calibrated phylogeny was calculated by the BEAST2
tutorial (https ://beast 2-dev.githu b.io). The concatenated
data set was used as a primary input to BEAST2 analyze
and the choice of the GTR substitution model was based
on pre-analysis using jModelTest v2.0 (Darriba et al. 2012)
and the substitution rate was estimated. The divergence time
We investigated broad ecological trends of 254 species by
consulting original literature, NCBI database, Westerdijk
database, MycoBank (www.MycoBank.org), and Index Fungorum (www.indexfungorum.org); additional information
to extend hypothesized ecological trends per species was
abstracted from specific literature where available. Average
ecologies were summarized as a single symbol per species,
13
Fungal Diversity (2020) 103:47–85
and quantified relative to the number of species recognized
per families (Table 1; Fig. 2). This aimed to extract broad
evolutionary trends per family, which was used to strengthen
or to falsify clades generated by ribosomal data.
94
94
94
94
94
94
94
–
–
94
94
–
70
100
100
100
100
100
100
100
100
100
100
100
99
100
100
100
100
100
100
100
100
100
100
100
100
100
96
95
95
95
95
95
95
95
95
95
95
95
100
100
100
100
100
100
100
100
100
100
100
100
100
93
98
100
100
100
100
100
100
100
100
100
–
–
98
99
70
70
70
70
70
70
70
70
70
70
70
99
71
100
100
100
100
100
100
100
100
100
100
100
100
100
97
97
97
97
97
97
97
97
97
100
100
100
99
14/8
14/8
14/8
14/8
14/8
14/8
14/8
23/32
23/32
27/26
27/26
21/33
13/10
Ancestral character state reconstruction
Epibryon hepaticola
Capronia villosa
Cladophialophora modesta
Cladophialophora hostae,C.scille
Paracladophialophora
Coccodinium bartschii
Bacillicladium dematidis
Capronia nigerrima
Rhinocladiella mackenziei
Arthrophiala arthreospora
Strelitziana
Capnodium without incertae sedis
Capnodium with incertae sedis
cLade 2
13
Clade 1
Bootstrap
Outgroups
Table 2 Outgroup test for long branches base on ML tree
Clade 3
Clade 4
Clade 5
Clade 6
Clade 7
Clade 8
Clade 9
Supported/unsupported clades
1.75
1.75
1.75
1.75
1.75
1.75
1.75
0.72
0.72
1.04
1.04
0.63
1.30
Ratio
58
Trends in evolutionary ancestry and its impact on lineage
and species diversification was analyzed in the following steps: (i) simulation of quantitative traits among the
phylogenetic tree, (ii) stochastical character mapping and
inference of a multi-rate Brownian motion model fitting
and its visualization, (iii) calculation of phylogenetic signals, and (iv) ecological disparity, and comparison to (v)
lineage diversification over time. Discretely valued ecological character traits are listed in Table 1. Discrete characters were converted into continuous states to estimate
their evolution along the previously inferred phylogeny
based on ITS and LSU gene sequences (Fig. 3). Stochastic
character mapping onto the phylogeny was done according to Hulsenbeck et al. (2003) with subsequent fitting of
a multi rate Brownian motion model (Likelihood test for
rate variation in a continuous trait) to estimate evolutionary rates (= Sigma parameter) for each character and to
infer the ancestral state at the root node (O’Meara et al.
2006). Quantitative traits (= ecologies) were simulated
among the phylogeny and were plotted as phenogram to
visualize trait dynamics. To assess the phylogenetic signal of our data we computed the K statistic (Blomberg
et al. 2003) and λ (Pagel 1999) to assess resolution quality
of our dataset. Disparity relative to lineage diversification was calculated to assess success of species cladogenesis according to Pybus & Harvey (2000). Analyses
were done with R statistical software (https://www.r-proje
ct.org/), employing mainly the packages APE (Paradis and
Schliep 2019), PEGAS (Paradis 2010), GEIGER (Pennell
et al. 2014), MAPS (https://cran.r-project.org/web/packa
ges/maps/index .html), TAXONOMIZR (https ://cran.rproject.org/web/packages/taxonomizr/index.html), PHYTOOLS (Revel 2011), and all their reverse dependencies.
We used the functions ‘MAKE.SIMMAP’ for stochastically map characters (i), ‘BROWNIE.LITE’ to model in
the Brownian motion process (ii), and to reconstruct the
ancestral character state. Quantitative trait simulation
(iii), was conducted via the ‘TRAIGRAM’ and ‘PHENOGRAM’ functions as well to plot the Brownian motion
process of character evolution and to visualize the phenotype to the phylogeny (iv). Phylogenetic signal for K and
λ were computed via the function ‘PHYLOSIG’ (vi). To
assess lineage diversification rates we plotted a ‘lineage
through time’ (LTT) via the function ‘LTT’ plot to define
the relative time ratio required for the Chaetothyriales to
give rise to its present lineages. Subsequently, to assess
Fungal Diversity (2020) 103:47–85
59
Fig. 1 Divergence time of the order Chaetothyriales based on ITS and LSU sequences. The bottom scale presents the main geological and periods and eras
morphological disparity we calculated and plotted a disparity through time (DTT) distribution via the function
‘DTT’ (vii). Details of the analysis and compiled scripts
are available upon request.
Results
Phylogeny
The single gene ITS and partial LSU, and combined
sequences of ITS with partial LSU of 254 strains of black
fungi were applied to determine phylogenetic trees of the
entire order Chaetothyriales, using Capnodium salicinum
and Capnodium coffeae as outgroups taxa. The alignment
contained 522 characters for ITS, 497 for LSU, 1019 for
combined sequences. The alignment of combined sequences
had the following base frequencies: f (A) = 00.243, f (T)
= 00.247, f (C) = 00.234, f (G) = 00.275, among which
642 were variable and 548 parsimony-informative sites.
When separate trees of LSU and ITS were compared with
the tree based on the concatenated alignment, bootstrap
values in the combined tree on average were higher than
those found in single-gene trees. Some families did not form
supported clades in single gene trees, but obtained higher
bootstrap support in combined trees. The non-collapsed NJ
tree showed that this algorithm is not suitable for analysis
of Chaetothyriales at ordinal level, judging from the low
number of supported branches. With Bayesian analysis (BA)
(Fig. 3) the combined tree contained a total of 153 supported
clades (posterior probabilities PP ≥ 95%), and with maximum likelihood (ML) 123 supported clades (bootstrap support BS ≥ 70 %). A total of 120 clades were recognized
consistent in the two algorithms; in Fig. 3 both types of
support are indicated by thickness of the branches.
For the reconstruction of the possible evolution of the
order Chaetothyriales, the order of appearance of recognized groups is significant. In most literature on Chaetothyriales, topologies of phylogenetic inferences suggest
the existence of six families (Réblová et al. 2013; Gueidan
et al. 2014; Teixeira et al. 2017). The family Phaeosaccardinulaceae was introduced by Batista and Ciferri (1962)
and is represented by three species (Wijayawardene et al.
2020). The recently described families Strelitzianaceae and
Paracladophialophoraceae have four and two species in the
tree, respectively. Three more groups were added in recent
studies exploring novel habitats (Muggia et al. 2020; Wang
unpublished data). These groups were mostly recognized as
separate clades supported with high bootstrap in the bi-locus
tree with all algorithms applied.
13
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Fungal Diversity (2020) 103:47–85
100%
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
clade 9 clade 5 clade 4 clade 3 clade 7 clade 8 clade 2 clade 6 clade 1
other
epilithic
bryophy c
doma um
carton
epiphy c
opportunis c
Fig. 2 Approximate types of ecology distributed over different
families of Chaetothyriales, normalized to 100%. Pink represents
‘epilithic/lichenolytic’, orange ‘bryophytic’, black ‘ant domatiumassociated’, blue ‘ant-made carton-associated’, green ‘epiphytic’, red
‘opportunistic’; brown unites ‘other’, remaining categories, mainly
soil, water and fungus
Six species, Atrokylindriopsis (Ma et al. 2015), Lichenodiplis (Hawksworth and Dyko 1979), Melnikomyces (Crous
et al. 2014), Bacillicladium (Réblová et al. 2016), Muellerella (Muggia et al. 2020) and Uncispora (Sinclair 1979),
mentioned as having an uncertain phylogenetic position by
Wijayawardene et al. (2020), were included in the ML analysis. Atrokylindriopsis setulosa and Uncispora in Clade 1 had
bootstrap support of 72 %. When Neostrelitziana acaciigena
was added to the tree, it clustered in Clade 6, almost all species of this clade were described as Trichomeriaceae, with
bootstrap support remaining at 100%. Paracladophialophora
formed a sister clade to a cluster of undescribed ant-domatia associated fungi. Lichenodiplis, for which only an LSU
sequence was available, formed a sister clade to a group of
endolichenic fungi (Muggia et al. 2020). Bacillicladium was
monophyletic next to Trichomeriaceae with low bootstrap
support. The tree including the genera above is shown in
Fig. 3. The genera Melnikomyces and Muellerella seemed
remote from Chaetothyriales and were excluded from further
analysis.
In the literature, the following fungi are treated as members of Chaetothyriales, at least by some authors, but were
found at relatively long branches in the ML tree: Epibryon
hepaticola, Capronia villosa, Cladophialophora modesta,
Cladophialophora hostae, Cladophialophora scillae, Paracladophialophora spp., Coccodinium bartschii, Arthrophiala arthreospora, Capronia nigerrima, Bacillicladium dematidis, Rhinocladiella mackenziei, and Strelitziana spp., of
which Coccodinium has been surmised to be dothideaceous
(Hyde et al. 2013). Species were individually rearranged as
outgroups and the effect on statistical support of resulting
ML trees was compared with the supposition as to whether
these are members or non-members, the bootstrap values
should change significantly. Supported and unsupported
clades were calculated; trees with highest ratios supported
13
vs. unsupported clades at a low number of supported clades
in the backbone were considered to be optimal. The ratio
of the combined ML tree including all incertae sedis above
is 1.30 (Table 2). The highest ratios (1.75) were obtained
when Epibryon hepaticola, Capronia villosa, Cladophialophora modesta, Cladophialophora hostae and Cladophialophora scillae, Paracladophialophora spp., Bacillicladium
dematidis, or Coccodinium bartschii were used as outgroup,
the ratios increased slightly compared to the reference tree
(1.30, with Capnodium as outgroup); these species were
consequently regarded as incertae sedis. Four of the items
tested as outgroups, i.e. Capronia nigerrima (0.72), Rhinocladiella mackenziei (0.72), Arthrophiala arthreospora
(1.04), and Strelitziana spp. (1.04) had a negative impact on
the tree and taken as belonging in Chaetothyriales. Bacillicladium dematidis, Cladophialophora modesta, and Capronia villosa, similar to dothidealean Coccodinium bartschii,
appeared as single-species branches in the tree, could not
be affiliated to any of the known families and are therefore
regarded as incertae sedis. Whether or not these species
are members of Chaetothyriales could not be established.
The complete tree including these species was compared
to the same tree without these species, which led to drop of
the ratio to 0.63. The complete tree with Paracladophialophora as outgroup remained the optimal tree, with a high
ratio (1.75) of supported/unsupported branches and with a
relatively low number of clades. This suggest that the group
(Clade 3) represents a separate family, as proposed by Crous
et al. (2016).
The best-fit models of evolution obtained for the different datasets were ITS = TVM+I+G, LSU = GTR+I+G,
combined sequences = TIM2+I+G. No topological conflicts
between the datasets were detected. The ML tree was constructed with GTRGAMMA + I in the CIPRES webserver.
Robustness of trees was tested by comparing different algoritms on the individual datasets of LSU and ITS, and the
combined dataset, placing accent on the backbone by collapsing all supported clades. The best tree is judged to be the
one with the most resolved backbone, i.e. an optimal ratio of
supported/unsupported branches, combined with high support values for all clades, starting at the outermost position
(lowest value) which was variably taken by Capronia villosa
or Cladophialophora modesta (Fig. 4; Table 3). With these
criteria, the Bayesian tree of the combined dataset appeared
to be optimal. Nine well-supported clades were recognized,
which represent five existing families and several uncharacterized groups.
Clade 7 (Chaetothyriaceae) was relatively heterogeneous
with low support, most likely caused by undersampling of
sequence data as compared to the large diversity described
on the natural substrate. One of the two Chaetothyrium
species defining family and order, C. brischoficola, was
found in this clade in several datasets (Fig. 3). The families
Fungal Diversity (2020) 103:47–85
Clade 1 Herpotrichiellaceae
Ecology
epiphy c
opportunis c
carton
epilithic
bryophy c
doma a
other
61
100/95 Cladophialophora minourae CBS 556 83 T
100/97
Phialophora americana CBS 400 67
Phialophora verrucosa CBS 286 47
Cladophialophora subtilis CBS 122642 T
99/86
Cladophialophora yegresii CBS 114405 T
Cladophialophora samoensis CBS 259 83 T
Cladophialophora abundans CBS 126736
Chaetothyriales sp CBS 128945
100/95
Chaetothyriales sp CBS 128948
100/89
Chaetothyriales sp CBS 128935
100/100
Cladophialophora tumbae JCM 28746 T
Cladophialophora mycetomatis CBS 122637 T
100/99
Cladophialophora
tumulicola JCM 28768
100/75
Cladophialophora matsushimae MFC1 P384 T
Cladophialophora lanosa KNU 16032 T
100/98 Chaetothyriales sp CBS 129044
100/99
Cladophialophora chaetospira CBS 114747
100/95
Cladophialophora parmeliae CBS 129337
Cladophialophora boppii CBS 126 86 T
99/85 Chaetothyriales sp MP 2014 T367
Fonsecaea multimorphosa CBS 980 96 T
Cladophialophora arxii CBS 306 94 T
100/76
Fonsecaea minima CBS 125757 T
Fonsecaea erecta CBS 125763
100/97
100/97 Fonsecaea brasiliensis BMU 07620
100/94
Cladophialophora devriesii CBS 147 84 T
Cladophialophora immunda CBS 834 96
100/100100/100 Fonsecaea pugnacius CBS 139214 T
100/98Fonsecaea pedrosoi CBS 271 37 T
Cladophialophora psammophila CBS 110553 T
Cladophialophora emmonsii CBS640 96
100/95
Cladophialophora australiensis CBS 112793
Cladophialophora
potulentorum CBS 114772
100/95
Exophiala alcalophila CBS 520 82 T
100/95
Chaetothyriales sp MP 2014 T22
Chaetothyriales sp MP 2014 T171
100/100 Capronia pilosella AFTOLID 657
Capronia camelliae yunnanensis CGMCC 3 19061 T
100/100Capronia coronata ATCC 56201 T
100/82
Exophiala angulospora CBS 482 92
100/90Chaetothyriales sp CBS 129050
Melanoctona tectonae MFLUCC 12 0389 T
Chaetothyriales sp CBS 129051
100/95 Exophiala bonariae CCFEE 5792 T
100/94
Exophiala opportunistica CBS 122268
Exophiala lacus FMR 3995
100/95
Exophiala cancerae CBS 115142
Exophiala psychrophila CBS 191 87
100/100 Exophiala pisciphila CBS 537 73 T
Exophiala radicis P2854 T
Exophiala equina CBS 116009 T
100/97
Exophiala salmonis CBS 157 67 T
100/97 Veronaea compacta CBS 268 75 T
100/90 Exophiala brunnea CBS 587 66 T
100/98
Veronaea japonica CBS 776 83 T
Veronaea botryosa CBS 254 57 T
99/91 Veronaea constricta CBS 572 90
Chaetothyriales sp CBS 128956
Minimelanolocus asiaticus MFLUCC 15 0237 T
Minimelanolocus curvatus MFLUCC 15 0259 T
Minimelanolocus aquaticus MFLUCC 15 0414 T
Minimelanolocus rousselianus CBS 126086
100/99 Minimelanolocus melanicus MFLUCC 15 0415 T
Minimelanolocus thailandensis MFLUCC 15 0971
99/79 100/100
Thysanorea aquatica MFLUCC 15 0966
Thysanorea papuana CBS 212 96 T
Minimelanolocus obscurus MFLUCC 15 0416
Uncispora sp YMF1 04133
100/100 Exophiala mesophila CBS 402 95
100/100
Exophiala castellanii CBS 158 58 T
100/95
Exophiala lecanii corni CBS 123 33 T
Exophiala attenuata F10685
100/86
Exophiala eucalypti CPC 27630
Exophiala crusticola CBS 119970 T
Capronia parasitica CBS 123 88
Exophiala palmae UPCB 86822 T
100/100 Exophiala spinifera D22I
100/72
100/92 Exophiala exophialae CBS 66876 T
Exophiala oligosperma CBS 127587
Rhinocladiella similis PW3041
100/91
Exophiala jeanselmei CBS 507 90 T
96/73
Rhinocladiella basitona CBS 101460 T
Exophiala polymorpha CBS 138920 T
100/98
98/71
Exophiala hongkongensis HKU32 T
Exophiala nishimurae CBS 101538
100/100
Exophiala italica MFLUCC 16 0245
Exophiala moniliae CBS 520 76 T
Fig. 3 Phylogenetic tree of Chaetothyriales based on ITS and LSU
sequences, obtained by Bayesian analysis and maximum likelihood
(values of ≥ 95% for Bayesian probability and ≥ 70 % for maximum
likelihood shown in bold branches). Capnodium coffeae and Capnodium salicinum were used as outgroup
13
62
Fungal Diversity (2020) 103:47–85
Clade 2 Cyphellophoraceae
Clade 3 Phaeosaccardinulaceae
Clade 4 Doma a
Clade 5
Clade 6 Trichomeriaceae
Fig. 3 (continued)
13
Exophiala nigra CBS 535 94 T
100/96 Exophiala sideris D88
100/77
Exophiala capensis CBS 128771 T
Phaeoannellomyces elegans CBS 101597
Exophiala bergeri CBS 353 52 T
Aculeata aquatica MFLUCC 11 0529
