Mycologia, 98(6), 2006, pp. 1053–1064.
# 2006 by The Mycological Society of America, Lawrence, KS 66044-8897
Eurotiomycetes: Eurotiomycetidae and Chaetothyriomycetidae
David M. Geiser1
phylogenetically associated with this group. The
recently proposed order Mycocaliciales shows a sister
relationship with Eurotiomycetes. The great majority
of human pathogenic Pezizomycotina are Eurotiomycetes, particularly in Eurotiales, Onygenales and
Chaetothyriales. Due to their broad importance in
basic research, industry and public health, several
genome projects have focused on species in Onygenales and Eurotiales.
Key words: Cleistothecium, industrial fungi,
medically important fungi
Department of Plant Pathology, Pennsylvania State
University, University Park, Pennsylvania 16802
Cécile Gueidan
Jolanta Miadlikowska
François Lutzoni
Frank Kauff
Valérie Hofstetter
Emily Fraker
Department of Biology, Duke University, Durham,
North Carolina, 27708
Conrad L. Schoch
INTRODUCTION
Department of Botany and Plant Pathology, Oregon
State University, Corvallis, Oregon, 93133
Molecular data have been crucial in defining the class
Eurotiomycetes, which is now known to comprise
a morphologically and ecologically disparate set of
fungi. Early phylogenetic analyses of the Ascomycota
based on nuclear small ribosomal subunit sequences
revealed a common ancestry between Capronia
pilosella (Chaetothyriales), with bitunicate asci and
ascolocular development, and the fungi then recognized as the monophyletic Plectomycetes (Geiser and
LoBuglio 2001) and as Eurotiomycetes by Eriksson
(1999) (Berbee 1996, Spatafora et al 1995), which
generally produce prototunicate asci in enclosed
ascomata. This link led Berbee (1996) to propose
that the Eurotiomycetes evolved by loss of the
bitunicate ascus and its corresponding mode of
forcible discharge. The possibility of the cleistothecium evolving by means of paedomorphosis or
‘‘arrested development’’ was proposed by Eriksson
(1982). Later phylogenetic analyses further supported
a connection between the Chaetothyriales and the
prototunicate Eurotiomycetes (Liu et al 1999,
Lumbsch et al 2000, Silva-Hanlin and Hanlin 1999,
Winka et al 1998). Based on the distinctiveness of
Chaetothyriales, Chaetothyriomycetes (Eriksson and
Winka 1997) and Chaetothyriomycetidae (Kirk et al
2001) were proposed as supraordinal taxa.
Despite the generally low node support in some
previous studies of the Eurotiomycetes comprising
both Eurotiomycetidae and Chaetothyriomycetidae
(Liu and Hall 2004, Lutzoni et al 2001, Reeb et al
2004), the result appears to be supported by multiple
datasets involving multiple genes and taxon sets
(Lutzoni et al 2004). As shown in this volume,
weighted parsimony analysis of sequences from five
gene regions yielded 89% bootstrap support and
Bayesian analysis yielded 100% posterior probability
for the common ancestry of the subclasses (Spatafora
Leif Tibell
Department of Systematic Botany, Uppsala University,
Norbyvägen 18 D, Uppsala, Sweden
Wendy A. Untereiner
Department of Botany, Brandon University, Brandon,
Manitoba, Canada R7A 6A9
André Aptroot
ABL Herbarium, G. v.d. Veenstraat 107, NL-3762 XK
Soest, The Netherlands
Abstract: The class Eurotiomycetes (Ascomycota,
Pezizomycotina) is a monophyletic group comprising
two major clades of very different ascomycetous fungi:
(i) the subclass Eurotiomycetidae, a clade that
contains most of the fungi previously recognized as
Plectomycetes because of their mostly enclosed
ascomata and prototunicate asci; and (ii) the subclass
Chaetothyriomycetidae, a group of fungi that produce ascomata with an opening reminiscent of those
produced by Dothideomycetes or Sordariomycetes. In
this paper we use phylogenetic analyses based on data
available from the Assembling the Fungal Tree of Life
project (AFTOL), in addition to sequences in
GenBank, to outline this important group of fungi.
The Eurotiomycetidae include producers of toxic and
useful secondary metabolites, fermentation agents
used to make food products and enzymes, xerophiles
and psychrophiles, and the important genetics model
Aspergillus nidulans. The Chaetothyriomycetidae include the common black yeast fungi, some of which
are pathogens of humans and animals, as well as some
primarily lichenized groups newly found to be
Accepted for publication 29 November 2006.
1
Corresponding author. E-mail: dgeiser@psu.edu
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MYCOLOGIA
et al 2006). Furthermore this analysis placed Coryneliales in a basal position within a strongly supported
Eurotiomycetidae clade, indicating that members of
this clade evolved from fissitunicate/ascolocular
ancestors (Schoch et al 2006, Spatafora et al 2006).
Changing concepts of class Eurotiomycetes.—Nannfeldt
(1932) played a key role in integrating ontogenetic
features into ascomycete taxonomy, creating three
major groups based on ascomal development. One of
these groups, Plectascales, was defined based on the
production of naked asci and antheridia. In this
group enclosed cleistothecial ascomata form after
ascogenous hyphae are enveloped in sterile mycelia.
This group included all fungi with globose ascomata
and irregularly disposed evanescent asci.
Eurotiomycetidae is a monophyletic group encompassing a wide variety of morphologies, which
includes many traditionally defined plectomycete-like
fungi. Based on phylogenetic analyses of the nuclear
ribosomal small subunit RNA gene (SSU), Eriksson
(1999) proposed the class Eurotiomycetes for the
clade comprising most fungi known morphologically
as ‘‘Plectomycetes’’ and outlined as ‘‘the monophyletic Plectomycetes’’ by Geiser and LoBuglio
(2001). Although some concepts have included
perithecial taxa (Benny and Kimbrough 1980, Luttrell
1951) ‘‘Plectomycetes’’ generally refers to fungi with
these morphological characters: (i) thin-walled, globose to pyriform, prototunicate asci (i.e. asci with
walls that break down at maturity to release the
ascospores within the ascoma in a passive fashion,
rather than forcible discharge through an apical
pore); (ii) ascomata without a distinct hymenial layer
and with asci forming scattered within the ascomatal
cavity; (iii) unicellular ascospores; (iv) ascomata
varying from gymnothecial to cleistothecial, lacking
an ostiolar opening and with highly variable cleistothecial peridia, that may or may not be produced
within a stromatal structure; and (v) highly variable
phialoblastic and thallic hyphomycetous anamorphs
(Alexopoulos et al 1996, Geiser and LoBuglio 2001).
Both Eriksson (1999) and Geiser and LoBuglio
(2001) recognized similar fungi as making up this
clade. Eriksson organized them into two major
orders. Eurotiales contained families Elaphomycetaceae, Monascaceae and Trichocomaceae and
Onygenales comprised Arthrodermataceae, Ascosphaeraceae, Eremascaceae, Gymnoascaceae and
Onygenaceae. Based on SSU sequences Gibas et al
(2002) defined the new order Arachnomycetales to
accommodate fungi in the genus Arachnomyces. This
genus previously had been placed within Onygenales
based on morphology, but DNA characters grouped
it with Eurotiales. Previous analyses based on SSU
sequences showed Ascosphaera and Eremascus to form
a clade distinct from Onygenales (Berbee and Taylor
1992), leading Geiser and LoBuglio (2001) to infer
Ascosphaerales as a distinct order. (Lutzoni et al
2004) added further evidence in support of Ascosphaerales based on SSU and nuclear ribosomal large
subunit RNA gene (LSU) sequences, showing Ascosphaera apis, Eremascus albus and Paracoccidioides
brasiliensis to form a strongly supported clade.