90/93 Capronia kleinmondensis CBS 122671
90/99
Capronia leucadendri CBS 122672 T
Rhinocladiella atrovirens CBS 264 49 T
Capronia dactylotricha CBS 604 96 T
Rhinocladiella quercus CPC 26621 T
Capronia nigerrima CBS 513 69
Exophiala abietophila CBS 145038 T
100/100Chaetothyriales sp MP 2014 T210
100/92 Rhinocladiella phaeophora CBS 496 78 T
100/100
Rhinocladiella aquaspersa CBS 122635
100/94
Rhinocladiella tropicalis RA776
99/78
Rhinocladiella fasciculata CBS 132 86 T
Rhinocladiella anceps AFTOL ID 659
Exophiala lignicola CBS 144622 T
Rhinocladiella coryli CPC 26654 T
Exophiala eucalypticola CBS 143412 T
100/97 Exophiala nidicola FMR 3889 T
Exophiala heteromorpha CBS 232 33 T
100/97
Exophiala dermatitidis CBS 207 35 T
100/98Capronia mansonii CBS 101 67 T
Capronia munkii CBS 615 96 T
Marinophialophora
Atrokylindriopsis setulosa HMAS245592
Capronia fungicola CBS 614 96 T
Capronia acutiseta CBS 618 96 T
Rhinocladiella mackenziei CBS 368 92
100/76 Cyphellophora laciniata CBS 190 61 T
100/92
100/100 Cyphellophora vermispora CBS 228 86 T
Cyphellophora suttonii CBS 449 91 T
Cyphellophora fusarioides CBS 130291 T
Cyphellophora pauciseptata CBS 284 85 T
Cyphellophora gamsii CPC 25867 T
Cyphellophora filicis DP002B
100/100 Cyphellophora eucalypti CBS 124764 T
100/100 Cyphellophora guyanensis CBS 129342 T
Cyphellophora artocarpi CHCJHBJBLM T
100/85
Phialophora intermedia CBS 235 93
Cyphellophora musae GLZJXJ41 T
Cyphellophora olivacea CBS 122 74 T
100/100 Cyphellophora phyllostachydis HLHNZWYZZ08 T
Cyphellophora europaea CBS 101466 T
100/100
Cyphellophora reptans CBS 113 85 T
Cyphellophora pluriseptata CBS 286 85 T
100/97 Cyphellophora livistonae CPC 19433 T
Cyphellophora sessilis CBS 243 85
100/92
100/100
Cyphellophora jingdongensis IFRDCC 2659
Chaetothyriales sp CBS 128959
Cyphellophora oxyspora CBS 698 73 T
100/80
Phialophora capiguarae CBS 131954
Phialophora attae CBS 132767
100/97
Cyphellophora clematidis CBS 144983
Anthopsis deltoidea CBS 263 77
100/100
Paracladophialophora carceris CPC 27596 T
Paracladophialophora cyperacearum CPC 33046 T
Chaetothyriales sp CBS 132003
Chaetothyriales sp Cecr4
Chaetothyriales sp CR13Ceci2
Chaetothyriales sp CBS 128973
100/86
Chaetothyriales sp Trii4
Chaetothyriales sp CBS 135086
Chaetothyriales sp MACrb1
Chaetothyriales sp CBS 132039
Chaetothyriales sp CBS 129057
Chaetothyriales sp CBS 135085
Chaetothyriales sp CBS 134916
100/100 Chaetothyriales sp CBS 134920
100/95
Chaetothyriales sp CBS 134923
Chaetothyriales sp CBS 128966
100/99
Chaetothyriales sp CBS 128963
100/100
Cladophialophora scillae CBS 116461
Cladophialophora hostae CBS 121637
100/99 Chaetothyriales sp A581
Chaetothyriales sp A957
100/96
Chaetothyriales sp A872
Chaetothyriales sp A933
Knufia karalitana CCFEE 5921
Knufia marmoricola CCFEE 6201
Knufia petricola CBS 726 95 T
Knufia perforans CBS 885 95 T
Knufia vaticanii CCFEE 5939 T
Fungal Diversity (2020) 103:47–85
63
Chaetothyriales sp MP 2014 T261
Knufia cryptophialidica DAOM 216555 T
Knufia peltigerae CGMCC 3 17283
Knufia tsunedae FMR 10621
Knufia epidermidis CBS 120353 T
Knufia mediterranea CBS 139721 T
94/86 Arthrocladium tropicale CBS 134926 T
100/100 Arthrocladium fulminans CBS 136243 T
Arthrocladium tardum CBS 127021 T
Arthrocladium caudatum CBS 457 67 T
Bradymyces oncorhynchi CCF 4369 T
100/100
Bradymyces graniticola F6A
100/73
Bradymyces alpinus CCFEE 5493
Neostrelitziana acaciigena CBS 139903 T
Chaetothyriales sp CBS 129049
100/93
Chaetothyriales sp CBS 128958
Chaetothyriales sp CBS 129047
100/100 Anthracinomyces petraeus CGMCC 317315
Anthracinomyces ramosus CGMCC 316367
100/99
Cladophialophora pucciniophila KUS F23645
Arthrophiala arthrospora COAD 658
100/84
Metulocladosporiella musicola CBS 110960 T
Trichomerium dioscoreae 138870 T
Trichomerium deniqulatum MFLUCC10 0884 T
100/100Trichomerium foliicola MFLUCC10 0078 T
Trichomerium gleosporum MFLUCC10 0087 T
100/92
Trichomerium eucalypti CBS 143443 T
100/94 Chaetothyriales sp MP 2014 T13
Chaetothyriales sp MP 2014 T9
100/99
100/100 Chaetothyriales sp CBS 128943
Chaetothyriales sp CBS 129046
100/100
Chaetothyriales sp MP 2014 T333
100/77
Chaetothyriales sp MP 2014 T179
Ceramothyrium melastoma CPC 19837T
100/100 Strelitziana eucalypti CBS 128214
Strelitziana australiensis CBS 124778 T
100/97
100/89 100/100
Strelitziana africana CBS 120037
Strelitziana albiziae CBS 126497 T
Strelitziana cliviae CPC 19822 T
Lithohypha aloicola CPC 35996 T
100/91
Exophiala placitae CBS 121716 T
Cladophialophora proteae CBS 111667 T
Brycekendrickomyces acaciae CBS 124104
100/98
Cladophialophora eucalypti CBS 145551
Exophiala encephalarti CBS 128210
Bacillicladium clematidis
Coccodinium bartschii CPC 13861
100/100
Ceramothyrium aquaticum VTCCF 1210 T
100/86
Ceramothyrium phuquocense VTCCF 1206 T
100/90
Ceramothyrium exiguum VTCCF 1209 T
Ceramothyrium carniolicum CBS 175 95
Chaetothyrium agathis MFLUCC 12 0113 T
100/100 Ceramothyrium ficus MFLUCC 15 0228 T
100/87
Ceramothyrium longivolcaniforme MFLU 16 1306 T
Ceramothyrium podocarpi CPC 19826 T
Nullicamyces eucalypti CPC 32942 T
Ceramothyrium thailandicum MFLUCC 100008 T
Ceramothyrium menglunense MFLUCC 16 1874
Camptophora schimae IFRDCC 2664
Camptophora hylomeconis CBS 113311 T
Exophiala eucalyptorum CBS 121638 T
Aphanophora eugeniae CBS 124105 T
Vonarxia vagans CBS 123533 T
100/72
100/100 Phaeosaccardinula ficus MFLUCC10 0009 T
100/100
Phaeosaccardinula multiseptata IFRDCC 2639T
Phaeosaccardinula dendrocalami IFRDCC 2649 T
100/94
Fumagopsis stellae CBS 145078 T
Chaetothyrium brischoficola MFLUCC 10 0083T
Cladophialophora modesta CBS 985 96
Epibryon interlamellare CBS 126286
Epibryon turfosorum CBS 126587
Cladophialophora sylvestris CBS 350 83 T
100/100
Cladophialophora humicola CBS 117536 T
100/89
Cladophialophora minutissima CBS 121758 T
Epibryon bryophilum CBS 126278
Epibryon hepaticola M10 T
100/100 Chaetothyriales sp L1994
Chaetothyriales
sp L1992
100/99
Chaetothyriales sp L1993
Lichenodiplis lecanorae L
Capronia villosa ATCC 56206
Capnodium coffeae CBS 147 52
Capnodium salicinum CBS 131 34
100/76
Clade7 Chaetothyriaceae
100/100
Clade 8 Epibryaceae
Clade 9
0.20
Fig. 3 (continued)
13
64
Fungal Diversity (2020) 103:47–85
Fig. 4 Outgroup test for long branches base on ML tree. a Cladophialophora modesta as outgroup; b Paracladophialophora sp. as outgroup; c
Rhinocladiella mackenziei as outgroup; d all species without incertae sedis; e all species including incertae sedis
Phaeosaccardinulaceae and Strelitzianaceae were found as
part of the Chaetothyriaceae cluster; their family status is
doubtful. Clade 1 (Herpotrichiellaceae) were also found
to be diverse and resolved into two groups in some of the
trees. The remaining families Cyphellophoraceae (Clad 2),
Epibryaceae (Clade 8), and Trichomeriaceae (Clade 6) had
consistent support. Three further clades had consistently
high support values, i.e. a group of ant-domatia associated
species (Clade 4) and two clusters of endolichenic species
(Clade 5 and Clade 9).
Family Trichomeriaceae (Clade 6) comprised 50 strains,
ten of which represented as yet undescribed species from
an ant carton. Two species, Metulocladosporiella musicola
and M. musae, were originally thought to belong to Herpotrichiellaceae (Crous et al. 2006), but in our tree clustered in Trichomeriaceae. The type strains of three species,
Cladophialophora pucciniophila, Cladophialophora proteae and Cladophialophora eucalypti also clustered in this
clade, although the type species of Cladophialophora, C.
ajelloi (= C. carrionii) is a member of Herpotrichiellaceae.
Exophiala placitae and Exophiala encephalarti should morphologically belong to Herpotrichiellaceae, but cluster in
Trichomeriaceae.
Clade 4 comprised a total of 15 strains originating from
ant domatia inside plant stems, known as domatia. Species typically produce sympodial conidia with flat conidial
scars, and sometimes have additional catenate conidial states
13
(Wang unpublished data). The clade has sufficient support
and ecological homogeneity to be recognized as a separate
family. Two species, reported as causing leaf spots on different plant hosts (Crous et al. 2007), described after their plant
hosts as Cladophialophora scillae and C. hostae, had exclusively catenate micromorphology. They cluster in one clade
with a long branch, and upon taking them as outgroups, the
general support values of tree improved (ratio rise from 1.30
to 1.75); consequently, Cladophialophora scillae and C. hostae are listed here as incertae sedis.
Clade 2 with 100% (ML/BI) bootstrap support contains
25 species belonging to family Cyphellophoraceae. Twenty
strains described Cyphellophora species are clustered in this
clade together with four Phialophora species (P. livistona,
P. attae, P. capiguarae, and P. intermedia), together with
a strain from the ant-made carton strain (CBS 128959).
Cyphellophora and Phialophora traditionally differ by
conidial shape, either lunate and septate, or subsphaerical,
respectively, but the type species of Phialophora, P. verrucosa, is a member of the ‘carrionii-clade’ in Herpotrichiellaceae (de Hoog et al. 2011).
Clade 7 contains 21 species belonging to Chaetothyriaceae. The clade is well-supported in ML and BI trees
(73/100). Inter-specific distances are relatively large due to
incomplete taxon sampling. Members of this family have
been reported since the 19th century after their ascomata on
the natural substrate; culture and sequence data are available
Fungal Diversity (2020) 103:47–85
65
Table 3 Overview of genera described in Chaetothyriales, with number of species in brackets
Family
Genus
Chaetothyriaceae Hansf. ex Chaetothyrium Speg. 1888
(T) (67)
M.E. Barr 1979 (T)
Euceramiaceae Bat. & Cif.
1962
Phaeosaccardinulaceae Bat.
& Cif. 1962
Type species
Chaetothyrium guaraniticum Speg. 1888, NT C.
agathis
Actinocymbe v. Hoehn. 1911 Actiniopsis separato-setosa
(3)
Henn. 1908
Ainsworthia Bat. & Cif.
Ainsworthia zanthoxyli Bat.
1962 (1)
& Costa 1962
Aithaloderma Syd. & P.
Aithaloderma clavatisporum
Syd. 1913 (12)
Syd. & P. Syd.
Almeidaea Cif. & Bat. 1962 Chaetothyrium vermisporum
(1)
Hansf. 1946
Aphanophora Réblová &
Cyphellophora eugeniae
Unter. 2013 (1)
Crous & Alfenas 2009
Arthrophiala Lisboa et al.
Arthrophiala arthrospora
2016 (1)
Lisboa et al. 2016
Batistaella Ciferri 1962 (2) Phaeosaccardinula coumae
Bat. & Vital 1955
Camptophora Réblová &
Cyphellophora hylomeconis
Unter. 2013 (2)
Crous et al. 2007
Capnobatista Cif. & Leal
Capnobatista serrulata Cif.
1962 (1)
& Leal 1962
Ceramothyrium Bat. & Maia Ceramothyrium paiveae
1956 (39)
Bat. & Maia 1956, REF
C. thailandicum
Ceratocarpia Rolland 1896 Ceratocarpia cactorum Rol(3)
land 1896
Chaetasterina Bubak 1909
Asterina anomala Cooke &
(1)
Harkness 1881
Chaetopotius Bat. 1951 (2) Chaetopotius commistum
Bat. 1951
Chaetothyriomyces Pereira- Chaetothyriomyces brasilCarv. et al.
iensis Pereira-Carv. et al.
Cyphellophoriella Crous & Cyphellophoriella pruni
A.J. Smith
Crous & A.J. Smith
Euceramia Bat. & Cif. 1962 Euceramia palmicola Bat.
(1)
& Cif. 1962
Fumagopsis Speg. 1910 (3) Fumagopsis triglifioides
Speg. 1911
Gilmania Bat. & Cif. 1962
Setella buchenaviae Bat. &
Lima 1955
Kazulia Nag Raj 1977 (2)
Ypsilonia vagans Speg. 1908
Microcallis Syd. 1926 (9)
Microcallis phoebes Syd.
1926
Neostrelitziana Crous &
Neostrelitziana acaciigena
Wingf. 2015
Crous & Wingf. 2015
Nullicamyces Crous 2018
Nullicamyces eucalypti
(1)
Crous 2018
Phaeopeltis Clem. 1909 (2) Phaeosaccardinula diospyricola Henn. 1905
Phaeosaccardinula Henn.
Phaeosaccardinula diospy1905 (41)
ricola Henn. 1905, REF
P. ficus
Sphaerochaetia Bat. & Cif. Meliola loganiensis Sacc. &
1962 (1)
Berl. 1885
Type material
Suggested identity
IF550893
Chaetothyrium
Type unknown
Doubtful
Illeg., non Ainsworthia
1844
Syd. Fung. Exot No. 174
Invalid
Illeg., non Almeidaea 1903
Invalid
CBS 124105
Aphanophora
VIC 30505
Arthrophiala
Type lost
Doubtful
CBS 113311
Camptophora
Reynolds 1982
Trichomerium
Type lost
Ceramothyrium
Type lost
Doubtful
Limacinula (Coccodiniaceae)
Reynolds 1982
Excluded
Trichomerium
UB12116
No sequence data
CBS 140001
Cyphellophoriella
Invalid
Invalid
LPS
Fumagopsis
Incertae sedis
Excluded
LPS
Syd. Fung. Exot No. 161,
170h
CBS 139903
Vonarxia
Excluded
CBS 144426
Ceramothyrium
Name change
Superfluous
IFRD 9041
Phaeosaccardinula
Nom. inval., Art. 41.1
Doubtful
Chaetothyrium
Neostrelitziana
13
66
Fungal Diversity (2020) 103:47–85
Table 3 (continued)
Family
Strelitzianaceae Crous &
Wingf. 2015
Genus
Type species
Type material
Suggested identity
Stanhughesia Constant. (4)
Halbaniella linnaeae Dearn.
1929
Strelitziana africana Arzanlou & Crous 2006
Treubiomyces pulcherrimus
v. Hoehn. 1907
Trotterula chilensis Speg.
1921
Halbaniella linnaeae Dearn.
1929
Vonarxia anacardii Bat. &
Bezerra 1960
Wiltshirea quercifolia Bat.
et al. 1962
Yatesula calami Syd.
Meliola loganiensis Sacc. &
Berl. 1885
Cyphellophora laciniata de
Vries 1962
Anthopsis deltoidea Fil.
March et al. 1977
Kumbhamaya indica Jacob
& Bhat 2000
Paracladophialophora carceris Crous & Roets 2016
Coleroa casaresii var. plagiochilae Fragoso 1919
Herpotrichiella moravica
Petr. 1914
Aculeata aquatica Dong
et al. 2018
Pseudobeltrania selenoides
de Hoog 1977
Atrokylindriopsis setulosa
Ma & Zhang 2015
Sphaeria nigerrima Bloxam
1859
Botrytoides monophora
Moore & Almeida 1937
Sphaeria sexdecimspora
Cooke 1871, REF Capronia pilosella
Melanomma pleisporum
Mouton 1886
Sphaeria sexdecimspora
Cooke 1871
Hormodendrum pedrosoi
Brumpt 1922
Cladophialophora ajelloi
Borelli 1980
Dictyotrichiella pulcherrima
Munk 1953
Didymotrichiella inconspicua Munk 1953
Anamorph
Ceramothyrium
CBS 120037
Strelitziana
Type lost
Doubtful
Speg. 1918 Fig.
Chaetothyrium
Dearness
Superfluous
ET CBS 123533
Vonarxia
PH205
Phaeosaccardinula
PNH 25031
Type lost
Doubtful
Doubtful
CBS 190.61
Cyphellophora
CBS 263.77
Anthopsis
Jacob GUFCC-02 (PC)
Cyphellophora
CBS 142068
Paracladophialophora
Type unclear
Epibryon
Type lost
Capronia
MFLU 11-1094
Aculeata
IMI 107006-IIe
No sequence data
HSAUP H4560
Atrokylindriopsis
CBS 513.69
Capronia
CBS 269.37
Phialophora
AFTOL 657
Capronia
Nomen confusum
Doubtful
Strelitziana Arzanlou &
Crous 2006 (8)
Treubiomyces v. Hoehn.
1909 (7)
Trotterula Speg. 1921 (1)
Uloseia Bat. 1963 (1)
Vonarxia Bat. 1960 (2)
Wiltshirea Bat. & Peres
1962 (1)
Yatesula Syd.
Zukalia Sacc. 1891 (33)
Cyphellophora de Vries
1962 (25)
Anthopsis Fil. March. et al.
1977 (3)
Kumbhamaya M. Jacob &
Bhat 2000 (1)
Paracladophialophoraceae Paracladophialophora
Crous 2018
Crous & Roets 2016 (2)
Epibryaceae Stenroos &
Epibryon Döbbeler 1978
Guiedan 2014
(T) (47)
Herpotrichiellaceae Munk Herpotrichiella Petr. 1914
1953
(T)
Aculeata Dong et al. 2018
Cyphellophoracere
Reblova & Unter. 2013
Ardhachandra Subram. &
Sudha (5)
Atrokylindriopsis Ma &
Zhang 2015
Berlesiella Sacc. 1888 (11)
Botrytoides Moore &
Almeida (1)
Capronia Sacc. 1883 (81)
Caproniella Berl. 1896 (1)
Caproniella Berl. 1899 (1)
Carrionia Bric.-Irag. 1939
Cladophialophora Borelli
1980 (41)
Dictyotrichiella Munk (6)
Didymotrichiella Munk (1)
13
Illeg., non Caproniella Berl. Invalid
1896
Name change
Superfluous
CBS 160.54
Cladophialophora
CBS 609.96
Capronia
Unknown
Capronia
Fungal Diversity (2020) 103:47–85
67
Table 3 (continued)
Family
Genus
Type species
Type material
Suggested identity
Exophiala Carmichael 1967
(59)
Fonsecaea Negroni 1936
(16)
Foxia Castell. 1908 (1)
Exophiala salmonis Carmichael 1967
Hormodendrum pedrosoi
Brumpt 1922
Microsporum mansonii
Castell. 1905
Hormodendrum pedrosoi
Brumpt 1922
Marinophialophora garethjonesii Li et al. 2018
Melanchlenum eumetabolus
Calendron 1953
Sphaeria porothelia Berk. &
Curtis 1876
Melanoctona tectonae Tian
Cladosporium musae Mason
1945
Pseudospiropes navicularis
Castañeda 1987
Nadsoniella nigra Issatch.
1914
Phaeoannellomyces elegans
McGinnis & Schell 1985
Phialoconidiophora
guggenheimia Moore &
Almeida 1937
Phialophora verrucosa
Medlar 1915
Pleomelogramma argentinensis Speg. 1909
Herpotrichiella polyspora
Barr 1959
Rhinocladiella atrovirens
Nannf. 1934
Sympodina coprophila Subram. & Lodha 1964
Periconiella papuana
Aptroot
Veronaea botryosa Cif. &
Mont. 1957
Wangiella dermatitidis
McGinnis 1977
Limacinia coffeicola Puttemans 1904, NT T. foliicola
Arthrocladium caudatum
Papendorf 1969
Bacillicladium lobatum
Hubka et al. 2016
Bradymyces oncorhynchi
Hubka et al. 2014
Brycekendrickomyces acaciae Crous & Wingf.
Brycekendrickomyces acaciae Crous & Wingf.
CBS 157.67
Exophiala
CBS 271.37
Fonsecaea
Nomen nudum
Doubtful
CBS 271.37
Phialophora
MFLUCC 16-1449
Marinophialophora
CBS 264.49
Rhinocladiella
Type lost
Doubtful
MFLUCC 12-0389
CBS 161.74
Melanoctona
Metulocladosporiella
Unknown
Minimelanolocus
CBS 535.94
Exophiala
CBS 122.95
Exophiala
CBS 272.37
Fonsecaea
NT CBS 140325
Phialophora
Type lost
Doubtful
Type lost
Capronia
CBS 264.49
Rhinocladiella
CBS 350.65
Veronaea
CBS 212.96
Thysanorea
CBS 254.57
Veronaea
CBS 207.35
Exophiala
MFLUCC10-00780
Trichomerium
CBS 457.67
Arthrocladium
CBS 141.179
Bacillicladium
CBS 133066
Bradymyces
CBS 124104
Brycekendrickomyces
CBS 124104
Brycekendrickomyces
Hormodendroides Moore &
Almeida (1)
Marinophialophora Li et al.
2018 (1)
Melanchlenus Calandron
1953 (2)
Melanostigma Kirschst.
1939 (1)
Melanoctona Tian 2016 (1)
Metulocladosporiella Crous
et al. 2006 (6)
Minimelanolocus Castañeda
& Heredia 2001 (34)
Nadsoniella Issatch. 1914
(4)
Phaeoannellomyces McGinnis & Schell 1985 (1)
Phialoconidiophora Moore
& Almeida 1937
Phialophora Medlar 1915
(63)
Pleomelogramma Speg.
(1909)
Polytrichiella Barr (3)
Trichomeriaceae
Chomnunti et al. 2012
Rhinocladiella Nannf. 1934
(21)
Sympodina Subram. &
Lodha 1964 (1)
Thysanorea Arzanlou et al.
2007 (14)
Veronaea Cif. & Mont.
1957 (1)
Wangiella McGinnis 1977
(3)
Trichomerium Speg. 1918
(36)
Arthrocladium Papendorf
1969 (4)
Bacillicladium Hubka et al.
2016 (2)
Bradymyces Hubka et al.
2014 (3)
Brycekendrickomyces Crous
& Wingf. 2009 (1)
Brycekendrickomyces Crous
& Wingf. 2009 (1)
13
68
Fungal Diversity (2020) 103:47–85
Table 3 (continued)
Family
Genus
Type species
Type material
Suggested identity
Knufia Hutchinson & Unter.
1996 (14)
Lithohypha Selbmann &
Isola 2017 (1)
Lithophila Selbmann &
Isola 2015 (1)
Neophaeococcomyces Crous
& Wingf. 2015 (2)
Knufia cryptophialidica
Hutchinson & Unter. 1996
Lithophila guttulata
Selbmann & Isola 2015
Lithophila guttulata
Selbmann & Isola 2015
Phaeococcomyces aloes
Crous & Wingf. 2013
DAOM 216555
Knufia
CCFEE 5907
Lithohypha
Illeg., non Lithophila 1788
Lithohypha
CBS 136431
Neophaeococcomyces
Accepted families in bold
REF proposed reference, T type, ET epitype, NT neotype
of only a fraction of these. Appropriate description of the
family Chaetothyriaceae is therefore as yet impossible.
Clade 8 contains members of Epibryaceae, with 100%
ML and 100% BI bootstrap support. The phylogeny of this
family also suffers from a severe taxon sampling effect, as
of the 47 species listed in Index Fungorum, only seven are
available in GenBank. Of these, Epibryon hepaticola clusters at some distance from remaining taxa, but given the
poor representation of extant biodiversity this is probably
insignificant. When E. hepaticola was treated as outgroup,
the ratio rose from 1.30 to 1.75; consequently, the species is listed as incertae sedis. This clade also contained
three species belonging to Cladophialophora, classified as
such on the basis of catenate conidia. The original strain
of Cladophialophora minutissima was isolated from bryophytes, while other Epibryon species had been described
on the basis of their ascomata produced inside moss thalli;
obviously this Cladophialophora is a cultural state of an
Epibryon species. Cladophialophora humicola and C. sylvestris were derived from soil and decaying pine needles,
respectively. The cladophialophora-type of conidiation is
common throughout the entire order Chaetothyriales.
Herpotrichiellaceae (Clade 1) is best represented by
sequence data, because a large part of the known species
was described from isolates in culture, thus only representing the asexual state. Traditionally, species were described
after their ascomata on the natural substrate, classified in
the genus Capronia. Index Fungorum lists 89 described species, of which 85 belong to Herpotrichiellaceae and one to
Trichomeriaceae. For a total of 119 strains in Herpotrichiellaceae, sequence data were available, including 11 carton
fungi. It is unknown whether these are asexual isolates of
known sexual species; the connection between sexual and
asexual morphs has been made only occasionally (Müller
et al. 1987; Untereiner 1997). The core structure of Herpotrichiellaceae was poorly resolved. The group fell apart
into several, poorly supported subclusters. On the basis
of LSU-data, de Hoog et al. (2011) distinguished a number of approximate clades within the family, of which the
13
‘bantiana-clade’ and the ‘carrionii-clade’ could be recognized. In a third, large remainder of species, numerous novel
taxa had been added since 2011; no clades or clusters could
be distinguished.
Nomenclature
The order Chaetothyriales was validated by Barr (1987a, b)
for epiphytic sooty molds mostly producing setose, clypeolate ascomata containing dark, multi-celled ascospores, with
Chaetothyriaceae (Barr 1979) as type family. The invalidly
described families Phaeosaccardinulaceae and Euceramiaceae (Batista and Ciferri 1962) were regarded as synonyms
(Barr 1987a, b).
Chaetothyriaceae had provisionally been introduced by
Hansford (1946) with Chaetothyrium, based on C. guaraniticum Speg., as the type species. The original dried material of the type species, described in 1888, insufficiently
allows interpretation. The Index Fungorum lists 76 published names in Chaetothyrium, of which 67 are accepted
as members of Chaetothyriaceae. However, GenBank
contains only two sequenced species, viz. Chaetothyrium
agathis (Liu et al. 2015) and C. bischofiicola (Chomnunti
et al. 2012b), both isolated on a single occasion from leaves
of tropical plants. It remains uncertain whether this is in
accordance with the intention of Spegazzini (1888), but
numerous authors maintained the ecological concept of
‘sooty moulds’, i.e. epiphytic colonizers of living plants: at
least 64 of the 67 species mentioned above were described
from plant leaves, generally without symptoms. In order to
stabilize the nomenclatural reference of Chaetothyriales,
we herewith propose Chaetothyrium agathis Hongsanan &
K.D. Hyde (Liu et al. 2015) as a neotype of Chaetothyrium.
Chaetothyrium agathis takes a central position in the clade
of Chaetothyriaceae (Fig. 3) and is the reference point of the
order Chaetothyriales. Wijayawardene et al. (2020) listed
the genus Aithaloderma in the Chaetothyriaceae. Hansford
(1946) reexamined the type of A. clavatisporum which
Fungal Diversity (2020) 103:47–85
displayed a Triposporium asexual state, and reclassified it
in Chaetothyrium.
Chaetothyriaceae further comprises the genus Ceramothyrium. This genus is listed with 41 names in Index Fungorum, of which 39 are surmised to belong to Chaetothyriaceae. The type species is Ceramothyrium paivieae (Batista
1956), originally reported from leaves of Paivea langsdortii
(= Copaifera langsdorfii; Leguminosae) in Brazil. No
molecular data are available for this species. Judging from
older literature, this genus is also reserved for species colonizing plant leaves, with 37 of 39 species demonstrating this
ecology, including the nine species of which LSU sequences
are available in GenBank. Of these, Ceramothyrium thailandicum colonizes living leaves of Lagerstroemia (Lythraceae)
in Thailand. Awaiting selection of neotype material which is
closer to the original type location of Batista (Batista 1956),
we regard Ceramothyrium thailandicum as the reference species for Ceramothyrium in the present paper.
Phaeosaccardinula, introduced by Hennings (1905)
with type species P. diospyricola on leaves of Diospyros
(Ebenaceae) in Amazonian Brazil, contains 47 species in
Index Fungorum, of which 41 were regarded as members of
Chaetothyriaceae. The genus currently has six synonymous
generic names (Table 3), all containing a very small number of species that were mostly discarded for nomenclatural
reasons. In accordance with the type species P. diospyricola,
nearly all authors in older literature classified plant-colonizing species in the genus. Of three species, LSU sequences
are available in GenBank, í.e. P. dendrocalami and P. multiseptata (Yang et al. 2014), and P. ficus (Chomnunti et al.
2012b), all from living plant leaves, in (sub)tropical China
and Thailand, respectively. In absence of sequence data of
the remaining 39 species of Phaeosaccardinula, we regard
these species as representative for the genus, with P. ficus
as reference.
Two species are known in Vonarxia of which V. anacardii is the type species (Batista 1960). The species is in
poor condition (van der Aa and von Arx 1986) and is currently judged to be of uncertain affinity (Index Fungorum),
while V. vagans has been sequenced and described by several authors (Réblová et al. 2013; Crous et al. 2009). That
taxon, based on Ypsilonia vagans Speg. on leaves of Spiraea
cantonensis (Rosaceae) in Brazil, has setose sporodochia
with splayed stauroconidia. Crous et al. (2009) epitypified
the species with CBS 123533 as the type culture. Given the
unclear status of the type species V. anacardii, we might
regard V. vagans as a reference species for the genus Vonarxia, but it should be noted that it is also the type species
of Kazulia (Raj 1977). The morphologically similar genus
Fumagopsis was described by Spegazzini (1910) with F.
triglifioides, on living leaves of Lucuma neriifolia (Sapotaceae) in Argentina, as the type species. Using the dried
herbarium specimen of the holotype, van der Aa and van
69
Oorschot (1985) redescribed this specimen. It is characterized by setose sporodochia bearing stauroconidia, similar
to those of Vonarxia vagans but differing by the conidia
being pronouncedly multicellular. Fumagopsis triglifioides
has as yet not been sequenced. Three species records of
Fumagopsis are listed in Index Fungorum, but only one, F.
stellae, CBS 145078 from leaves of Eucalyptus (Myrtaceae)
in Australia, has been deposited in NCBI. This species had
similar morphology, with setose sporodochia and multicellular stauroconidia on the natural substrate, and sequences
placed it in Chaetothyriales (Crous et al. 2018). Numerous
other sporodochial, morphologically reminiscent genera
have been described, such as Zelopelta (Sutton and Gaur
1984), Phalangispora (Nawawi and Webster 1982), which
are in need of modern sequence data.
Four small genera were recently described for which
sequence data are available, i.e. Aphanophora, Arthrophiala, and Camptophora. All type species of these genera
(Table 3) cluster in the supported clade of Chaetothyriaceae
(Fig. 3), all at relatively long branches, underlining their
position as separate genera. Nullicamyces clusters amidst
species of Ceramothyrium in a cluster that is however not
supported (Fig. 3). Stanhughesia was described as Ceramothyrium asexual states (Constantinescu et al. 1989). Species
of Microcallis have been reclassified in Chaetothyrina which
is a genus of Micropeltidaceae.
Cyphellophoraceae was introduced by Réblová and
Untereiner (Réblová et al. 2013) with Cyphellophora (de
Vries 1962) as the type genus and C. laciniata as the type
species. CBS 190.61 is available as the type strain, and the
taxon has several genes in GenBank. Currently, 28 species have been described in the genus, two of which were
transferred as independent genera of Chaetothyriaceae (C.
eugeniae as type of Anaphora, and C. hymeloconis as type
of Camptophora) and one, C. suttonii, has been excluded.
Another genus of this family is Anthopsis, based on A.
deltoidea as type species with CBS 263.77 as type strain
(Moussa et al. 2017a, b).
Trichomeriaceae was introduced by Chomnunti et al.
(2012b) with Trichomerium as type genus. This genus is
based on the sooty mold Limacinia coffeicola Puttemans
[non Phaeosaccardinula coffeicola (Maharachchikumbura
et al. 2018)] as the type species (Puttemans 1904). Reynolds
(1983) judged this species as being close to or identical to T.
grandisporum, which he considered as the only recognized
species in Trichomerium with a large number of synonymous
names. No living ex-type material was available to recent
authors (Chomnunti et al. 2012a), who consequently took
T. foliicola, with sequence data, as reference for genus and
family. From their extensive illustrations of the sexual state
of this fungus, it appears that the ascigerous fruit bodies of
Trichomerium are morphologically very similar to those of
Capronia, the rather monomorphic sexual state observed
13
70
in numerous species of Herpotrichiellaceae. Conidia were
not observed, but several members of Trichomeriaceae [e.g.
Trichomerium gloeosporum (Hongsanan et al. 2016a) and T.
changmaiensis (Maharachchikumbura et al. 2018)] produce
elaborate stauroconidia.
The family Epibryaceae was introduced by (Gueidan
et al. (2014) with Epibryon (Döbbeler 1978, 1980) as type
genus which has Epibryon plagiochilae as the type species.
This species was described with molecular data by Stenroos
et al. (2010a, b) in a detailed overview of the genus, and is
accepted here as reference for this group of phylogenetically
consistent moss endophytes.
The best-known family in the order Chaetothyriales is
Herpotrichiellaceae, introduced by Munk (1953) with
Herpotrichiella (Petrak 1914) as the type genus. Herpotrichiella moravica was selected as the type species,
which is considered to be a synonym of Capronia pilosella
(Untereiner 1997). Consequently, the currently accepted
name for Herpotrichiella is that of its older synonym Capronia, introduced by Saccardo (1883) with Capronia sexdecimspora (Cooke) Sacc. as type species, characterized by
setosa ascomata with asci containing 16 hyaline, 3-4-septate
ascospores. As no interpretable type material of this species
is available, the identity of this species remains uncertain.
As yet, none of the species with 16-spored asci has been
sequenced, and thus replacement of C. sexdecimspora by
an extant neotype is difficult and the exact position of the
reference for Capronia in the Herpotrichiellaceae remains
uncertain. We propose to stabilize the nomenclature of Herpotrichiellaceae by selecting Capronia pilosella AFTOL 657
as reference for the family.
A large number of Capronia species has been subsequently described (e.g. Barr 1987a, b; Friebes 2012), of
which Index Fungorum considers 81 to be of chaetothyrialean affinity. The family Herpotrichiellaceae comprises 30
generic names (Table 3), which are principally available for
a future taxonomic rearrangement with phylogenetic affinity
as leading principle and which therefore are in need of redefinition with reference material. The oldest name of these
is Berlesiella, based on Sphaeria nigerrima Bloxam 1859,
which in spite of absence of usable type material is now considered to be Capronia nigerrima (Barr 1991). Sequenced
material of this species is available from Untereiner and
Naveau (1999) who used strain CBS 513.69 described by
Müller et al. (1987). Caproniella was introduced (Berlese
1896) with Melanomma pleiosporum as a single species,
now known as Capronia pleisporum (MycoBank), but no
recent material is known to be available. Berlese (1899) used
Caproniella with Sphaeria sexdecimspora as the type. This
generic name is superfluous as S. sexdecimspora was the
type of Capronia, and Caproniella Berlese 1899 is a later
homonym of Caproniella Berlese 1896. For these reasons
we consider Caproniella as a nomen confusum. Moussa et al.
13
Fungal Diversity (2020) 103:47–85
(2017a, b) noted that Foxia and Melanchlenus were invalid
due to absence of descriptions in the protologues. Most of
the remaining genera are represented by extant type strains
with molecular data (Table 3).
Ecology and evolution
Members of Chaetothyriales have a rich ecological diversity,
with a general tendency to extremotolerance (Gostincar et al.
2019) and toxin management (Teixeira et al. 2017). The difficulty to isolate the fungi from the environment (Sudhadham
et al. 2008, Vicente et al. 2008) interferes with understanding of the preferred ecological niche. Available data may
provide distorted information since unspecific habitats may
have been sampled thus far. For example, Cyphellophora
europaea is commonly encountered colonizing human nails.
It has been found in bathrooms where this fungus is likely
to have been acquired by the patients. A natural habitat has
not been found, but colonization of moist surfaces suggests
oligotrophy. For only a small number of species of Cyphellophoraceae, environmental data are available. Numerous
species have been described from a single strain on a single
host plant, without indication of a specific plant-pathogenic
lifestyle. We have assumed oligotrophy for these species as
well, listing them as colonizers of the phyllosphere with an
epiphytic lifestyle.
Ecologies of 254 strains and their relatives in Chaetothyriales were investigated (Table 1). Many species of
Chaetothyriales have been described from single collections and hence epidemiological investigations are problematic. Habitat data were abstracted from the sampling
sites of strains described in the original publications, supplemented with a summary of ecological trends per species abstracted from the literature. Seven categories were
summarized as follows, ‘epilithic/lichenolytic’ (on bare or
parasitizing on lichens), ‘epiphytic’ (colonizing plant leaves
without symptoms), ‘opportunistic’ (deep, single- or multiorgan infection in humans, also infection in cold-blooded
vertebrates), ‘carton’ (carton of chewed wood in ant nests),
‘domatium’ (ant nest inside living plant stem), ‘bryophytic’
(endophytic in mosses), and ‘other’ (aquatic, fungicolous,
in soil). Members of the family Herpotrichiellaceae showed
highly diverse ecological sources. In a total of 119 strains,
five ecologies were distinguished. In the main categories,
38 strains derived from opportunistic infections, 30 from
other, 36 were epiphytic, 4 were epilithic/lichenolytic, while
11 as yet undescribed strains had been isolated from carton
material in ant nests.
Available information on members of Cyphellophoraceae
was scant, not allowing definitive conclusions. Several
species were isolated from living plants, but it remained
unclear whether this was an infectious process, or epiphytic
growth without notable invasion. Data are abstracted from a
Fungal Diversity (2020) 103:47–85
summary given by Feng et al. (2014). Cyphellophora europaea is the only common species of the family. It is a commensal or mild infectious agent on human skin and nails, and
was repeatedly isolated in bathrooms where the fungus was
suggested to be picked up (Lian and de Hoog 2010); for this
reason, we prefer ‘opportunistic’ as its ecology. In total, four
ecology types are observed in this family. Given the frequent
plant origin without clear description of disease, we listed
the main ecology as ‘epiphytic’ (44%).
Members of Trichomeriaceae are surface colonizers: 42
% of the species were isolated from rock. Knufia epidermidis was originally described as repeatedly being involved
in mild nail infections (Li et al. 2008), but Zakharova et al.
(2013) found the same fungus occurring as a rock colonizer
with an ecology similar to remaining Knufia species. 38 %
of members of Trichomeriaceae reportedly were derived as
‘sooty molds’ from plants which often had somewhat leathery leaves. Since these were single sampling events and no
reports about plant disease have been published, we listed all
species as being epiphytic. The species of Bradymyces had
single isolation events (rock and fish) for which no common
denominator could be found.
Members of Chaetothyriaceae have nearly always been
reported from living plants. Detection was generally by
ascomata on the natural substrate, which eventually were
immersed on a stroma fixed to the undamaged host tissue.
We listed those members as ‘epiphytic’; only 10% of the
species were described from other habitats.
Clade 4 contains a major subclade of 15 strains that
were derived exclusively from domatia of tropical ants. The
second subclade contained two species with cladophialophora-like morphology which caused leaf spots on their
host plants; they are known from single sampling events.
Two more undescribed clades (Clades 5 and 9) were noted
which all were derived from rock environments (Muggia
et al. 2020).
Epibryon species are fungi forming small ascomata inside
moss tissue. Index Fungorum lists 48 species, most of which
have been described after material on the host and could
not be included in this study for lack of sequence information. Three cladophialophora-like species clustered in the
Epibryaceae, of which C. minutissima was derived from
mosses without observation of the ascigerous state. The
ecologies of the five cultured Epibryon species are consistently bryophilous.
Of the distinguished ecological categories, epilithic and
epiphytic are commonly encountered in several families
(Herpotrichiellaceae, Trichomeriaceae, Cyphellophoraceae,
Chaetothyriaceae, and Clades 5 and 9). Also carton-material
of ant nests and tunnels is widely distributed (Herpotrichiellaceae, Trichomeriaceae and Cyphellophoraceae). Human
infection is nearly exclusively found in Herpotrichiellaceae,
occasionally in Trichomeriaceae, and restricted to mild,
71
superficial infections in Cyphellophoraceae. Infections in
cold-blooded vertebrates are restricted to Herpotrichiellaceae. Dominant ecology in Clades 9 and 5 is ‘epilithic’;
in Epibryaceae this is ‘bryophytic’, in Clade 4 ‘ant-domatium associated’, in Chaetothyriaceae ‘epiphytic’, and in
Trichomeriaceae it is ‘epiphytic’. The overview contains 39
ant-associated strains, isolated either from carton material
of nests and tunnels, or from domatia inside living plants.