Newly included orders.—The subclass Chaetothyriomycetidae first was proposed to accommodate the
order Chaetothyriales (Kirk et al 2001). The order
Verrucariales subsequently was shown to be sister to
Chaetothyriales (Lutzoni et al 2001) and was added to
this subclass (Eriksson 2001). Recent molecular
studies also placed the order Pyrenulales in this
group (reviewed in Lutzoni et al 2004). Members of
these three orders all are characterized by perithecial
ascomata and bitunicate asci with a dehiscence
ranging from fissitunicate to evanescent. Historically
classifications of ascomycetes treated either lichenized or nonlichenized taxa, but rarely both, because
they were recognized as two different groups (Acharius 1810, Lindau 1897, Zahlbruckner 1926). It was
only in the 20th century that these classifications were
merged (Luttrell 1951, 1955; Nannfeldt 1932), and
indeed the Chaetothyriomycetidae stands as the
prime example of the need for such a combined
system. The family Pyrenulaceae, together with
species from the Verrucariaceae, then were included in the order Xylariales based on their ascus
type and centrum, identified as Xylaria-type (Luttrell 1951, 1955). In the same classification the
family Herpotrichiellaceae was assigned to Pleosporales based on its centrum development (Luttrell
1951, 1955).
Eriksson’s (1982) system divided what is now
recognized as the Pezizomycotina into four groups
according to ascus type; the new orders Pyrenulales
and Verrucariales were placed in the bitunicate
group. The existing families Chaetothyriaceae and
Herpotrichiellaceae were included in the bitunicate
order Dothideales (Eriksson 1982). Barr was one of
the first authors to consider the three orders
Verrucariales, Chaetothyriales and Pyrenulales (at
that time included in the Melanommatales) as closely
related, based on ascus type (bitunicate or secondarily
prototunicate) and hamathecium structure (insertion
of sterile filaments in the centrum, either pseudoparaphyses or periphysoids) (Barr 1983). Molecular
studies confirmed the close phylogenetic relationships among these three orders as proposed by Barr
(Lutzoni et al 2004 and references therein). The
Verrucariales was added to the Chaetothyriomyceti-
GEISER ET AL: EUROTIOMYCETES
dae (Eriksson 2001), followed by the Pyrenulales
(Eriksson 2006).
Inclusion of Mycocalicales and Coryneliales.—Mycocaliciales was described to include nonlichenized
members of the families Mycocaliciaceae and Sphinctrinaceae (Tibell and Wedin 2000). These fungi are
parasites or commensals on lichenized or saprotrophic fungi and produce stalked or sessile apothecial ascomata, often referred to as mazaedia. Analysis
of nuclear ribosomal small subunit data showed
a weakly supported phylogenetic connection between
Mycocalicium and plectomycetous Eurotiomycetes
(Wedin et al 1998). A broader analysis of lichenized
fungi, including Mycocaliciales, recovered a moderately supported clade that placed Mycocaliciales basal
to a group that included Eurotiales, Lichinales (now
recognized at the class level), Chaetothyriales and
Verrucariales (Wedin et al 2005), leading to its
placement as an order of uncertain position within
Eurotiomycetes (Eriksson 2006).
Our aim in this paper is to combine ribosomal as
well as protein-coding DNA sequences obtained by
the AFTOL project and those available through
GenBank and the various genome projects to infer
a phylogeny for the class. The inferred phylogeny will
be used as the basis for a discussion of character
evolution in this diverse and important group of
fungi.
MATERIALS AND METHODS
Sampling and alignments.—Sequence data were obtained
from GenBank and the Assembling the Fungal Tree of Life
Project (AFTOL, http://www.aftol.org). All strains and
sequences used in this study are provided (SUPPLEMENTARY
TABLE I). DNA alignments were assembled with Clustal X
(Thompson et al 1997) and manually edited with the
shareware package BioEdit (v7.0; Tom Hall, Carlsbad,
California). Newly generated DNA sequences were deposited at GenBank (SUPPLEMENTARY TABLE I). Isolates
obtained from the culture collections were verified where
possible by comparison with DNA sequences obtained from
previous studies and deposited at GenBank. Herbaria and
culture collections where strains and specimens used in this
study are deposited are listed (SUPPLEMENTARY TABLE I).
Phylogenetic analysis.—Maximum and weighted parsimony
(MP and WP) analyses were performed in PAUP* v4.0b
(Swofford 2002) on a combined dataset with a total of 81
taxa that included 49 taxa classified as Eurotiomycetes and
representatives of all classes of Ascomycota except the
Laboulbeniomycetes, Lichinomycetes and Orbiliomycetes.
The sequence alignment was submitted in TreeBASE
(www.treebase.org) under accession No. SN2996. Thirteen
taxa used contained data only for the ribosomal loci but
were included to maximize taxon sampling. Comparative
analyses with only ribosomal data yielded congruent
1055
topologies (data not shown). We rooted the tree with four
taxa from the class Pezizomycetes as outgroups (Pyronema
domesticum, Caloscypha fulgens, Aleuria aurantia and
Gyromitra californica) (not shown in figure).
For WP analyses unambiguously aligned regions were
subjected to symmetric step matrices for 11 partitions (i.e.
nuc SSU rDNA, nuc LSU rDNA, and codon positions of
tef1, RPB1 and RPB2) to incorporate the differences in
substitution rates and patterns as described in Lutzoni et al
(2004). MP and WP analyses were performed with these
settings: 100 replicates of random sequence addition, TBR
branch swapping, and MULTREES in effect. Maximum likelihood was performed with RAxML-VI-HPC (Stamatakis et al
2005) using a GTRCAT model of evolution with 50 rate
categories. In all preceding cases nodal support was verified
by nonparametric bootstrapping under the conditions
mentioned, with 500 replicates.
Initial incongruence in the single gene trees for the taxa
used was tested by examining single gene analyses with WP
under the conditions previously mentioned for a set of taxa
containing data for all four loci (Lutzoni et al 2004). A 70%
majority rule consensus tree was compared in each case.
A Bayesian analysis was performed with a parallelized
version of MrBayes v3.1.2 across four processors (Huelsenbeck and Ronquist 2001, Ronquist and Huelsenbeck 2003).
MrBayes was run with these parameters: a general time
reversible (GTR) model of DNA substitution with gammadistributed rate variation across sites (invariance, partitioning across genes and codons). A Markov chain Monte Carlo
(MCMC) analysis with metropolis coupling was run starting
from a random tree for 10 3 106 generations, sampling
every 100th cycle. Four chains were run simultaneously with
the initial 10 000 cycles discarded as burn-in. Two additional
runs with 5 3 106 generations were compared to confirm
that stationarity in likelihood values was reached and
compared. The phylogenies obtained in all cases were
congruent. A 50% majority rule tree from a total of 90 000
trees obtained from a single run is presented (FIG. 1).
RESULTS AND DISCUSSION
An inferred Eurotiomycete phylogeny (FIG. 1) indicates that the class is monophyletic and contains two
strongly supported subclasses, Eurotiomycetidae and
Chaetothyriomycetidae. A discussion of the major
characters associated with the Eurotiomycetes and its
resident taxa follows with attention given to their
evolution.
Eurotiomycetidae.— Eurotiomycetidae (F IGS. 2–7)
comprises most of the taxa known previously as ‘‘the
monophyletic Plectomycetes’’ (Geiser and LoBuglio
2001) and ‘‘Eurotiomycetes’’ (Eriksson 1999), as well
as the Coryneliales, which possess more dothideomycete-like characters.
Coryneliales.—The missing link? Members of Coryneliales (Caliciopsis orientalis, Ca. pinea and Cornelia
uberata) form a strongly supported, basally positioned
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MYCOLOGIA
FIG. 1. Eurotiomycete phylogeny. Fifty percent Majority rule consensus tree of 90 000 trees obtained by Bayesian inference
under GTR+I+C applied across 11 partitions. MP BP5 maximum parsimony bootstrap, WP BP 5 weighted parsimony
bootstrap, ML BP 5 maximum likelihood bootstrap, PP 5 Bayesian posterior probability. Dashes are shown for nodes with ,
50% support and an asterisk indicates nodes that are differently resolved under the specific statistical sampling method used.
clade within the Eurotiomycetidae, consistent with
the results based on a comprehensive phylogenetic
analysis of five loci across the Pezizomycotina (Spatafora et al 2006). Coryneliales is associated with
fissitunicate asci and ascolocular ascomata (FIGS. 1–
2) and was considered an order of uncertain position
within the Pezizomycotina (Eriksson 2006). Neither
character is observed elsewhere in the Eurotiomycetidae, and their absence strongly indicates that they
were lost in concert as the unitunicate Eurotiomyce-
tidae evolved modes of passive spore discharge. The
results presented in this paper are consistent with
previous analyses showing that the SSU sequence of
Corynelia uberata indicated its relationship to the
Eurotiomycetes (Inderbitzin et al 2004, Winka 2000).