The latter type (15 entries) is restricted to Clade 4, while
carton-associated species (24 entries) have a wide distribution in Herpotrichiellaceae, Trichomeriaceae and Cyphellophoraceae and are not found in Clade 4, confirming data
of Voglmayr et al. (2011) and Nepel et al. (2014).
The evolutionary time estimation (Fig. 1) reveals that the
Chaetothyriales crown order emerged in the late Devonian
Period. Between the end of the Cretaceous, i.e. 151.69 Mya,
the family was split, separating Clade 8, Epibryion hepaticola M10, Clade 9 and Capronia villosa from the remaining species. Fundamental speciation events occurred through
the Cretaceous and Paleocene periods. The formation of the
family Chaetothyriaceae (Clade 7) appears ancestral, starting about 122 Mya. The diversification of the family Herpotrichiellaceae was later, around 111 Mya (Fig. 1).
Ancestral character state reconstruction
In a first step, ecological traits were plotted model-free on
to the phylogeny via the function ‘phenogram’ over time,
in order to determine approximate number of ancestral
trait changes (Fig. 5). Seven major directions of trait evolution are obvious (1–7 in Fig. 5). Although the phenogram
does not indicate the exact ancestral state to the Chaetothyriales, particularly the traits ‘epiphytic’ and ‘epilithiclichenicolous’ (branching point 1) suggests ancestry as a
‘epilithic-lichenicolous-epiphytic’ type. This assumption
is strongly supported by absence of early overlapping trait
changes. Branching point 1 gave rise to at least 3 major traits
(branching points 2–4), which subsequently led to a strong
lineage diversification and occupation of vacant ecological
space leading to extant traits. During this process, most traits
underwent multiple trait shifts visualized by overlapping
branches, which is apparent for the epiphytic (branching
points 2, 3 and 6) and the opportunistic characters (branching points 6, 7). Particularly the opportunistic trait appears
to have sourced its extant trait from a strong random walk
of ancestral intermediate traits (strong branch/line overlap).
Traits ‘carton’, ‘domatia’ and ‘bryophytic’ have a non-random distribution. ‘Carton’ has diversified from early ancestral branching point (5), with almost no overlap to other
traits.
To assess trait transitions, we calculated conditional likelihood for each character state at each node of the phylogenetic tree, including the root and simulated ancestral states at
13
72
Fungal Diversity (2020) 103:47–85
7
Discrete character
Epibryon turfosorum CBS 126587
Bryophytic
Chaetothyriales sp MP 2014 T171
Epibryon interlamellare CBS 126286
Chaetothyriales sp CBS 129051
Chaetothyriales sp CBS 129049
Chaetothyriales sp CBS 128948
Chaetothyriales sp MP 2014 T9
Chaetothyriales sp CBS 129047
Chaetothyriales sp CBS 128935
Chaetothyriales sp CBS 129050
Chaetothyriales sp CBS 128956
Chaetothyriales sp CBS 128959
Chaetothyriales sp CBS 129044
Chaetothyriales sp MP 2014 T210
Chaetothyriales sp CBS 128958
Chaetothyriales sp CBS 129046
Chaetothyriales sp CBS 128943
Phialophora attae CBS 132767
Chaetothyriales sp MP 2014 T13
Chaetothyriales sp MP 2014 T367
Chaetothyriales sp MP 2014 T333
Chaetothyriales sp MP 2014 T261
6
Chaetothyriales sp MP 2014 T179
Chaetothyriales sp CBS 128945
Phialophora capiguarae CBS 131954
Chaetothyriales sp MP 2014 T22
Carton
Cladophialophora australiensis CBS 112793
Cladophialophora lanosa KNU 16032 T
Cladophialophora potulentorum CBS 114772
Cladophialophora subtilis CBS 122642 T
Minimelanolocus aquaticus MFLUCC 15 0414 T
Rhinocladiella phaeophora CBS 496 78 T
Capronia nigerrima CBS 513 69
Capronia dactylotricha CBS 604 96 T
Exophiala sideris D88
Exophiala lacus FMR 3995
Capronia pilosella AFTOLID 657
Veronaea constricta CBS 572 90
Cladophialophora psammophila CBS 110553 T
Minimelanolocus thailandensis MFLUCC 15 0971
Capronia parasitica CBS 123 88
Cladophialophora parmeliae CBS 129337
Phialophora intermedia CBS 235 93
Exophiala alcalophila CBS 520 82 T
Ceramothyrium exiguum VTCCF 1209 T
Exophiala exophialae CBS 66876 T
Ceramothyrium aquaticum VTCCF 1210 T
Cyphellophora olivacea CBS 122 74 T
Exophiala nishimurae CBS 101538
Exophiala crusticola CBS 119970 T
Minimelanolocus obscurus MFLUCC 15 0416
Cyphellophora oxyspora CBS 698 73 T
Exophiala mesophila CBS 402 95
Minimelanolocus asiaticus MFLUCC 15 0237 T
Cyphellophora vermispora strain CBS 228 86 T
Capronia coronata ATCC 56201 T
Cyphellophora reptans CBS 113 85 T
Capronia fungicola CBS 614 96 T
Exophiala nidicola FMR 3889 T
Capronia kleinmondensis CBS 122671
Minimelanolocus melanicus MFLUCC 15 0415 T
Rhinocladiella anceps AFTOL ID 659
Exophiala nigra CBS 535 94 T
5
Epibryon hepaticola M10 T
Cladophialophora minutissima CBS 121758 T
Epibryon bryophilum CBS 126278
Minimelanolocus curvatus MFLUCC 15 0259 T
Unknown-Other ecology
Arthrocladium tropicale CBS 134926 T
Chaetothyriales sp CBS 129057
Chaetothyriales sp CBS 132003
Chaetothyriales sp CBS 134916
Chaetothyriales sp CBS 128973
Chaetothyriales sp CBS 132039
Chaetothyriales sp CBS 135086
Chaetothyriales sp CBS 128966
Chaetothyriales sp Trii4
Chaetothyriales sp CBS 128963
Chaetothyriales sp Cecr4
Chaetothyriales sp CBS 135085
Chaetothyriales sp CR13Ceci2
Chaetothyriales sp CBS 134920
4
Domatium
Cladophialophora matsushimae MFC1 P384 T
Cladophialophora devriesii CBS 147 84 T
Exophiala castellanii CBS 158 58 T
Exophiala angulospora CBS 482 92
Cyphellophora europaea CBS 101466 T
Rhinocladiella similis PW3041
Cladophialophora immunda CBS 834 96
Exophiala spinifera D22I
Rhinocladiella aquaspersa CBS 122635
Exophiala attenuata F10685
Cyphellophora fusarioides strain CBS 130291 T
Cladophialophora modesta CBS 985 96
Exophiala oligosperma CBS 127587
Cladophialophora samoensis CBS 259 83 T
Fonsecaea multimorphosa CBS 980 96 T
Arthrocladium fulminans CBS 136243 T
Fonsecaea brasiliensis BMU 07620
Veronaea botryosa CBS 254 57 T
Cladophialophora minourae CBS 556 83 T
Fonsecaea pedrosoi CBS 271 37 T
Phaeoannellomyces elegans CBS 101597
Cladophialophora pucciniophila KUS F23645
Cyphellophora laciniata CBS 190 61 T
Rhinocladiella mackenziei CBS 368 92
Exophiala psychrophila CBS 191 87
Exophiala salmonis CBS 157 67 T
Exophiala jeanselmei CBS 507 90 T
Exophiala equina CBS 116009 T
5
Exophiala cancerae CBS 115142
Phialophora americana CBS 400 67
Rhinocladiella basitona CBS 101460 T
Rhinocladiella tropicalis RA776
Exophiala dermatitidis CBS 207 35 T
3
phenotype
Chaetothyriales sp CBS 134923
Chaetothyriales sp MACrb1
Cyphellophora pauciseptata CBS 284 85 T
Bradymyces oncorhynchi CCF 4369 T
Cyphellophora suttonii CBS 449 91 T
Cladophialophora proteae CBS 111667 T
Exophiala hongkongensis HKU32 T
Fonsecaea pugnacius CBS 139214 T
Exophiala opportunistica CBS 122268
Cladophialophora mycetomatis CBS 122637 T
Exophiala pisciphila CBS 537 73 T
Exophiala bergeri CBS 353 52 T
Exophiala lecanii corni CBS 123 33 T
Cladophialophora arxii CBS 306 94 T
Cyphellophora pluriseptata CBS 286 85 T
Phialophora verrucosa CBS 286 47
Exophiala polymorpha CBS 138920 T
Cladophialophora emmonsii CBS640 96
Opportunistic
7
4
Knufia marmoricola CCFEE 6201
Chaetothyriales sp A957
Cladophialophora tumbae JCM 28746 T
Cladophialophora tumulicola JCM 28768
Chaetothyriales sp A933
Bradymyces graniticola F6A
Lichenodiplis lecanorae L
Chaetothyriales sp A872
Exophiala bonariae CCFEE 5792 T
Chaetothyriales sp L1994
Knufia perforans CBS 885 95 T
Chaetothyriales sp L1992
Knufia peltigerae CGMCC 3 17283
Rhinocladiella quercus CPC 26621 T
Aphanophora eugeniae CBS 124105 T
Bradymyces alpinus CCFEE 5493
Knufia vaticanii CCFEE 5939 T
Knufia karalitana CCFEE 5921
Chaetothyriales sp A581
Knufia petricola CBS 726 95 T
Knufia mediterranea CBS 139721 T
Chaetothyriales sp L1993
Anthracinomyces ramosus CGMCC 316367
Knufia epidermidis CBS 120353 T
6
1
3
2
Fig. 5 Quantitative trait simulation among the phylogeny
inferred via the R package
‘PHYTOOLS’. The plot depicts
phenotypic distribution over the
phylogeny and its associated
changes over time. While it is
similar the Brownian motion
phenogram, the quantitative trait
simulation does not depict the
stochastically mapped character
on to the phylogeny, and with
that the phenotypic changes
estimated for each branch,
neither the relative evolutionary
rate ratio (σ parameter) for each
phenotype. Instead, it visualizes trait changes, uniformity and discreteness of such
changes over time in a more
comprehensive way. Branching
points indicate approximated
major directions of phenotypic
changes at the root node to the
entire order Chaetothyriales.
X-axis depicts relative time
for the phenotype (ecology)
to evolve given the underlying
phylogeny. Y-axis depicts relative phenotypic categories
Epilithic-Lichenicolous
2
Capronia munkii CBS 615 96 T
Exophiala moniliae CBS 520 76 T
Cyphellophora livistonae CPC 19433 T
Cyphellophora musae GLZJXJ41 T
Cladophialophora yegresii CBS 114405 T
Cladophialophora boppii CBS 126 86 T
Cyphellophora jingdongensis IFRDCC 2659
Phaeosaccardinula ficus MFLUCC10 0009 T
Brycekendrickomyces acaciae CBS 124104
Capronia mansonii CBS 101 67 T
Cyphellophora eucalypti CBS 124764 T
Ceramothyrium thailandicum MFLUCC 100008 T
Ceramothyrium carniolicum CBS 175 95
Trichomerium deniqulatum MFLUCC10 0884 T
Trichomerium dioscoreae 138870 T
Nullicamyces eucalypti CPC 32942 T
Exophiala abietophila CBS 145038 T
Atrokylindriopsis setulosa HMAS245592
Paracladophialophora carceris CPC 27596 T
Ceramothyrium phuquocense VTCCF 1206 T
Capnodium coffeae CBS 147 52
Strelitziana eucalypti CBS 128214
Anthracinomyces petraeus CGMCC 317315
Cyphellophora phyllostachydis HLHNZWYZZ08 T
Capronia villosa ATCC 56206
Cladophialophora scillae CBS 116461
Vonarxia vagans CBS 123533 T
Cyphellophora filicis DP002B
Ceramothyrium menglunense MFLUCC 16 1874
Ceramothyrium podocarpi CPC 19826 T
Arthrocladium tardum CBS 127021 T
Trichomerium eucalypti CBS 143443 T
Metulocladosporiella musicola CBS 110960 T
Trichomerium gleosporum MFLUCC10 0087 T
Exophiala eucalypticola CBS 143412 T
Cladophialophora hostae CBS 121637
Cladophialophora humicola CBS 117536 T
Exophiala capensis CBS 128771 T
Phaeosaccardinula multiseptata IFRDCC 2639T
Knufia cryptophialidica DAOM 216555 T
Phaeosaccardinula dendrocalami IFRDCC 2649 T
Veronaea compacta CBS 268 75 T
Chaetothyrium agathis MFLUCC 12 0113 T
Exophiala eucalyptorum CBS 121638 T
Metulocladosporiella musae CBS 113863
Ceramothyrium longivolcaniforme MFLU 16 1306 T
Trichomerium foliicola MFLUCC10 0078 T
Paracladophialophora cyperacearum CPC 33046 T
Exophiala brunnea CBS 587 66 T
Ceramothyrium ficus MFLUCC 15 0228 T
Strelitziana cliviae CPC 19822 T
Exophiala italica MFLUCC 16 0245
Cyphellophora clematidis CBS 144983
Coccodinium bartschii CPC 13861
Arthrocladium caudatum CBS 457 67 T
Thysanorea papuana CBS 212 96 T
Capronia acutiseta CBS 618 96 T
Strelitziana albiziae CBS 126497 T
Uncispora sp YMF1 04133
Capronia camelliae yunnanensis CGMCC 3 19061 T
Fumagopsis stellae CBS 145078 T
Capnodium salicinum CBS 131 34
Exophiala encephalarti CBS 128210
Camptophora schimae IFRDCC 2664
Cyphellophora guyanensis CBS 129342 T
Exophiala lignicola CBS 144622 T
Cyphellophora sessilis CBS 243 85
Melanoctona tectonae MFLUCC 12 0389 T
Cladophialophora eucalypti CBS 145551
Capronia leucadendri CBS 122672 T
Exophiala heteromorpha CBS 232 33 T
Exophiala eucalypti CPC 27630
Cladophialophora abundans CBS 126736
Fonsecaea minima CBS 125757 T
Veronaea japonica CBS 776 83 T
Exophiala radicis P2854 T
Rhinocladiella atrovirens CBS 264 49 T
Thysanorea aquatica MFLUCC 15 0966
Rhinocladiella coryli CPC 26654 T
Camptophora hylomeconis CBS 113311 T
Knufia tsunedae FMR 10621
Rhinocladiella fasciculata CBS 132 86 T
Cyphellophora gamsii CPC 25867 T
Cyphellophora artocarpi CHCJHBJBLM T
Cladophialophora sylvestris CBS 350 83 T
Minimelanolocus rousselianus CBS 126086
Exophiala palmae UPCB 86822 T
Epiphytic
0.00
Fonsecaea erecta CBS 125763
Cladophialophora chaetospira CBS 114747
0.31
0.62
Neostrelitziana acaciigena CBS 139903 T
Ceramothyrium melastoma CPC 19837T
Exophiala placitae CBS 121716 T
Strelitziana australiensis CBS 124778 T
Chaetothyrium brischoficola MFLUCC 10 0083T
0.93
1.24
Time (relative)
Table 4 Brownian rate parameters σ estimated via the Brownian model, including the approximated standard error for each phenotype (ecology)
σ2 (Brownian rate)
Standard error
Epiphytic
Epilithic
Opportunistic
Domatium
Other
Carton
Bryophytic
8.9783
2.5921
0.0056
0
46.019
12.1818
0.0056
0
227.9022
40.3123
194.7455
30.1685
518.9015
262.1754
The higher the rate, the more likely a given phenotype is diversifying at present time. Lower rates indicate a slow down for ancestral, but an
increase (with higher rates) for derived phenotypes
each internal node by sampling from the posterior distribution of states (stochastical character mapping). The waiting
times between substitutions are drawn from an exponential
distribution with the rate being the diagonal elements of the
model’s instantaneous rate matrix (Q), conditioned on the
current state to infer a character transition matrix (Table 6).