Caliciopsis and other taxa in the Coryneliales possess
morphological characters that bridge those found in
taxa in the Chaetothyriomycetidae with characters that
dominate elsewhere in the Eurotiomycetidae. Coryneliales tend to produce plectomycete-like, globose to
GEISER ET AL: EUROTIOMYCETES
pyriform asci that have been described mostly as
unitunicate or prototunicate, which have a thin wall
that deliquesces at maturity to release ascospores
within the ascoma (Barr and Huhndorf 2001).
Ascospores usually are single-celled and spherical,
and they are released through irregular openings in
the ascomata, which lack sterile hyphal elements.
In contrast to their clademates members of Coryneliales also show nonplectomycete-like characteristics:
Ascomatal development is ascolocular and asci possess
long tails that are retained from their ascohymenial
origins.
Luttrell (1951, 1955, 1973) consistently recognized
Coryneliales as a member of Pyrenomycetes, the
unitunicate perithecial fungi that mostly occupy
Sordariomycetes in the current system, and proposed
that it gained its ascostromatic characteristics through
a reduction of the perithecium. The asci of Coryneliales were considered unitunicate, and by definition
fungi with unitunicate asci could not be considered
Loculoascomycetes in Luttrell’s system, even if they
showed ascolocular centrum development. Luttrell
(1951) clearly saw Coryneliales as problematic in his
system of classification based on ascomal ontogeny,
and it was with some qualification that he placed
them in the Pyrenomycetes. However later studies of
the corynelialean ascus revealed that it was indeed
bitunicate, albeit in a distinctive way that appears to
be a transition state between the bitunicate asci
observed in the Chaetothyriomycetidae and the
prototunicate asci characteristic of the classical
Plectomycetes. Based on light microscopic studies,
Johnston and Minter (1989) described asci in the
Coryneliales as bitunicate with an outer wall that
breaks away to release a thin-walled, young ascus
(FIG. 3). However the two walls are present only in
the earliest stages of development, before the delimitation of ascospores, so that their bitunicate nature is
easily overlooked. In Corynelia uberata the outer wall
breaks near the ascus base long before the formation
of ascospores. The asci lengthen before and during
ascospore formation, yielding the distinctive longtailed asci harboring eight single-celled ascospores.
At maturity the inner ascus walls break open in an
irregular fashion, often on the side of the ascus,
releasing free ascospores into the ascomatal cavity. The
mature, unitunicate asci are thus essentially prototunicate, lacking an apical pore or fissure from which
ascospores are released. Johnston’s and Minter’s
(1989) observation of bitunicate asci in this group,
along with the seemingly ascolocular mode of ascomatal development, seemed to seal its placement among
the Loculoascomycetes. However these authors suggested that there were fundamental structural differences between the wall layers found in the Coryneliales
1057
and those found in other bitunicate ascomycetes and
cast doubts on their homology.
Most members of the Coryneliales are biotrophic
on woody hosts, especially on Podocarpaceae in the
southern hemisphere and some northern temperate
species that occur on conifers. The presence of
spermogonia and spermatia acting as male gametangia also distinguish Coryneliales from Onygenales and
Eurotiales, both of which produce hyphal gametangia
that are difficult or impossible to distinguish (Benjamin 1955). Only one genus in Coryneliales, Coryneliopsis, has a known anamorph that is placed in the
coelomycetous genus Anthracoderma.
Core Eurotiomycetidae.—Onygenales (including Ascosphaerales/Arachnomycetales) and Eurotiales. These orders form the core taxa referred to as ‘‘monophyletic
Plectomycetes’’ by Geiser and LoBuglio (2001) and
originally defined as Eurotiomycetes by Eriksson
(1999). They produce a variety of ascomata that may
include cleistothecia, some sort of ascostroma, and in
some cases neither. Asci are always produced in
a scattered fashion and do not form in a distinctive
fertile layer. Asci tend to be pyriform to globose and
evanescent, and bear eight, unordered ascospores.