This matrix served as input for the Brownian motion model
fitting to estimate evolutionary rate changes (Table 4), and
are visualized by mapped character changes along each individual branch (Fig. 6). The plotted Brownian motion process
(Fig. 6) indicated that three traits can be considered as ancestral: ‘epilithic’, ‘carton’, and, at a more derived position,
‘epiphytic’. Short sections of ‘opportunistic’ among initial
branches indicate that these traits, although later subject of a
13
diversification burst, had precursor traits at a very early stage
of evolution (as a result of the stochstically mapped characters). Conversely, the Brownian null model inferred the
ancestral state as being quantitatively in between ‘epilithic’
and ‘epiphytic’, with tendency towards ‘epilithic’ (recoded
discrete character ‘epiphytic’ = 1, ‘epilithic’ = 2, Brownian
null model ancestral state = 1.71). The more ancestral characters ‘epilithic’ and ‘epiphythic’, as well the highly derived
character ‘domatia’ have low evolutionary rates (Brownian
rates σ2); remaining traits, which are randomly distributed
over the taxa, experience a strong rate burst. Paucity of niche
shifts on internal branches decreases covariances among
tips relative to the neutral expectation and repress phylogenetic signals; conversely, an initially high rate of niche
Fungal Diversity (2020) 103:47–85
Chaetothyriales sp CBS 128948
0.15
Phenotype
Chaetothyriales sp CBS 128945
Rhinocladiella quercus CPC 26621 T
Chaetothyriales sp MACrb1
Chaetothyriales sp CBS 128935
Capronia villosa ATCC 56206
Exophiala nishimurae CBS 101538
Rhinocladiella tropicalis RA776
Cladophialophora tumbae JCM 28746 T
Exophiala hongkongensis HKU32 T
Chaetothyriales sp CBS 128966
Cladophialophora yegresii CBS 114405 T
Cladophialophora abundans CBS 126736
Exophiala capensis CBS 128771 T
Chaetothyriales sp Trii4
Exophiala nigra CBS 535 94 T
Cladophialophora mycetomatis CBS 122637 T
Chaetothyriales sp CBS 134916
Chaetothyriales sp CBS 129044
Cladophialophora tumulicola JCM 28768
Exophiala sideris D88
Chaetothyriales sp CBS 134920
Rhinocladiella aquaspersa CBS 122635
Exophiala palmae UPCB 86822 T
Cladophialophora boppii CBS 126 86 T
Chaetothyriales sp CBS 129051
Atrokylindriopsis setulosa HMAS245592
Cyphellophora phyllostachydis HLHNZWYZZ08 T
Cladophialophora minourae CBS 556 83 T
Phaeosaccardinula dendrocalami IFRDCC 2649 T
Chaetothyriales sp CBS 132039
Chaetothyriales sp L1992
Cyphellophora livistonae CPC 19433 T
Cladophialophora potulentorum CBS 114772
Phialophora americana CBS 400 67
Cyphellophora oxyspora CBS 698 73 T
Chaetothyriales sp CBS 135085
Chaetothyriales sp MP 2014 T171
Thysanorea aquatica MFLUCC 15 0966
Minimelanolocus obscurus MFLUCC 15 0416
Cladophialophora matsushimae MFC1 P384 T
Rhinocladiella phaeophora CBS 496 78 T
Exophiala eucalypticola CBS 143412 T
Paracladophialophora carceris CPC 27596 T
Exophiala dermatitidis CBS 207 35 T
Chaetothyriales sp CBS 129050
Phaeoannellomyces elegans CBS 101597
Thysanorea papuana CBS 212 96 T
Chaetothyriales sp MP 2014 T210
Exophiala heteromorpha CBS 232 33 T
0.10
Chaetothyriales sp MP 2014 T22
Capronia parasitica CBS 123 88
Cladophialophora modesta CBS 985 96
Veronaea compacta CBS 268 75 T
Fonsecaea pugnacius CBS 139214 T
Cyphellophora europaea CBS 101466 T
Chaetothyriales sp CR13Ceci2
Exophiala nidicola FMR 3889 T
Rhinocladiella anceps AFTOL ID 659
Chaetothyriales sp L1993
Cyphellophora gamsii CPC 25867 T
Cladophialophora subtilis CBS 122642 T
Cyphellophora jingdongensis IFRDCC 2659
Exophiala bergeri CBS 353 52 T
Cladophialophora australiensis CBS 112793
Chaetothyriales sp CBS 134923
Cladophialophora scillae CBS 116461
Capronia camelliae yunnanensis CGMCC 3 19061 T
Exophiala italica MFLUCC 16 0245
Exophiala moniliae CBS 520 76 T
Rhinocladiella fasciculata CBS 132 86 T
Capronia pilosella AFTOLID 657
Cladophialophora parmeliae CBS 129337
Strelitziana australiensis CBS 124778 T
Capronia mansonii CBS 101 67 T
Phialophora verrucosa CBS 286 47
Chaetothyriales sp CBS 128963
Chaetothyriales sp L1994
Chaetothyriales sp CBS 135086
Cladophialophora lanosa KNU 16032 T
Chaetothyriales sp CBS 132003
Fonsecaea minima CBS 125757 T
Phialophora capiguarae CBS 131954
Capronia munkii CBS 615 96 T
Fonsecaea multimorphosa CBS 980 96 T
Exophiala brunnea CBS 587 66 T
Strelitziana eucalypti CBS 128214
Chaetothyriales sp CBS 129057
Strelitziana albiziae CBS 126497 T
Cyphellophora pauciseptata CBS 284 85 T
Exophiala attenuata F10685
Strelitziana cliviae CPC 19822 T
Cladophialophora chaetospira CBS 114747
Exophiala lignicola CBS 144622 T
Exophiala
castellaniiCBS
CBS520
1588258TT
Exophiala
alcalophila
Cyphellophora
CBS 113 85 T
Cladophialophora
hostaereptans
CBS 121637
Cyphellophora pluriseptata CBS 286 85 T
Phialophora attae CBS 132767
Veronaea japonica CBS 776 83 T
Fonsecaea pedrosoi CBS 271 37 T
Cladophialophora arxii CBS 306 94 T
Aphanophora eugeniae CBS 124105 T
Lichenodiplis lecanorae L
Chaetothyriales sp MP 2014 T367
Cladophialophora samoensis CBS 259 83 T
Chaetothyriales sp Cecr4
Cyphellophora guyanensis CBS 129342 T
Cyphellophora
sessilis CBS 243 85
Cyphellophora eucalypti CBS 124764
T
Minimelanolocus rousselianus CBS 126086
Cyphellophora musae GLZJXJ41 T
Chaetothyriales sp CBS 128956
Epibryon turfosorum CBS 126587
Cyphellophora filicis DP002B
Cladophialophora psammophila CBS 110553 T
Melanoctona tectonae MFLUCC 12 0389 T
Chaetothyriales sp CBS 128973
Exophiala polymorpha CBS 138920 T
Exophiala psychrophila CBS 191 87
Fonsecaea brasiliensis BMU 07620
Exophiala lacus FMR 3995
Exophiala cancerae CBS 115142
Cyphellophora artocarpi CHCJHBJBLM T
Cladophialophora devriesii CBS 147 84 T
Exophiala opportunistica CBS 122268
Fonsecaea erecta CBS 125763
Epibryon interlamellare CBS 126286
Phialophora intermedia CBS 235 93
Veronaea constricta CBS 572 90
Chaetothyriales sp CBS 128959
Rhinocladiella coryli CPC 26654 T
Ceramothyrium melastoma CPC 19837T
Rhinocladiella basitona CBS 101460 T
Capronia dactylotricha CBS 604 96 T
Veronaea botryosa CBS 254 57 T
Capronia acutiseta CBS 618 96 T
Exophiala bonariae CCFEE 5792 T
Exophiala mesophila CBS 402 95
0.05
Minimelanolocus asiaticus MFLUCC 15 0237 T
Exophiala jeanselmei CBS 507 90 T
Cladophialophora immunda CBS 834 96
Capronia nigerrima CBS 513 69
Exophiala oligosperma CBS 127587
Phaeosaccardinula ficus MFLUCC10 0009 T
Cyphellophora olivacea CBS 122 74 T
Cyphellophora fusarioides strain CBS 130291 T
Exophiala eucalypti CPC 27630
Cladophialophora minutissima CBS 121758 T
Fumagopsis stellae CBS 145078 T
Exophiala eucalyptorum CBS 121638 T
Exophiala equina CBS 116009 T
Phaeosaccardinula multiseptata IFRDCC 2639T
Cyphellophora clematidis CBS 144983
Exophiala pisciphila CBS 537 73 T
Rhinocladiella atrovirens CBS 264 49 T
Cladophialophora emmonsii CBS640 96
Exophiala radicis P2854 T
Minimelanolocus aquaticus MFLUCC 15 0414 T
Minimelanolocus melanicus MFLUCC 15 0415 T
Cyphellophora laciniata CBS 190 61 T
Exophiala exophialae CBS 66876 T
Uncispora sp YMF1 04133
Exophiala spinifera D22I
Capronia kleinmondensis CBS 122671
Chaetothyriales sp A872
Chaetothyriales sp A581
Exophiala salmonis CBS 157 67 T
Chaetothyriales sp A957
Cladophialophora sylvestris CBS 350 83 T
Exophiala angulospora CBS 482 92
Minimelanolocus thailandensis MFLUCC 15 0971
Camptophora hylomeconis CBS 113311 T
Minimelanolocus curvatus MFLUCC 15 0259 T
Exophiala crusticola CBS 119970 T
Camptophora schimae IFRDCC 2664
Rhinocladiella similis PW3041
Arthrocladium fulminans CBS 136243 T
Bradymyces oncorhynchi CCF 4369 T
Capronia coronata ATCC 56201 T
Cyphellophora vermispora strain CBS 228 86 T
Rhinocladiella mackenziei CBS 368 92
Knufia cryptophialidica DAOM 216555 T
Exophiala lecanii corni CBS 123 33 T
Vonarxia vagans CBS 123533 T
Trichomerium gleosporum MFLUCC10 0087 T
Cladophialophora humicola CBS 117536 T
Arthrocladium tropicale CBS 134926 T
Exophiala abietophila CBS 145038 T
Chaetothyriales sp CBS 128943
Paracladophialophora cyperacearum CPC 33046 T
Capronia leucadendri CBS 122672 T
Bradymyces alpinus CCFEE 5493
Capronia fungicola CBS 614 96 T
Cyphellophora suttonii CBS 449 91 T
Bradymyces graniticola F6A
Arthrocladium tardum CBS 127021 T
Cladophialophora pucciniophila KUS F23645
Chaetothyrium brischoficola MFLUCC 10 0083T
Trichomerium foliicola MFLUCC10 0078 T
Cladophialophora eucalypti CBS 145551
Chaetothyriales sp MP 2014 T179
Ceramothyrium thailandicum MFLUCC 100008 T
Ceramothyrium menglunense MFLUCC 16 1874
Capnodium salicinum CBS 131 34
Epibryon hepaticola M10 T
0.00
Fig. 6 Brownian motion
phenogram inferred via the
R package ‘PHYTOOLS’.
Brownian rate parameter σ was
set to 0.1 to simulate trait evolution under Brownian motion.
X-axis depicts relative time
for the phenotype (ecology)
to evolve given the underlaying phylogeny. Y-axis depicts
relative phenotypic variation under the Brownian rate
parameter. Color coding for the
various ecologies derived from
stochastical character mapping: epiphytic (blue), epilithic/
lichenolytic (red), opportunistic
(brown), domatium (yellow),
other (orange), carton (green)
and bryophytic (pink). If lines
do not cross, vertically and or
horizontally the phenotype (=
character = ecology) does not
tend to be randomly distributed
(the situation towards the base,
ancestral state), while phenotypic changes towards the tips
of the phenogram underlay in
many cases (not all eg. ‘domatium’ or ‘bryophytic’) a strong
random distribution. Topological distribution is equivalent to
a late-burst model of phenotypic
evolution
73
Ceramothyrium carniolicum CBS 175 95
Cladophialophora proteae CBS 111667 T
Chaetothyriales sp CBS 128958
Chaetothyriales sp MP 2014 T13
Knufia mediterranea CBS 139721 T
Chaetothyriales sp CBS 129046
Epibryon bryophilum CBS 126278
Trichomerium deniqulatum MFLUCC10 0884 T
Chaetothyriales sp MP 2014 T9
Capnodium coffeae CBS 147 52
Trichomerium eucalypti CBS 143443 T
Chaetothyriales sp A933
Exophiala placitae CBS 121716 T
Brycekendrickomyces acaciae CBS 124104
Chaetothyriales sp CBS 129047
Coccodinium bartschii CPC 13861
Chaetothyriales sp MP 2014 T333
Arthrocladium caudatum CBS 457 67 T
Chaetothyrium agathis MFLUCC 12 0113 T
Chaetothyriales sp MP 2014 T261
Knufia vaticanii CCFEE 5939 T
Ceramothyrium ficus MFLUCC 15 0228 T
Knufia peltigerae CGMCC 3 17283
Exophiala encephalarti CBS 128210
Knufia marmoricola CCFEE 6201
Knufia perforans CBS 885 95 T
Nullicamyces eucalypti CPC 32942 T
Trichomerium dioscoreae 138870 T
Knufia petricola CBS 726 95 T
Metulocladosporiella musicola CBS 110960 T
Ceramothyrium podocarpi CPC 19826 T
Knufia karalitana CCFEE 5921
Ceramothyrium longivolcaniforme MFLU 16 1306 T
Knufia tsunedae FMR 10621
Anthracinomyces ramosus CGMCC 316367
Anthracinomyces petraeus CGMCC 317315
Metulocladosporiella musae CBS 113863
Ceramothyrium phuquocense VTCCF 1206 T
Knufia epidermidis CBS 120353 T
Chaetothyriales sp CBS 129049
Ceramothyrium exiguum VTCCF 1209 T
−0.05
Neostrelitziana acaciigena CBS 139903 T
Ceramothyrium aquaticum VTCCF 1210 T
0.00
0.31
Table 5 Statistical values obtained from calculations for the phylogenetic signal given the inferred phylogeny (Pagel’s λ and Blomberg’s
K)
Stastical value
p-Value
LogLikelihood
Pagel’s λ
Blomberg’s K
Pybus’s γ
0.726
NA
− 499.2
0.114
NA
NA
2.384
0.017
NA
Pybus’s γ statistic equates for speciation rates. The higher lambda and
K the higher the phylogenetic signal. If gamma is negative, it equates
for a slow down in speciation, if positive (in the case of our data) it
equates for increased speciation
differentiation which decreases towards the present, tends
to increase phylogenetic signal relative to the neutral expectation. Thus the most drastic niche shifts are concentrated
near the root of the tree during early evolutionary history.
The likelihood matrix for individual character transitions
0.62
0.93
1.24 Time (relative)
is given in Table 6, where higher values indicate a higher
likelihood that the character was derived from another entity.
The monophyletic character ‘domatia’ has a single character
origin likelihood shared by ‘opportunistic’ (Table 6). The
derived characters with high evolutionary rates (i.e. ‘domatia’ and ‘bryophytic’) expose a likelihood for a single character origin. Testing for the resolution of our dataset, assessment over the phylogenetic signal for the K and λ (lambda)
statistic was performed. While the K statistic indicates a low
phylogenetic signal for the global dataset, which is equivalent to a ‘tip-swap’ model, it is obvious from the Brownian
motion process (Fig. 6), that character evolution towards the
tips cannot be fully resolved given the current phylogeny
comprising solely ribosomal gene data, which indicate (e.g.
as for ‘opportunistic’ or ‘carton’) a strong random distribution (Brownian random walks) towards the tips. In contrast,
Pagels’ lambda indicates a higher phylogenetic signal, which
taken together as a result of the K statistic and the Brownian
13
74
Fungal Diversity (2020) 103:47–85
Table 6 Transition matrix; Character (trait=ecologies) transition matrix derived from stochastical character mapping
Epiphytic
Epilithic
Opportunistic
Domatium
Other
Carton
Bryophytic
Epiphytic
Epilithic
Opportunistic
Domatium
Other
Carton
Bryophytic
− 8.4913879
0.6391623
0.6391623
0.0000000
5.9463653
0.0000000
0.3100787
0.6391623
− 4.2168518
1.7859090
0.0000000
0.0000000
1.7917805
0.0000000
1.5957816
1.7859090
1.7859090
0.5035451
13.2359694
0.0000000
0.0000000
0.0000000
0.0000000
0.5035451
0.0000000
0.0000000
0.0000000
0.0000000
13.235969
0.0000000
13.235969
0.0000000
− 23.377706
4.195371
0.0000000
0.0000000
1.791780
0.0000000
0.0000000
4.195371
− 5.987151
0.0000000
− 0.3100787
0.0000000
0.0000000
0.0000000
0.0000000
0.0000000
− 0.3100787
2.5
2.0
1.5
1.0
0.5
0.0
disparity
Fig. 7 Disparity through time
(DTT) plot inferred via the R
package ‘GEIGER’. The plot
depicts morphological disparity
between phenotypes over time.
X-axis depicts relative time for
the lineages to disparate given
the underlaying phylogeny and
phenotypic data (ecologies).
Y-axis depicts relative disparity
between phenotypes (ecologies).
Remarkably, and in concordance with the Brownian motion
phenogram and the ‘LTT’ plot,
morphological disparity peaked
very early in Chaetothyrialian
evolution prior to most lineages
being born. This indicates that
major phenotypic innovations
occurred very early in Chaetothyrialian evolution, with a
significant slow down in novelty
and evolutionary rates (as of
the Brownian model) to mostly
the ancestral phenotypes and
increase towards more derived
phenotypes (e.g. ‘domatium’).
Multiple small phenotypic
disparate fluctuations (birth/
extinctions) equates to the rise
of the extant species
3.0
Higher values indicate higher likelihood that a character is derived from another entity (Read in rows to columns). For example, the character
state ‘domatium’ has a single value indicating that a key transition to this constrained lifestyle with highly specialized ants, was derived from the
‘opportunistic’ character (and associated intermediate character changes of ‘opportunistic’)
0.0
0.5
1.0
1.5
2.5
relative time
distribution, equates to a medium resolution quality of the
dataset (phylogenetic signal, discrete character evolution),
similar to Munkemueller et al. (2012) and Ackerly (2009),
supporting validity over the assumptions on trait transitions
above (Table 5).
13
Lineage diversification and disparity distribution over
time was demonstrated with a lineage through time plot
(LTT; Fig. 8). Given the late burst of lineage diversification
in Chaetothyriales, major phenotypic innovations occurred
very early in the evolution. Highest disparity coincides with
75
20
1
2
5
10
lineages
50
100
200
Fungal Diversity (2020) 103:47–85
0.0
0.2
0.4
0.6
0.8
time
Fig. 8 Lineage through time (LTT) plot inferred via the R package
‘PHYTOOLS’. The plot depicts lineage diversification (accumulation) over time. X-axis depicts relative time for the lineages to diversify given the underlying phylogeny. Y-axis depicts relative number
of lineages identified from the phylogeny. In concordance with the
Brownian motion phenogram, the ‘LTT’ plot equates for a late burst
model of diversification since a step increase (accumulation) in lineages accelerates only late in time. While establishing niche conservatism and occupation of niches took almost as much time for the early
Chaetothyrialian taxa to evolve relative to the total number of lineages, lineage diversification and speciation events for all extant taxa
in the present niches equates for less than one quarter of the total
time. The underlaying phylogeny, depicted as ultrametric tree where
evolutionary rates are set equal is shown as background graph in blue
earliest diversification events, and with novelty for vacant
niches (Fig. 7). After the late burst of diversification, beyond
the greatest disparity peak, niche conservatism limits further
character innovation; major trait innovation is subsequently
declining. However, significantly positive Pybus’s γ statistics (+2.384) indicates that cladogenesis increases over time
leading to pronounced and continuous species diversification
in existing niches (Table 5).
Discussion
The study of biodiversity
The scientific history of the order Chaetothyriales consists
of two parts, i.e. a phenotypic era using the sexual state
in its natural habitat, and a prevalently molecular phase
mostly applying asexual states in culture. The order attained
recognition particularly through the contributions of M.E.
Barr (1923‒2008) on Loculoascomycetes. Studies in that
time were performed by morphology of the sexual state on
the natural substrate, such as lichenized rock or decorticated
wood, of which dried voucher specimens were preserved
in herbaria. Only very few species were studied in culture.
Numerous older, previously described species became
assigned to the order (www.indexfungorum.org). Among
these were members of the group that had already been
recognized in the 19th century. As the early descriptions
have nomenclatural priority, comparison of type material
would be necessary to stabilize generic and specific names
in the order. However, much of this material is now lost or
is otherwise inaccessible, so that we are unsure about the
identity of reference material defining families, genera and
species. Even the identity of the species defining the order,
Chaetothyrium guaraniticum Spegazzini, described in 1888,
is uncertain, and hence an epitype will be designated below.
A similar line of research, after studies of Barr and others, has been on so-called ‘sooty moulds’, i.e. black fungi
colonizing plants, rock or other inert material without invasion, forming a moss-like black felt. Most of these studies
(Reynolds 1982; Reynolds 1983; Reynolds 1985; Chomnunti
et al. 2014) comprised members of Capnodiales as well as
Chaetothyriales. Only a fraction of these species, mainly
belonging to Chaetothyriaceae and Trichomeriaceae, have
cultures.
In the second half of the 20th century, an independent
line of research emerged that almost exclusively used living cultures. Schol-Schwarz (1968) systematically revised
phialophora-like organisms, and after studies of de Hoog
(1977) and Hermanides-Nijhof (1977) and the term ‘black
yeasts’ became adopted in the literature. Reference material
of these studies was deposited in culture collections, and
today sequence data are commonly available for almost all
species cultured after 1970. The great majority of novel taxa
initially belonged to a single family, Herpotrichiellaceae.
Later, diversity studies discovered a gamut of fungi that
phylogenetically clustered in other families of the Chaetothyriales. These studies take GenBank data as reference for
novelty of their isolates, neglecting older, nomenclaturally
valid but unsequenced taxa.
Müller et al. (1987) and Untereiner (1997) were the first
to make systematic connections between sexual and asexual
phases by either bringing ascospores to germinate, or by
stimulating asexual strains to produce ascomata, respectively. Today, the connection between the ascigerous state
in nature and the conidial state in culture can be verified
by sequence data. Remarkably, Haase et al. (1999), as confirmed in subsequent studies, noted that only very few of
the sexual strains brought into culture appeared to match
with any of the numerous available names of asexual
herpotrichiellaceous species. In our data, only possible
13
76
connections between Capronia coronata/Exophiala angulospora and Capronia semiimmersa/Phialophora americana
have been confirmed by sequencing. This suggests a preponderance of clonal reproduction as a survival strategy in
Herpotrichiellaceae.
The disruptive scientific history of Chaetothyriales
provides an unbalanced view on the order, due to current
accent on molecular data. As a result, most molecular studies
focus on Herpotrichiellaceae at the expense of other families
within the order. Generic circumscriptions before the year
2000 have been phenotypic, while simple forms of asexual
sporulation such as catenate cladophialophora-like conidia
are now known to occur widely throughout the order. For
example, members of Cladophialophora (Feng et al. 2013)
can be found scattered in four families, Herpotrichiellaceae,
Trichomeriaceae, Epibryaceae and Clade 4. Many morphological genera thus are obviously polyphyletic. Novel species
are introduced at a regular pace, phylogenetic trees suffering
from a significant taxon sampling problem, and therefore
redefinition of genera is recommended to be postponed until
a more complete overview of extant and still-to-be-described
species is obtained.