Cleistothecial and stromatic ascomata characteristic of
this group are depicted (FIGS. 4–6).
Onygenales. A well-resolved Onygenales clade is
supported with two subclades: the strongly supported
Onygenales sensu stricto and a weakly supported clade
that comprises fungi previously classified as Onygenales, Ascosphaerales and Arachnomycetales (FIG. 1).
Members of Onygenales produce highly variable
ascomata, ranging from macroscopic ascostromata to
more reduced cleistothecial and gymnothecial forms
(Currah 1985). Cleistothecial peridia are highly variable, often composed of distinctively shaped hyphae.
Anamorphs in Onygenales are almost exclusively
thallic, involving the production of simple terminal
and intercalary arthroconidia as well as more elaborate
forms (FIG. 7). An ability to degrade keratin is found
frequently among members of this order, and this trait
correlates with the common status of such species as
pathogens of vertebrates. Onygenalean mammalian
pathogens include agents of histoplasmosis and
coccidioidomycosis, which cause respiratory infections
in mammals that occasionally disseminate to other
parts of the body. As the major group of dermatophytic fungi, they also cause superficial tinea infections.
Despite this association with mammalian disease,
onygenalean fungi are probably mostly saprophytic,
and they are frequently isolated from soils. Currah’s
(1985) monograph recognized four families within
Onygenales, Arthrodermataceae, Onygenaceae, Gymnoascaceae and Myxotrichaceae. A possible connec-
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MYCOLOGIA
FIGS. 2–12. Representative sexual and asexual structures of Eurotiomycetes. 2–3. Coryneliales: Corynelia uberata
(photographs courtesy Peter Johnston). 2. Ascostroma on Podocarpus leaf. 3. Ascus with basal remnants of broken outer
wall visible (arrow). Bar 5 10 mm. 4–6. Eurotiales. 4. Eupenicillium cleistothecia/ascostromata in culture. Bar 5 1 mm. 5.
Ruptured Eurotium cleistothecium, globose asci (upper left) and lenticular ascospore (lower right). Bars 5 10 mm. 6.
Noncleistothecial Trichocoma paradoxa ascostromata. Bar 5 10 mm. 7. Onygenales: Thallic Microsporum gypseum
macroconidial anamorph (photograph courtesy James A. Scott). Bar 5 10 mm. 8–9. Verrucariales. 8. Verrucaria aspiciliicola
thallus on rock. Bar 5 100 mm. 10–11. 9. Cross-section of Dermatocarpon miniatum perithecium, with asci and hamathecial
GEISER ET AL: EUROTIOMYCETES
tion between Myxotrichaceae and certain Leotiomycetes was noted, however based on ecology and
morphology, and the connection was confirmed later
based on nucleotide sequence analysis (Currah 1994,
Sugiyama et al 1999, Wang et al 2006). Detailed
microscopic studies of ascomal development in
Myxotrichum arcticum also revealed strong evidence
for a connection to the Leotiomycetes, specifically
a distinct hymenial layer, paraphyses, and stipitate asci
(Tsuneda and Currah 2004). These results strongly
support removal of Myxotrichaceae from the Onygenales.