Origin and evolution of Chaetothyriales
Judging from results of divergence time estimations (Fig. 1),
the order Chaetothyriales emerged about 387 Mya, during
the end of Devonian (416–359 Mya), but the speciation
events occurred in the Jurassic (201–145 Mya), which was
initiated by the major Triassic-Jurassic extinction event, possibly as a result of rapid climate change due to volcanism or
methane production during the active split into continental
plates of the ancient Pangea continent (Ivanov 2007). During
the early period, animal and plant life on earth became very
scarce. Our hypothesis is that for a long time, the ancestral
Chaetothyriales colonized rock surfaces, and under these
extreme and oligotrophic conditions grew slowly without
much diversification.
A significant change in diversity in Chaetothyriales was
observed around 151 Mya. One possible hypothesis is that
the interaction of Chaetothyriales with toxin-containing
lichens and Cyanophytes on rock became a driver towards
toxin-management, which opened other windows of opportunity. As a result of the subsequent Cretaceous-Paleogene
extinction event (66 Mya), global species diversity greatly
declined again, resulting in many vacant ecological niches.
It took a long time for the ecosystem to restore general diversity (MacLeod et al. 1997; Wilf and Johnson 2004), but the
Chaetothyriales, which were not significantly impacted by
the extinction event, began an explosion of diversification.
Ancestral groups of Chaetothyriales had an epilithic,
lichen-associated strategy (Muggia et al. 2020). This is in
line with earlier assumptions, where black lichenized fungi
13
Fungal Diversity (2020) 103:47–85
of Verrucariales were listed in ancestral position to Chaetothyriales (Gueidan et al. 2008, 2011). Several clades with
identical non-lichenized, endolichenic lifestyles (Clades 8,
5 and 9) emerged, including the basal clade, oldest clade
(Clade 9). We speculate that the oldest Chaetothyriales coevolved with lichens that live on the surface of rocks. Metabolic products are accumulated in the lichen thallus during
the growth, known as lichenic acid or lichen substances
(Barnes 2000). Usnic acid, a dibenzofuran derivative, is
one of the most common and abundant lichen metabolites
(Cochietto et al. 2002). The Cyanobacteria that occur in
the lichens as photosynthetic accessory contain other toxins, such as microcystins (Oksanen et al. 2004) which are
larger molecules containing benzene rings. Early fungi living under these conditions must have the ability to tolerate
or to degrade these chemicals.
Cytochrome p450 genes (CYPs) play a fundamental role
in primary, secondary, and xenobiotic metabolism (van den
Brink et al. 1998). Some black yeasts are among the Ascomycota species with the highest number of CYPs (Teixeira
et al. 2017). Also genes related to alcohol dehydrogenase
(ADH), aldehyde dehydrogenase (ALDHs) and drug efflux
pumps were copied in large quantity, which helps the black
fungus adapt to the toxic environment better. The gene replications may have become the basis of metabolic versatility
observed in modern black yeast. These genetic adaptations
acquired in the common ancestor of the studied species are
maintained throughout the evolution of Chaetothyriales.
The apparent rapid explosion of diversification in the order,
underlined by the low rate of extinction and giving rise to
all within a very short time frame (Fig. 8) certainly has contributed to opening of numerous windows of opportunity for
members of the order.
Chaetothyrialean main families
Herpotrichiellaceae is the largest family within the order,
containing 19 recognized genera and 179 species (as per
01-10-2019); 117 species were analyzed in this study.
Excluded species were those without known ITS or LSU
sequences, or with obviously incorrect sequences as concluded from large distances to any of the taxa in the chaetothyrialean tree. In all trees, species published as being members of the family Herpotrichiellaceae showed instability
and low bootstrap values with different algorithms. In the
single-gene LSU or ITS trees, the family was not supported
but deteriorated into many subclades. With LSU + ITS, they
clustered together but the bootstrap values remained relatively low.
In search of common ecological features for Herpotrichiellaceae, Gostinčar et al. (2018) referred to these
fungi as being polyextremotolerant, i.e. combining tolerance
of e.g. temperature, dryness, toxin, and nutrient limitation.
Fungal Diversity (2020) 103:47–85
77
Numerous, as yet undescribed members of the family are
epilithic, colonizing hard, sun-exposed rock (Ruibal et al.
2008). The medical counterpart of the meristematic ecotype
on exposed habitats is the muriform cell formed in tissue of
patients with chromoblastomycosis, but members of the family are known from a plethora of opportunistic diseases (de
Hoog et al. 2019). Species are notoriously difficult to isolate
from natural environments (Sudhadham et al. 2008; Vicente
et al. 2014), but are enriched in human-created habitats, such
as oil-contaminated soil (Prenafeta-Boldú et al. 2001), creosoted railway sleepers (Gümral et al. 2014), gasoline (Isola
et al. 2013), dishwashers (Raghupathi et al. 2018), bathing
facilities (Matos et al. 2002), or household sinks (Nishimura
et al. 1987). These environments suggest, in line with suggestions of Gostincar et al. (2018), oligotrophy in addition
to extremotolerance and toxin management. Infective ability
seems to be consistently present in the family, as waterborne
species without thermotolerance infect numerous coldblooded vertebrates instead of humans (de Hoog et al. 2011).
Quan et al. (2019) developed an isolation method based on
enrichment with hydrocarbons, underlining the significance
of toxicity in the biology of these fungi, while earlier authors
successfully implemented experimental inoculation of environmental samples into laboratory animals (Gezuele et al.
1972; Dixon et al. 1980), high incubation temperature and
low pH (Sudhadham et al. 2008), extraction with mineral oil
(Satow et al. 2008; Vicente et al. 2008), and cycloheximide
as suppressor of contaminants (Wang et al. 2018). Generally,
low competitive ability with co-occurring saprobes has been
hypothesized, as a result of which they prevalently occupy
(micro-)habitats that are hostile to microbial life and are
inaccessible for their competitors (Gueidan et al. 2008).
The Cyphellophoraceae were previously known as
the ‘europaea-clade’ within Herpotrichiellaceae (de Hoog
et al. 2011) and were raised to family level by Réblová et al.
(2013). As yet, insufficient data are available to recognize an
unambiguous ecological trend in the family. Several species
are known from individual reports from plants, but mostly
without clear information on the type of growth, whether
as an endophyte, a pathogen, or a colonizer. Cyphellophora
europaea is a common species causing mild infections on
human skin and nails (de Hoog et al. 2000). Lian and de
Hoog (2010) hypothesized a life style as an oligotrophic
colonizer of moist, warm environments, where it could accidentally be picked up by human hosts. This might also hold
true for other clinical Cyphellophora species.
The clade representing Trichomeriaceae contained 48
strains, in addition to some undescribed species isolated
151 Mya
Opportunis c Clades 1,2,6
46.019
Doma a Clade 4
0.0056
Pleos gmaceae?
Epilithic Clades 1,6,5,9 0.0056
Irradiaon
Oligotrophy
Thermotolerance
Lichen-associaon
Disparity
Cytochrome expansion
Diversity burst
Carton Clades 1,2,6
194.7455
Bryophy c Clade 8
518.9015
Epiphy c Clades 1,2,3,6,7,8
8.9783
Fig. 9 Diagrammatic representation of evolution of Chaetothyriales over geological times. Epilithic lifestyle is ancestral, possibly
emerging from groups with uncertain phylogenetic position such as
Pleostigmaceae. Ecological disparity increased at an early stage,
followed by diversification with several ecotypes shortly after each
other and at low levels of innovation as expressed by Brownian rates
(Table 4). The red lines indicate multiple origins
13
78
from ant nest carton and four species of the genus Strelitziana described from living plants. Strelitziana australiensis,
S. eucalypti, S. albiziae and S. cliviae were all named after
their host plants and have been classified in a separate family, Strelitzianaceae (Crous et al. 2015). In our study, these
species cluster in the Trichomeriaceae clade albeit at rather
long branches; this result is different from previous studies (Cheewangkoon et al. 2009; Crous et al. 2010) and is
possibly explained by our larger dataset. Morphologically,
the asexual states of the species resemble those of Cyphellophora, and their growth on decaying leaves are not suggestive for primary pathogenicity. Thus we have reason to
believe that no separate family status is necessary and the
genus Strelitziana might well be maintained in the family
Trichomeriaceae. Members of this family are ‘sooty moulds’
colonizing inert substrates such as leathery plants (Chomnunti et al. 2014), while Knufia and relatives contains rockcolonizing species (Isola et al. 2016).
Chaetothyriaceae is the type family of the order Chaetothyriales. Although the family is monophyletic, bootstrap
values were relatively low, and distances between taxa rather
large. This clearly demonstrates a taxon sampling error, as
explained above. The majority of species has been isolated
from plants, with small populations as colonizers without
significant invasion of living tissue. Their epiphytic life style
is not associated with significant disease (Crous et al. 2006;
Crous et al. 2007; Gueidan et al. 2014; Hongsanan et al.
2016b).
Clade 4 mainly consists of ant-domatia colonizing species. The pronounced ability to metabolize monoaromatic
hydrocarbons explained the overabundance of members of
Herpotrichiellaceae in human-dominated environments; in
nature, this may be an association with ants (Voglmayr et al.
2011, Nepel et al. 2014), as these insects communicate with
similar compounds. Their nest materials of cartons, tunnels
or domatia are antimicrobial. Schlick-Steiner et al. (2008)
was the first to find a relationship between ants and Chaetothyriales. Defossez et al. (2009) revealed a symbiotic tripartite of domatia-forming plant, ant and fungus. In our study,
the domatia fungi all belong to a single, novel clade. Mayer
and Voglmayr (2009), Voglmayr et al. (2011), Nepel et al.
(2014) and Vasse et al. (2017) revealed a stunning biodiversity, of which the carton-associated species were divided
over families Herpotrichiellaceae, Trichomeriaceae and
Cyphellophoraceae. Attili-Angelis et al. (2014) described
some species in Cyphellophoraceae from leaf-cutting ants
in Brazil. Probably only a fraction of these fungi is known,
because there are thousands of tropical ants which build specific tunnel structures which may carry ant-specific black
yeasts.
13
Fungal Diversity (2020) 103:47–85
Ancestral character state reconstruction
Phenotypic plasticity (i.e. the sum of morphotypes and
growth abilities) enables a fungus to respond differentially
to novel environmental conditions. Most organisms are able
to survive outside their original and preferred habitat. In
the theory of ecological fitting (Janzen 1985), this operational environment is known as the ‘sloppy fitness space’
(Agosta and Klemens 2008). Under conditions of survival
stress, adaptation of the organism is promoted, whereas in
absence thereof, or with populations occupying different
environments and connected by gene flow, and thus being
subjected to heterogeneous pressure, more likely leads to
evolutionary stasis.
Brownian motion is an effective model as the sum of a
large number of very small, random forces relative to the
given trait changes. The wide species richness, the diverse
and fairly consistent ecotypes and the size of our dataset
provides an opportunity for modelling evolutionary transitions in comparison with the evolutionary timing of Chaetothyriales since its origin (Fig. 1). To this aim, ecological
traits are plotted along phenogram branches via stochastic
character mapping, revealing which traits in a population
follow a uniform pattern, and which may have evolved as
products of other traits and or transitions. While ecological
disparity peaked very early in Chaetothyriales evolutionary
history, interestingly a general trend in biology (e.g. as for
animals and plants; Harmon et al. 2012; Hughes et al. 2013),
it logically leads to a strong decline in occupying new niches
given the combinations of ancestral phenotypes and associated genetic abilities. While a Brownian process by means of
evolutionary history is driven by two indicators of a clade’s
success, i.e. diversity as measured by the number of species,
and disparity which is an estimate of the lineage’s occupancy
of a defined ecological space (Minelli 2016; Foote 1997;
McGhee 1999; Wills 2001; Erwin 2007), these attributes
are not mutually exclusive. Success in disparity does not
necessarily go together with success in diversity.
Ancestral, epilithic Chaetothyriales, possibly preceded
by rock-colonizing groups such as Pleostigmaceae (Muggia et al. 2020) colonized harsh and extreme environments,
with low diversity, while significant disparity is observed
with the abrupt evolution of e.g. ‘domatia’ and ‘bryophytic’
ecotypes in highly derived lineages. After these innovations, disparity decreased, but with explosive diversification
in similar habitats. As a general rule many large organism
genera show high diversity with low disparity, while others
are highly diverse but also exhibit high disparity, the latter being an important attribute to the Chaetothyriales (=
early high disparity burst lead to large diversity). The largest
taxonomic genera are often characterized by key innovations
that often, but not necessarily, coincide with their diagnostic
Fungal Diversity (2020) 103:47–85
apomorphies. A key principle in the black fungi strongly
supported by our data (=ecologies).
How is the evolution of fungal clades with high diversity
and/or disparity be explained? It can be addressed from three
main perspectives: (1) evolvability, in terms of release from
previous constraints and of the presence of genetic or developmental conditions favoring multiple parallel occurrences
of a given evolutionary transition and its reversal (clearly
supported by the Brownian analysis); (2) phenotypic plasticity as a facilitator of speciation; and (3) modularity, heterochrony and a coupling between the complexity of the life
cycle and the evolution of diversity and disparity in a clade.
The possible role of saltational evolution in the origination
of high diversity and/or disparity (eg. when considering our
transition matrix results, indicating highly abrupt evolution
of eg. ‘domatia’ or ‘bryophytic’ ecologies) in Chaetothyriales needs to be further explored. While under the simplest
conditions (neutral genetic drift) there is no relationship
between evolutionary rate and phylogenetic signal however,
such a relationship can exist when evolution is not entirely
neutral. For other circumstances, such as functional constraint, fluctuating selection, niche conservatism, and evolutionary heterogeneity, the relationship between process, rate,
and phylogenetic signal is complex. While our data precisely
reflects this complex case, it is due to its completeness an
example for macroevolutionary modelling and stochastical
effect discovery in kingdom fungi.
Conclusions
Numerous fungi with rock-inhabiting life styles have been
described, but the Chaetothyriales are special by representatives with intimate relationships with lichens, which led to
expansion of cytochromes providing windows of opportunity for diversification. Colonization of toxic environments
is an alternative way to escape microbial competition. Toxic
hydrocarbons are found in nature e.g. in ant-dominated
habitats. In human-made environments, toxic hydrocarbons
are present as compounds of oil- and gasoline-pollution
and industrial exhaust of xenobiotic volatiles. Members of
Herpotrichiellaceae have been proposed as agents of bioremediation, for example in industrial biofilters, where they
survive the conditions of acidification and dryness much
better than the bacteria that are currently used in air clean-up
(Cox et al. 1993; Groenestijn and Kraakman 2005). The vertebrate nervous system also contains aromatic hydrocarbon
neurotransmitters, which might be used by black yeasts once
they are introduced into the human body. This would explain
opportunism of these fungi, in analogy of hypotheses put
forward in Cryptococcus (Esher et al. 2018). A summarizing
diagram of the possible lines of adaptation in Chaetothyriales leading to species-rich families is given in Fig. 9.
79
Acknowledgements We would like to thank China Scholarship Council for financial support for Y.Q. (Number 201708520100). Hein van
der Lee and Marlou Tehupeiory-Kooreman are acknowledged for technical assistance. Qing Tian is thanked for double checking the ordinal
level tree of the Chaetothyriales.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
References
Ackerly D (2009) Conservatism and diversification of plant functional
traits: evolutionary rates versus phylogenetic signal. Proc Natl
Aacad Sci USA 106(2):19699–19706
Akaike H (1974) A new look at the statistical model identification.
Selected papers of hirotugu akaike. Springer, New York, pp
215–222
Arzanlou M, Crous P (2006) Strelitziana africana. Fungal Planet 8:2
Arzanlou M, Groenewald J, Gams W, Braun U, Shin H-D, Crous PW
(2007) Phylogenetic and morphotaxonomic revision of Ramichloridium and allied genera. Stud Mycol 58:57–93
Attili-Angelis D, Duarte A, Pagnocca F, Nagamoto N, de Vries M,
Stielow JB, de Hoog GS (2014) Novel Phialophora species from
leaf-cutting ants (tribe Attini). Fung Div 65(1):65–75
Badali H, Gueidan C, Najafzadeh M, Bonifaz A, Gerrits van den Ende
AHG, de Hoog GS (2008) Biodiversity of the genus Cladophialophora. Stud Mycol 61:175–191
Badali H, Bonifaz A, Barrón-Tapia T, Vázquez-González D, EstradaAguilar L, Cavalcante Oliveira N, Sobral Filho J, Guarro J, Meis
J, De Hoog G (2010) Rhinocladiella aquaspersa, proven agent of
verrucous skin infection and a novel type of chromoblastomycosis. Med Mycol 48(5):696–703
Barnes J (2000) Pharmacognosy in the 21st century. Pharm J
264:701–703
Barr ME (1976) Perspectives in the Ascomycotina. Mem New York
Bot Gard 28:1–8
Barr ME (1979) A classification of Loculoascomycetes. Mycologia
71(5):935–957
Barr ME (1987a) New taxa and combinations in the Loculoascomycetes. Mycotaxon 29:501–505
Barr ME (1987b) Prodromus to class Loculoascomycetes. Barr,
Amherst
Barr ME (1991) Notes on and additions to North American members
of the Herpotrichiellaceae. Mycotaxon 41(2):419–436
Barr M, Makkai M (1987) On representations of Grothendieck toposes.
Can J Math 39(1):168–221
Batista AC (1956) Systematic revision of the genera Ellisiella Sacc.
and Ellisiellina Da Camara and the new genus Ellisiopsis. Anais
Soc Biol Pernambuco 14:16–25
Batista AC (1960) Lembopodia, Yamamotoa e Peresiopsis, novos
gêneros de Asterinaceae. Publ Inst Micol Univ Recife 291:1–35
Batista AC, Ciferri R (1962) The chaetothyriales. Beih. Sydowia
3:1–129
13
80
Berlese AN (1896) Icones Fungorum (Abellini) 2(2–3):62
Berlese AN (1899) Icones Fungorum (Abellini) 2(4–2):177
Blomberg SPT, Garland JR, Ives AR (2003) Testing for phylogenetic
signal in comparative data: behavioral traits are more labile. Evolution 57:717–745
Campbell V, Legendre P, Lapointe F-J (2011) The performance of the
congruence among distance matrices (CADM) test in phylogenetic analysis. BMC Evol Biol 11(1):64
Cheewangkoon R, Groenewald J, Summerell B, Hyde K, To-Anun
C, Crous PW (2009) Myrtaceae, a cache of fungal biodiversity.
Persoonia 23:55–85
Chomnunti P, Schoch CL, Aguirre-Hudson B, Ko-Ko TW, Hongsanan S, Jones EG, Kodsueb R, Phookamsak R, Chukeatirote E,
Bahkali AH (2011) Capnodiaceae. Fungal Divers 51(1):103–134
Chomnunti P, Bhat D, Jones EG, Chukeatirote E, Bahkali AH, Hyde
KD (2012a) Trichomeriaceae, a new sooty mould family of
Chaetothyriales. Fung Div 56(1):63–76
Chomnunti P, Ko TWK, Chukeatirote E, Hyde KD, Cai L, Jones EG,
Kodsueb R, Hassan BA, Chen H (2012b) Phylogeny of Chaetothyriaceae in northern Thailand including three new species.
Mycologia 104(2):382–395
Chomnunti P, Bhat D, Jones EG, Chukeatirote E, Bahkali AH, Hyde
KD (2012c) Trichomeriaceae, a new sooty mould family of
Chaetothyriales. Fungal Divers 56(1):63–76
Chomnunti P, Hongsanan S, Aguirre-Hudson B, Tian Q et al (2014)
The sooty moulds. Fung Div 66(1):1–36
Cocchietto M, Skert N, Nimis P, Sava G (2002) A review on usnic
acid, an interesting natural compound. Naturwissenschaften
89(4):137–146
Constantinescu O, Holm K, Holm M (1989) Teleomorph-anamorph
connections in Ascomycetes. 1-3. Stanhughesia (Hyphomycetes) new genus, the anamorph of Ceramothyrium. Stud Mycol
31:69–84
Cox HHJ, Houtman JHM, Doddema HJ, Harder W (1993) Enrichment
of fungi and degradation of styrene in biofilters. Biotechnol Lett
15:737–742
Crous P, Groenewald J (2011) Why everlastings don’t last. Persoonia
26:70
Crous PW, Schroers H-J, Groenewald JZ, Braun U, Schubert K (2006)
Metulocladosporiella gen. nov. for the causal organism of Cladosporium speckle disease of banana. Mycol Res 110(3):264-275.
Crous PW, Schubert K, Braun U, de Hoog GS et al (2007) Opportunistic, human-pathogenic species in the Herpotrichiellaceae are
phenotypically similar to saprobic or phytopathogenic species
in the Venturiaceae. Stud Mycol 58:185–217
Crous PW, Braun U, Wingfield MJ, Wood AS et al (2009) Phylogeny and taxonomy of obscure genera of microfungi. Persoonia
788(22):139–161
Crous PW, Barreto RW, Alfenas AC, Alfenas RF, Groenewald JZ
(2010) What is Johansonia? IMA Fungus 1(2):117–122
Crous PW, Shivas R, Wingfield MJ, Summerell BA, Rossman AY,
Alves J, Adams G, Barreto R, Bell A, Coutinho M (2012) Fungal
Planet description sheets: 128–153. Persoonia 29:146
Crous PW, Wingfield MJ, Guarro J, Cheewangkoon R, Van der Bank
M, Swart W, Stchigel A, Cano-Lira J, Roux J, Madrid H (2013)
Fungal Planet description sheets: 154–213. Persoonia 31:188
Crous PW, Shivas R, Quaedvlieg W, Van der Bank M et al (2014) Fungal planet description sheets: 214–280. Persoonia 32:184
Crous PW, Wingfield MJ, Guarro J, Hernández-Restrepo M et al (2015)
Fungal planet description sheets: 320–370. Persoonia 34:167
Crous PW, Wingfield MJ, Burgess TI, Hardy GSJ et al (2016) Fungal
planet description sheets: 469–557. Persoonia 37:218
Crous PW, Wingfield MJ, Burgess TI, Carnegie AJ, Hardy GSJ, Smith
D, Summerell BA, Cano-Lira JF, Guarro J, Houbraken J (2017)
Fungal Planet description sheets: 625–715. Persoonia 39:270
13
Fungal Diversity (2020) 103:47–85
Crous PW, Luangsa-ard J, Wingfield M, Carnegie A et al (2018) Fungal
planet description sheets: 785–867. Persoonia 41:238
Crous PW, Schumacher RK, Akulov A, Thangavel R, HernándezRestrepo M, Carnegie A, Cheewangkoon R, Wingfield MJ, Summerell BA, Quaedvlieg W (2019) New and interesting fungi 2.
Fungal Syst Evol 3:57
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2:
more models, new heuristics and parallel computing. Nature
Meth 9(8):772
Das K, Lee S-Y, Jung H-Y (2019) Cladophialophora lanosa sp. nov.,
a New Species Isolated from Soil. Mycobiology 47(2):173–179
Davey ML, Currah RS (2007) A new species of Cladophialophora
(hyphomycetes) from boreal and montane bryophytes. Mycol
Res 111(1):106–116
de Azevedo CM, Gomes RR, Vicente VA, Santos DW, Marques SG, do
Nascimento MM, Andrade CE, Silva RR, Queiroz-Telles F, de
Hoog GS (2015) Fonsecaea pugnacius, a novel agent of disseminated chromoblastomycosis. J Clin Microbiol 53(8):2674–2685
Decock C, Delgado-Rodríguez G, Buchet S, Seng J (2003) A new
species and three new combinations in Cyphellophora, with a
note on the taxonomic affinities of the genus, and its relation to
Kumbhamaya and Pseudomicrodochium. Antonie van Leeuwenhoek 84(3):209
Defossez E, Selosse MA, Dubois MP, Mondolot L et al (2009)
Ant-plants and fungi: a new threeway symbiosis. New Phytol
182(4):942–949
de Hoog GS (1977) Rhinocladiella and allied genera. Stud Mycol
15:1–140
de Hoog GS, Mayser P, Haase G, Horré R, Horrevorts A (2000) A new
species, Phialophora europaea, causing superficial infections in
humans. Mycoses 43(11–12):409–416
De Hoog G, Vicente V, Caligiorne R, Kantarcioglu S, Tintelnot K, van
den Ende AG, Haase G (2003) Species diversity and polymorphism in the Exophiala spinifera clade containing opportunistic
black yeast-like fungi. J Clin Microbiol 41(10):4767–4778
De Hoog G, Nishikaku A, Fernandez-Zeppenfeldt G, Padín-González
C, Burger E, Badali H, Richard-Yegres N, van den Ende AG
(2007) Molecular analysis and pathogenicity of the Cladophialophora carrionii complex, with the description of a novel species.
Stud Mycol 58:219–234
de Hoog GS, Vicente VA, Najafzadeh M, Harrak M, Badali H, Seyedmousavi S (2011) Waterborne Exophiala species causing disease
in cold-blooded animals. Persoonia 27:46–72
de Hoog GS, Guarro J, Gené J, Ahmed SA, Al-Hatmi AMS et al (2019)
Atlas of clinical fungi. Web-edition, Utrecht
de Vries GA (1962) Cyphellophora laciniata nov. gen., nov. sp. and
Dactylium fusarioides Fragoso et Ciferri. Mycopath Mycol Appl
16(1):47–54
Diederich P, Ertz D, Lawrey JD, Sikaroodi M, Untereiner WA (2013)
Molecular data place the hyphomycetous lichenicolous genus
Sclerococcum close to Dactylospora (Eurotiomycetes) and S.
parmeliae in Cladophialophora (Chaetothyriales). Fungal Divers
58(1):61–72
Dixon DM, Shadomy H, Shadomy S (1980) Dematiaceous fungal
pathogens isolated from nature. Mycopathologia 70(3):153–161
Dobbeler P (1978) Moosbewohnende ascomyceten. I. Die pyrenocarpen, Den Gametophyten Besiedelnden Arten
Döbbeler P (1980) Epibryon endocarpum sp. nov. (Dothideales), ein
hepaticoler Ascomycet mit intrazellulären Fruchtkörpern. Z
Mykol 46:209–216
Döğen A, Ilkit M, De Hoog GS (2013) Black yeast habitat choices and
species spectrum on high altitude creosote-treated railway ties.
Fungal Biol 117(10):692–696
Dong W, Hyde KD, Bhat DJ, Zhang H (2018) Introducing Aculeata
aquatica gen. et sp. nov., Minimelanolocus thailandensis sp.
nov. and Thysanorea aquatica sp. nov. (Herpotrichiellaceae,
Fungal Diversity (2020) 103:47–85
Chaetothyriales) from freshwater in northern Thailand. Mycol
Progr 17(5):617–629
Erwin DH (2007) Disparity: morphologic pattern and developmental
context. Palaeontology 50:57–73
Esher SK, Zaragoza O, Alspaugh JA (2018) Cryptococcal pathogenic
mechanisms: a dangerous trip from the environment to the brain.
Mem Inst Oswaldo Cruz. 113(7):e180057
Feng P, Vicente VA, Najafzadeh MJ, Gerrits van den Ende AHG et al
(2013) Cladophialophora abundans, a novel environmental species in the Chaetothyriales. Mycol Prog 13(2):381–391
Feng P, Lu Q, Najafzadeh MJ, Gerrits van den Ende AHG et al (2014)
Cyphellophora and its relatives in Phialophora: Biodiversity and
possible role in human infection. Fung Div 65:17–45
Flakus A, Farkas E (2013) A contribution to the taxonomy of Lyromma
(Lyrommataceae, lichenized Ascomycota) with a species key.
Mycotaxon 124(1):127–141
Foote M (1997) The evolution of morphological diversity. Ann Rev
Ecol Syst 28:129–152
Friebes G (2012) A key to the non-lichenicolous species of the genus
Capronia (Herpotrichiellaceae). Ascomycete.org 4(3):55-64
Gao L, Ma Y, Zhao W, Wei Z, Gleason ML, Chen H, Hao L, Sun G,
Zhang R (2015) Three new species of Cyphellophora (Chaetothyriales) associated with sooty blotch and flyspeck. PLoS ONE
10(9):e0136857
Gezuele E, Mackinnon J, Conti-Diaz I (1972) The frequent isolation of
Phialophora verrucosa and Phialophora pedrosoi from natural
sources. Sabouraudia 10(3):266–273
Gjessing MC, Davey M, Kvellestad A, Vrålstad T (2011) Exophiala
angulospora causes systemic inflammation in Atlantic cod Gadus
morhua. Dis Aquat Org 96(3):209–219
Gomes RR, Vicente VA, Azevedo CMd, Salgado CG, da Silva MB,
Queiroz-Telles F, Marques SG, Santos DW, de Andrade TS,
Takagi EH (2016) Molecular epidemiology of agents of human
chromoblastomycosis in Brazil with the description of two novel
species. PLoS Negl Trop Dis 10(11):e0005102
Gostinčar C, Zajc J, Lenassi M, Plemenitaš A et al (2018) Fungi
between extremotolerance and opportunistic pathogenicity on
humans. Fung Div 93(1):195–213
Gostinčar C, Turk M, Zajc J, Gunde-Cimerman (2019) Fifty Aureobasidium pullulans genomes reveal a recombining polyextremotolerant generalist. Environ Microbiol 21(10):3638–3652
Groenestijn JW, Kraakman NJR (2005) Recent developments in biological waste gas purification in Europe. Chem Eng J 113:85–91
Gueidan C, Ruibal C, de Hoog GS, Gorbushina A, Untereiner W,
Lutzoni F (2008) A rock-inhabiting ancestor for mutualistic and
pathogen-rich fungal lineages. Stud Mycol 61:111–119
Gueidan C, Ruibal C, de Hoog GS, Schneider H (2011) Rock-inhabiting fungi originated during periods of dry climate in the late
Devonian and middle Triassic. Mycol Res 115:987–996
Gueidan C, Aptroot A, da Silva Cáceres ME, Badali H, Stenroos S
(2014) A reappraisal of orders and families within the subclass
Chaetothyriomycetidae (Eurotiomycetes, Ascomycota). Mycol
Prog 13(4):1027–1039
Gümral R, Tümgör A, Saraçlı MA, Yıldıran ŞT, Ilkit M, de Hoog
GS (2014) Black yeast diversity on creosoted railway sleepers changes with ambient climatic conditions. Microbial Ecol
68(4):699–707
Haase G, Sonntag L, Melzer-Krick B, de Hoog GS (1999) Phylogenetic
inference by SSU gene analysis of members of the Herpotrichiellaceae, with special reference to human pathogenic species. Stud
Mycol 43:80–97
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment
editor and analysis program for Windows 95/98/NT. Nucleic
Acids Symp Ser 41:95–98
Hansford CG (1946) The foliicolous ascomycetes, their parasites and
associated fungi. Mycol Pap 15:1–240
81
Harmon LJ, Schulte JA, Larson A, Losos JB (2012) Tempo and
mode of evolutionary radiation in inguanian lizards. Science
301:961–964
Hawksworth D, Dyko B (1979) Lichenodiplis and Vouauxiomyces: two
new genera of lichenicolous coelomycetes. The Lichenologist
11(1):51–61
Hennings PC (1905) Fungi Africae orientalis IV. Bot Jahrb Syst Pflges
Pflgeographie 38:102–118
Hermanides-Nijhof (1977) Aureobasidium and allied genera. Stud
Mycol 15:141–177
Hernández-Restrepo M, Schumacher RK, Wingfield MJ, Ahmad I,
Cai L, Duong TA, Edwards J, Gene J, Groenewald JZ, Jabeen S
(2016) Fungal systematics and evolution: FUSE 2.
Herrera-Campos M, Huhndorf S, Lücking R (2005) The foliicolous
lichen flora of Mexico IV: a new, foliicolous species of Pyrenothrix (Chaetothyriales: Pyrenothrichaceae). Mycologia
97(2):356–361
Hongsanan S, Hyde KD, Bahkali AH, Camporesi E, Chomnunti P,
Ekanayaka H, Gomes AA, Hofstetter V, Jones EG, Pinho DB
(2015a) Fungal biodiversity profiles 11–20. Cryptogam Mycol
36(3):355–380
Hongsanan S, Tian Q, Hyde K, Chomnunti P (2015b) Two new species of sooty moulds, Capnodium coffeicola and Conidiocarpus
plumeriae in Capnodiaceae
Hongsanan S, Tian Q, Hyde KD, Hu D (2016a) The asexual morph of
Trichomerium gloeosporum. Mycosphere 7(9):1473–1479
Hongsanan S, Sánchez-Ramírez S, Crous PW, Ariyawansa HA
et al (2016b) The evolution of fungal epiphytes. Mycosphere
7:1690–1712
Hubka V, Réblová M, Řehulka J, Selbmann L, Isola D, de Hoog SG,
Kolařík M (2014) Bradymyces gen. nov. (Chaetothyriales, Trichomeriaceae), a new ascomycete genus accommodating poorly
differentiated melanized fungi. Antonie van Leeuwenhoek
106(5):979–992
Hughes M, Gerber S, Wills MA (2013) Clades reach highest morphological disparity early in their evolution. Proc Natl Acad Sci USA
110(34):13875–13879
Hulsenbeck JP, Nielsen R, Bollback JP (2003) Stochastic mapping of
morphological characters. Syst Biol 52(2):131–158. https://doi.
org/10.1080/10635150390192780
Hyde KD, Jones EG, Liu J-K, Ariyawansa H et al (2013) Families of
dothideomycetes. Fung Div 63(1):1–313
Hyde KD, Norphanphoun C, Chen J, Dissanayake AJ et al (2018)
Thailand’s amazing diversity – up to 96% of fungi in northern
Thailand are novel. Fung Div 93:215–239
Isola D, Selbmann L, de Hoog GS, Fenice M et al (2013) Isolation
and screening of black fungi as degraders of volatile aromatic
hydrocarbons. Mycopathologia 175(5–6):369–379
Isola D, Zucconi L, Onofri S, Caneva G, de Hoog GS, Selbmann L
(2016) Extremotolerant rock inhabiting black fungi from Italian
monumental sites. Fung Div 76(1):75–96
Ivanov AV (2007) Evaluation of different models for the origin of the
Siberian traps. In: Foulger GR, Jurdy DM (eds) Plates, plumes
and planetary processes. Geol. Soc, Boulder
Iwatsu T, Udagawa S, Toyazaki N (1988) A new species of Phialophora. Mycotaxon 32:439–445
Kirk PM, Cannon PF, David J, Stalpers JA (2001) Ainsworth and
Bisby’s dictionary of the fungi, 9th edn. CABI Publishing,
Wallingford
Kiyuna T, An KD, Kigawa R, Sano C, Sugiyama J (2018) Two new
Cladophialophora species, C. tumbae sp. nov. and C. tumulicola sp. nov., and chaetothyrialean fungi from biodeteriorated
samples in the Takamatsuzuka and Kitora Tumuli. Mycoscience
59(1):75–84
13
82
Koukol O (2010) Revision of “Septonema ochraceum” revealed three
new species of Venturiaceae and Herpotrichiellaceae. Mycol
Prog 9(3):369–378
Kumar S, Stecher G, Peterson D, Tamura K (2012) MEGA-CC: computing core of molecular evolutionary genetics analysis program for automated and iterative data analysis. Bioinformatics
28(20):2685–2686
Legendre P, Lapointe FJ (2004) Assessing congruenceamong distance
matrices: single—malt scotch whiskies revisited. Austral N Z J
Statistics 46(4):615–629
Lian X, de Hoog GS (2010) Indoor wet cells harbour melanized agents
of cutaneous infection. Med Mycol 48(4):622–628
Liu JK, Hyde KD, Jones EG, Ariyawansa HAB et al (2015) Fungal
diversity notes 1–110: taxonomic and phylogenetic contributions
to fungal species. Fung Div 72(1):1–197
Liu J-K, Hyde KD, Jeewon R, Phillips AJL et al (2017) Ranking higher
taxa using divergence times: a case study in Dothideomycetes.
Fung Div 84:75–99
Li DM, de Hoog G, Saunte DL, Gerrits van den Ende AHG, Chen X
(2008) Coniosporium epidermidis sp. nov., a new species from
human skin. Stud Mycol 61:131–136
Li Y, Xiao J, De Hoog G, Wang X, Wan Z, Yu J, Liu W, Li R (2017)
Biodiversity and human-pathogenicity of Phialophora verrucosa
and relatives in Chaetothyriales. Persoonia 38:1
Li J, Jeewon R, Phookamsak R, Bhat DJ, Mapook A, Chukeatirote E,
Hyde KD, Lumyong S, Mckenzie EH (2018) Marinophialophora
garethjonesii gen. et sp. nov.: a new hyphomycete associated
with Halocyphina from marine habitats in Thailand. Phytotaxa
345(1):1–12
Ma Y-R, Xia J-W, Gao J-M, Li X-Y et al (2015) Atrokylindriopsis, a
new genus of hyphomycetes from Hainan, China, with relationship to Chaetothyriales. Mycol Prog 14(9):77
Maciá-Vicente JG, Glynou K, Piepenbring M (2016) A new species of
Exophiala associated with roots. Mycol Prog 15(2):18
MacLeod KG, Huber BT, Ward PD (1997). The biostratigraphy and
paleobiogeography of Maastrichtian inoce-ramids. In: Ryder G,
Fastovsky D, Gartner S (eds.) The cretaceous-tertiary event and
other catastrophes in earth history. Geol Soc America Spec Pap
307:361-373
Maddison W, Maddison D (2007) Mesquite: a modular system for evolutionary analysis. http://mesquiteproject.org.
Madrid H, Hernandez-Restrepo M, Gené J, Cano J, Guarro J, Silva V
(2016) New and interesting chaetothyrialean fungi from Spain.
Mycol Prog 15(10–11):1179–1201
Maharachchikumbura S, Haituk S, Pakdeeniti P, Al-Sadi A et al (2018)
Phaeosaccardinula coffeicola and Trichomerium chiangmaiensis, two new species of Chaetothyriales (Eurotiomycetes) from
Thailand. Mycosphere 9(4):769–778
Marincowitz S, Crous PW, Groenewald JZ, Wingfield MJ (2008)
Microfungi occurring on Proteaceae in the fynbos. CBS Biodivers Ser
Matos T, de Hoog GS, de Boer A, de Crom I, Haase G (2002) High
prevalence of the neurotrope Exophiala dermatitidis and
related oligotrophic black yeasts in sauna facilities. Mycoses
45(9–10):373–377
Mayer VE, Voglmayr H (2009) Mycelial carton galleries of Azteca
brevis (Formicidae) as a multi-species network. Proc R Soc B
276(1671):3265–3273
McGhee GR (1999) Theoretical morphology: the concept and its applications. Columbia University Press, New York
Minelli A (2016) Species diversity vs. morphological disparity in
the light of evolutionary developmental biology. Ann Bot
117:781–794
Moreno LF, Vicente VA, de Hoog GS (2018) Black yeasts in the
omics era: achievements and challenges. Med Mycol 56(Suppl
1):S32–S41
13
Fungal Diversity (2020) 103:47–85
Moussa TA, Al-Zahrani HS, Kadasa NM, Moreno LF et al (2017a)
Nomenclatural notes on Nadsoniella and the human opportunist
black yeast genus Exophiala. Mycoses 60(6):358–365
Moussa TA, Gerrits van den Ende BH, Al Zahrani HS, Kadasa
NM, de Hoog SG, Dolatabadi S (2017b) The genus Anthopsis and its phylogenetic position in Chaetothyriales. Mycoses
60(4):254–259
Moustafa A, Abdul-Wahid O (1990) Veronaea constricta, a new hyphomycete from Egyptian soils. Mycotaxon 38:167–171
Muggia L, Kopun T, Ertz D (2015) Phylogenetic placement of
the lichenicolous, anamorphic genus Lichenodiplis and
its connection to muellerella-like teleomorphs. Fung Biol
119(11):1115–1128
Muggia L, Fleischhacker A, Kopun T, Grube M (2016) Extremotolerant fungi from alpine rock lichens and their phylogenetic relationships. Fung Div 76(1):119–142
Muggia L, Kopun T, Grube M (2017) Effects of growth media on
the diversity of culturable fungi from lichens. Molecules 22:824
Muggia L, Quan Y, Gueidan C, Al-Hatmi AMS et al (2020) Ancestral
Chaetothyriales with two novel lineages of lichen-associated
fungi. Fung. Div, (in press)
Müller E, Petrini O, Fisher P, Samuels GJ, Rossman AY (1987) Taxonomy and anamorphs of the Herpotrichiellaceae with notes on
generic synonymy. Trans Br Mycol Soc 88(1):63–74
Munk A (1953) The System of the Pyrenomycetes: a contribution to
a natural classification of the group Sphaeriales sensu Lindau.
Munksgaard, Copenhagen
Munkemueller T, Lavergne S, Bzeznik B, Dray S et al (2012) How to
measure and test phylogenetic signal. Meth Ecol Evol 3:743–756
Nai C, Wong HY, Pannenbecker A, Broughton WJ, Benoit I, de Vries
RP, Gueidan C, Gorbushina AA (2013) Nutritional physiology of
a rock-inhabiting, model microcolonial fungus from an ancestral
lineage of the Chaetothyriales (Ascomycetes). Fungal Genet Biol
56:54–66
Nascimento MM, Selbmann L, Sharifynia S, Al-Hatmi AM, Voglmayr
H, Vicente VA, Deng S, Kargl A, Moussa TA, Al-Zahrani HS
(2016) Arthrocladium, an unexpected human opportunist in Trichomeriaceae (Chaetothyriales). Fungal Biol 120(2):207–218
Nascimento MM, Vicente VA, Bittencourt JV, Gelinski JML, Prenafeta-Boldú FX, Romero-Güiza M, Fornari G, Gomes RR,
Santos GD, Van Den Ende AG (2017) Diversity of opportunistic
black fungi on babassu coconut shells, a rich source of esters and
hydrocarbons. Fungal Biol 121(5):488–500
Nawawi A, Webster J (1982) Phalangispora constricta gen. et. sp.
nov., a sporodochial hyphomycete with branched conidia. Trans
Br Mycol Soc 79(1):65–68
Nepel M, Voglmayr H, Schönenberger J, Mayer VE (2014) High
diversity and low specificity of Chaetothyrialean fungi in carton galleries in a Neotropical ant-plant association. PLoS ONE
9(11):e112756
Nishimura K, Miyaji M, Taguchi H, Tanaka R (1987) Fungi in bathwater and sludge of bathroom drainpipes. Mycopathologia
97(1):17–23
O’Meara BC, Ane C, Sanderson MJ, Wainwright PC (2006) Testing
for different rates of continuous trait evolution using likelihood.
Evolution 60:922–933
Oksanen I, Jokela J, Fewer DP, Wahlsten M et al (2004) Discovery of
rare and highly toxic microcystins from lichen-associated cyanobacterium Nostoc sp. strain IO-102-I. Appl Environ Microbiol
70(10):5756–5763
Overy DP, Martin C, Muckle A, Lund L, Wood J, Hanna P (2015)
Cutaneous phaeohyphomycosis caused by Exophiala attenuata
in a domestic cat. Mycopathologia 180(3–4):281–287
Pagel M (1999) Inferring the historical patterns of biological evolution.
Nature 401:877–884
Fungal Diversity (2020) 103:47–85
Papendorf M (1969) New south african soil fungi. Transactions of the
British Mycological Society 52(3):483-IN420
Papendorf M (1976) Notes on Veronaea including V compactci sp. nov.
Bothalia 12(1):119–121
Paradis E, Schliep K (2019) APE 5.0: an environment for modern
phylogenetics and evolutionary analyses in R. Bioinformatics
35(3):526–528. https://doi.org/10.1093/bioinformatics/bty633
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20(2):289–290
Park M-J, Shin H-D (2011) Cladophialophora pucciniophila, a
new hyphomycete parasitizing a rust fungus. Mycotaxon
116(1):449–456
Pennell MW, Eastman JM, Slater GJ, Brown JW et al (2014) Geiger
v2.0: an expanded suite of methods for fitting macroevolutionary
models to phylogenetic trees. Bioinformatics 30(15):2216–2218.
https://doi.org/10.1093/bioinformatics/btu181
Petrak F (1914) Beiträge zur Pilzflora von Mähren und Österr.Schlesien. Annls Mycol 19(56):273–295
Phookamsak R, Hyde KD, Jeewon R, Bhat DJ, Jones EG, Maharachchikumbura SS, Raspe O, Karunarathna SC, Wanasinghe DN,
Hongsanan S (2019) Fungal diversity notes 929–1035: taxonomic and phylogenetic contributions on genera and species of
fungi. Fungal Divers 95(1):1–273
Pratibha J, Prabhugaonkar A (2015) New record of Thysanorea papuana from India. Mycosphere 6:480–485
Prenafeta-Boldú FX, Luykx D, Vervoort J, de Bont JA (2001) Fungi
growing on volatile aromatic hydrocarbons as sole carbon and
energy source. In: Proc 5th Int Symp Environm Biotechnol,
Kyoto, pp. 253-256
Puttemans A (1904) Contribution à l’étude de la fumagine des caféiers.
Bull Soc Mycol Fr 20:152–154
Pybus OG, Harvey PH (2000) Testing macro-evolutionary models
using incomplete molecular phylogenies. Proc R Soc Lond B
267:2267–2272
Quan Y, Gerrits van den Ende B, Shi D, Prenafeta-Boldú FX et al
(2019) A comparison of isolation methods for black fungi
degrading aromatic toxins. Mycopathologia 184(5):653–660
Raghupathi PK, Zupančič J, Brejnrod AD, Jacquiod S et al (2018)
Microbial diversity and putative opportunistic pathogens in
dishwasher biofilm communities. Appl Environ Microbiol
84(5):e02755-02717
Raj TN (1977) Ypsilonia, Acanthotheciella, and Kazulia gen nov. Can
J Bot 55(12):1599–1622
Rambaut A, Drummond A (2009) Tracer v1. 5.0. http://beast.bio.ed.ac.
uk/Tracer.
Réblová M, Untereiner WA, Réblová K (2013) Novel evolutionary lineages revealed in the Chaetothyriales (Fungi) based on multigene
phylogenetic analyses and comparison of ITS secondary structure. PLoS ONE 8(5):e63547
Réblová M, Hubka V, Thureborn O, Lundberg J, Sallstedt T, Wedin M,
Ivarsson M (2016) From the tunnels into the treetops: new lineages of black yeasts from biofilm in the Stockholm metro system
and their relatives among ant-associated fungi in the Chaetothyriales. PLoS ONE 11(10):e0163396
Revel LJ (2011) Phytools: an R package for phylogenetic comparative
biology (and other things). Methods Ecol Evol 3(2):217–223.
https://doi.org/10.1111/j.2041-210X.2011.00169.x
Reynolds D (1982) Foliicolous Ascomycetes. 4. The capnodiaceous
genus Trichomerium Spegazzini emend. [Fungi]. Mycotaxon
14:189–220
Reynolds D (1983) Foliicolous ascomycetes. 5. The capnodiaceous
clypeate genus Treubiomyces. Mycotaxon 17:349–360
Reynolds D (1985) Foliicolous ascomycetes. 6. The capnodiaceous
genus Limacinia. Mycotaxon 23:153–168
83
Ruibal C, Platas G, Bills G (2008) High diversity and morphological
convergence among melanised fungi from rock formations in the
Central Mountain System of Spain. Persoonia 21:93–100
Ruibal C, Selbmann L, Avci S, Martin-Sanchez P, Gorbushina A
(2018) Roof-inhabiting cousins of rock-hnhabiting fungi: novel
melanized microcolonial fungal species from photocatalytically
reactive subaerial surfaces. Life 8(3):30
Ruiz RFC, Heredia G, Reyes M, Arias R, Decock C (2001) A revision
of the genus Pseudospiropes and some new taxa. Cryptogam
Mycol 22(1):3–18
Saccardo PA (1883) Sylloge Fungorum (Abellini) 2:288
Samarakoon MC, Hyde KD, Hongsanan S, McKenzie EHC et al (2019)
Divergence time calibrations for ancient lineages of Ascomycota
classification based on a modern review of estimations. Fung
Div 96:285–346
Satow M, Attili-Angelis D, de Hoog G, Angelis D, Vicente V (2008)
Selective factors involved in oil flotation isolation of black yeasts
from the environment. Stud Mycol 61:157–163
Schlick-Steiner BC, Steiner FM, Konrad H, Seifert B et al (2008)
Specificity and transmission mosaic of ant nest-wall fungi. Proc
Nat Acad Sci USA 105(3):940–943
Schol-Schwarz MB (1968) Rhinocladiella, its synonym Fonsecaea
and its relation to Phialophora. Antonie van Leeuwenhoek
34(1):119–152
Seyedmousavi S, Badali H, Chlebicki A, Zhao J, Prenafeta-Boldu FX,
De Hoog GS (2011) Exophiala sideris, a novel black yeast isolated from environments polluted with toxic alkyl benzenes and
arsenic. Fungal Biol 115(10):1030–1037
Sinclair R (1979) Notes on Hyphomycetes. XXVI. Uncispora harroldii
gen. et sp. nov. Mycotaxon 8(1):140–143
Spegazzini G (1888) Fungi Guaranitici. Pug. II. An Soc Cient Argent
pp. 1-72
Spegazzini C (1910) Mycetes argentinenses, series V. An Mus Nac Hist
Nat B Aires 20:329–467
Stenroos S, Laukka T, Huhtinen S, Döbbeler P et al (2010a) Multiple
origins of symbioses between ascomycetes and bryophytes suggested by a five-gene phylogeny. Cladistics 26(3):281–300
Stenroos S, Laukka T, Huhtinen S, Döbbeler P, Myllys L, Syrjänen
K, Hyvönen J (2010b) Multiple origins of symbioses between
ascomycetes and bryophytes suggested by a five-gene phylogeny.
Cladistics 26(3):281–300
Stielow J, de Hoog G (2014) Novel Phialophora species from leafcutting ants (tribe Attini). Fungal Divers 65:6575Badali
Su L (2015) Taxonomy and ecology research of Chinese Stone Fungi.
China Agricultural University (In Chinese)
Sudhadham M, Prakitsin S, Sivichai S, Chaiyarat R et al (2008) The
neurotropic black yeast Exophiala dermatitidis has a possible
origin in the tropical rain forest. Stud Mycol 61:145–155
Sutton B, Gaur R (1984) Zelopelta thrinacospora gen. et. sp. nov. (Pycnothyriales). Trans Br Mycol Soc 82(3):556–559
Sutton DA, Rinaldi MG, Sanche SE (2009) Dematiaceous fungi.
Clinical mycology, 2nd edn. Churchill Livingstone, London, pp
329–354
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6:
molecular evolutionary genetics analysis version 6.0. Molec Biol
Evol 30(12):2725–2729
Teixeira M, Moreno LF, Stielow B, Muszewska A et al (2017) Exploring the genomic diversity of black yeasts and relatives (Chaetothyriales, Ascomycota). Stud Mycol 86:1–28
Tian Q, Doilom M, Luo ZL, Chomnunti P, Bhat JD, Xu J-C, Hyde
KD (2016) Introducing Melanoctona tectonae gen. et sp. nov.
and Minimelanolocus yunnanensis sp. nov. (Herpotrichiellaceae,
Chaetothyriales). Cryptogam Mycol 37(4):477–492
Tibpromma S, Hyde KD, Jeewon R, Maharachchikumbura SS, Liu
JK, Bhat DJ, Jones EG, McKenzie EH, Camporesi E, Bulgakov TS (2017) Fungal diversity notes 491–602: taxonomic
13
84
Fungal Diversity (2020) 103:47–85
and phylogenetic contributions to fungal taxa. Fungal Divers
83(1):1–261
Tsuneda A, Hambleton S, Currah R (2011) The anamorph genus Knufia and its phylogenetically allied species in Coniosporium, Sarcinomyces, and Phaeococcomyces. Botany 89(8):523–536
Tsurumi Y, Van Hop D, Ando K (2018) Three new anamorph of
Ceramothyrium from fallen leaves in Vietnam. Adv Microbiol.
8(04):314
Untereiner WA (1997) Taxonomy of selected members of the ascomycete genus Capronia with notes on anamorph-teleomorph connections. Mycologia 89(1):120–131
Untereiner WA, Naveau FA (1999) Molecular systematics of the Herpotrichiellaceae with an assessment of the phylogenetic positions
of Exophiala dermatitidis and Phialophora americana. Mycologia 91(1):67–83
van den Brink HM, van Gorcom RF, van den Hondel CA, Punt PJ
(1998) Cytochrome P450 enzyme systems in fungi. Fung Genet
Biol 23:1–17
Van den Ende A, De Hoog G (1999) Variability and molecular diagnostics of the neurotropic species Cladophialophora bantiana.
Stud Mycol 43:151–162
van der Aa HA, van Oorschot CAN (1985) A redescription of some
genera with staurospores. Persoonia 12(4):415–425
van der Aa HA, von Arx JA (1986) On Vonarxia, Kazulia and other
fungi with stauroconidia. Persoonia 13(1):127–128
Vasse M, Voglmayr H, Mayer V, Gueidan C et al (2017) A phylogenetic
perspective on the association between ants (Hymenoptera: Formicidae) and black yeasts (Ascomycota: Chaetothyriales). Proc
R Soc B 284(1850):20162519
Veerkamp J, Gams W (1983) Los hongos de colombia-VIII some new
species of soil fungi from Colombia. Caldasia:709-717
Vicente V, Attili-Angelis D, Pie M, Queiroz-Telles F et al (2008) Environmental isolation of black yeast-like fungi involved in human
infection. Stud Mycol 61:137–144
Vicente VA, Orélis-Ribeiro R, Najafzadeh M, Sun J, Guerra RS,
Miesch S, Ostrensky A, Meis JF, Klaassen CH, de Hoog G
(2012) Black yeast-like fungi associated with Lethargic Crab
Disease (LCD) in the mangrove-land crab, Ucides cordatus (Ocypodidae). Vet Microbiol 158(1–2):109–122
Vicente V, Najafzadeh M, Sun J, Gomes R, Robl D, Marques S,
Azevedo C, De Hoog G (2014) Environmental siblings of
black agents of human chromoblastomycosis. Fungal Divers
65(1):47–63
Voglmayr H, Mayer V, Maschwitz U, Moog J et al (2011) The diversity
of ant-associated black yeasts: insights into a newly discovered
world of symbiotic interactions. Fung Biol 115(10):1077–1091
Wang XF, Cai WY, Gerrits van den Ende AHG, Zhang J et al (2018)
Indoor wet cells as a habitat for melanized fungi, opportunistic
pathogens on humans and other vertebrates. Sci Rep 8:7685
Wiens JJ (2006) Missing data and the design of phylogenetic analyses.
J Biomed Inform 39(1):34–42
Wiens JJ (2008) Missing data and the accuracy of Bayesian phylogenetics. J Syst Evol 46(3):307–314
Wijayawardene NN, Hyde KD, Khalil Tawfeeq Al-Ani L, Tedersoo L,
et al. (2020) Outline of fungus and fungi-like taxa. Mycosphere
11 (2020)
Wilf P, Johnson KR (2004) Land plant extinction at the end of the
Cretaceous: a quantitative analysis of 1039 the North Dakota
megafloral record. Paleobiology 30(3):347–368
Wills MA (2001) Morphological disparity: a primer. In: Adrain JM,
Edgecombe GD, Lieberman BS (eds) Fossils, phylogeny, and
form. Kluwer/Plenum, New York, pp 55–144
Winka K, Eriksson OE, Bång Å (1998) Molecular evidence for recognizing the Chaetothyriales. Mycologia 90(5):822–830
Woo PC, Ngan AH, Tsang CC, Ling IW, Chan JF, Leung S-Y, Yuen
K-Y, Lau SK (2013) Clinical spectrum of Exophiala infections
and a novel Exophiala species, Exophiala hongkongensis. J Clin
Microbiol 51(1):260–267
Yang GZ, Lu J, Yu Z, Zhang K, Qiao M (2011) Uncispora sinensis, a
new species from China.
Yang H, Chomnunti P, Ariyawansa H, Wu H, Hyde KD (2014) The
genus Phaeosaccardinula (Chaetothyriales) from Yunnan, China,
introducing two new species. Chiang Mai J Sci 41:873–884
Yang H, Hyde KD, Karunarathna SC, Deng C, Gu CH, Yang SA,
Zhang ZC (2018) New species of Camptophora and Cyphellophora from China, and first report of sexual morphs for these
genera. Phytotaxa 343(2):149–159
Yong LK, Wiederhold NP, Sutton DA, Sandoval-Denis M, Lindner JR,
Fan H, Sanders C, Guarro J (2015) Morphological and molecular
characterization of Exophiala polymorpha sp nov isolated from
sporotrichoid lymphocutaneous lesions in a patient with myasthenia gravis. J Clin Microbiol 53(9):2816–2822
Zakharova K, Tesei D, Marzban G, Dijksterhuis J et al (2013) Microcolonial Fungi on rocks: a life in constant drought? Mycopathologia
175:537–547
Zeng J, Sutton D, Fothergill A, Rinaldi M, Harrak M, De Hoog G
(2007) Spectrum of clinically relevant Exophiala species in the
United States. J Clin Microbiol 45(11):3713–3720
Zeng XY, Wen TC, Chomnunti P, Liu JK, Boonmee S, Hyde KD
(2016) Ceramothyrium longivolcaniforme sp. nov., a new species of Chaetothyriaceae from northern Thailand. Phytotaxa
267(1):51–60
Affiliations
Yu Quan1,2,3 · Lucia Muggia4 · Leandro F. Moreno5 · Meizhu Wang1,2 · Abdullah M. S. Al‑Hatmi1,6,7
Nickolas da Silva Menezes14 · Dongmei Shi9 · Shuwen Deng10 · Sarah Ahmed1,6 · Kevin D. Hyde11 ·
Vania A. Vicente8,14 · Yingqian Kang2,13 · J. Benjamin Stielow1,12 · Sybren de Hoog1,6,8,10
1
2
Centre of Expertise in Mycology of Radboud University
Medical Centre/Canisius Wilhelmina Hospital, Nijmegen,
The Netherlands
Key Laboratory of Environmental Pollution Monitoring
and Disease Control, Ministry of Education of Guizhou &
Key Laboratory of Medical Microbiology and Parasitology,
13
·
School of Basic Medical Sciences, Guizhou Medical
University, Guiyang, China
3
College of Food and Pharmaceutical Engineering, Guizhou
Institute of Technology, Guiyang, China
4
Department of Life Sciences, University of Trieste, Trieste,
Italy
Fungal Diversity (2020) 103:47–85
5
Amsterdam Medical Center, Amsterdam, The Netherlands
6
Foundation Atlas of Clinical Fungi, Hilversum,
The Netherlands
7
Ministry of Health, Directorate General of Health Services,
Ibri, Oman
8
Postgraduate Program in Microbiology, Parasitology
and Pathology, Biological Sciences, Department of Basic
Pathology, Federal University of Parana, Curitiba, Brazil
9
Department of Dermatology & Laboratory of Medical
Mycology, Jining No. 1 People’s Hospital, Jining, Shandong,
China
85
10
Department of Medical Microbiology, People’s Hospital
of Suzhou National New & Hi-Tech Industrial Development
Zone, Suzhou, China
11
Center of Excellence in Fungal Diversity, Mae Fah Luang
University, Chiang Rai, Thailand
12
Thermo Fisher Diagnostics, Specialty Diagnostics Group,
Landsmeer, The Netherlands
13
Guizhou Academy of Tobacco Science, Guiyang, China
14
Engineering Bioprocess and Biotechnology Post-graduation
Program, Department of Bioprocess Engineering
and Biotechnology, Federal University of Parana, Curitiba,
Brazil
13
vania vicente