Ascosphaerales/Arachnomycetales. Ascosphaerales, as
previously defined, comprise osmotolerant to osmophilic fungi with reduced ascomata and thallic
anamorphs. Early workers placed these fungi in
Hemiascomycetes because of their reduced hyphal
systems (Bessey 1950). In light of its reduced
gametangia, the genus Ascosphaera in Ascosphaeraceae
was proposed as a member of Plectascales (Spiltoir and
Olive 1955). Tightly aggregated asci and ascospores
take the form of spore balls, which are released from
a mature spore cyst. In mass the spore balls have
a chalky appearance, the basis of the term ‘‘chalkbrood’’ applied to the disease these fungi cause in
insects. Larvae infected with the fungus become filled
with spore balls, giving them a chalky appearance. The
genus Eremascus is morphologically distinct, and its
connection to Ascosphaera went unnoticed until the
advent of molecular phylogenetics (Berbee and Taylor
1992); the strongly supported relationship based on
SSU sequences led Geiser and LoBuglio (2001) to
recognize Ascosphaera and Eremascus together as
a distinct order. Eremascus produces a thin mycelium
and undifferentiated gametangia, with globose, eightspored asci that are typical of the plectomycetous
Eurotiomycetes. Eriksson et al (2004) recognized two
families for these fungi, Ascosphaeraceae and Eremascaceae, placed in Onygenales, but Lutzoni et al (2004)
found that Ascosphaera and Eremascus occurred in
a strongly supported clade that included Paracoccidioides brasiliensis, distinct from the major clade of
Onygenales. Paracoccidioides brasiliensis is a human
pathogenic fungus previously considered aligned with
Onygenales. This dimorphic fungus produces multiply
budding cells in its yeast phase, and an aleurioconidial
stage reminiscent of chrysosporium-like stages found
across Onygenales as defined broadly. Based on
a phylogenetic analysis of nuclear ribosomal small
1059
subunit data which showed it to be distinctive from
other members of Onygenales, the order Arachnomycetales was erected to accommodate the genus
Arachnomyces (Gibas et al 2002). However that analysis
did not include sequences from Ascosphaera, Eremascus and Paracoccidioides. Maximum parsimony analysis
of the dataset in our study yielded a weakly supported
clade that includes Arachnomyces, Ascosphaera, Eremascus, Paracoccidioides and Ajellomyces capsulata (results
not shown), opening up the possibility that the clades
inferred as Arachnomycetales by Gibas et al (2002)
and as Ascosphaerales by Lutzoni et al (2004)
represent the same group. However these data are
based mostly on SSU and LSU data alone, and neither
Bayesian (FIG. 1) nor ML analysis (results not shown)
support the inclusion of Arachnomyces in this clade, so
we will cautiously follow Eriksson (1999) and recognize
these fungi as members of Onygenales.
Eurotiales. Eurotiales, which receives consistently
strong support in our analysis, contains a diverse range
of ascomatal types similar to that found in Onygenales.
Asci are globose, and ascospores tend to be lenticular,
often with two equatorial rings. Ascomata include
highly reduced forms with hyphal peridia, cleistothecia, cleistothecia borne within a surrounding stroma,
and noncleistothecial stromata (Malloch 1981). Highly
reduced forms include Byssochlamys, which produces
asci in loosely organized hyphal structures, sometimes
referred to as protothecia. Cleistothecial forms comprise a variety of peridial types, ranging from hyphal
forms (often referred to as gymnothecia) found in
genera such as Talaromyces, to more rigid, pseudoparenchymatous forms found in genera such as Eurotium.
When a stroma is present, it may or may not surround
a cleistothecium. Stromatic/cleistothecial ascomata
are diverse. In Emericella cleistothecia have a distinct
peridium, with an outer layer of stromatic cells of
unknown function called Hülle cells (Malloch 1985).
Elaphomyces produces the largest ascomata in the
Eurotiomycetes, hypogeous, truffle-like fruiting bodies
measuring up to ˜3 cm across. Finally eurotialean
ascomata sometimes take a stromatic form that is not
enclosed and does not take the form of a cleistothecium. These include Trichocoma, which produces
a brush-like ascostroma in which ascogenous hyphae
and asci extend like bristles from a stromatic base, and
the more recently discovered genus Pseudotulostoma.
In this genus a tulostomoid (i.e. similar to a stalked
puffball) inner structure enclosing asci and ascospores
r
elements visible. Bar 5 100 mm. Chaetothyriales: Capronia pilosella. 10. Phialophora anamorph, featuring phialides with
distinctive collarettes. Bar 5 10 mm. 11. Fissitunicate asci with eight septate ascospores. Bar 5 10 mm. 12. Pyrenulales: Pyrenula
concatervans thallus on bark, with perithecial ascomata visible. Bar 5 5 mm.
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MYCOLOGIA
extends from an Elaphomyces-like ascostroma, leaving
behind a structure analogous to an agaricalean volva
(Miller et al 2001).
Eurotiales includes many well known and common
fungi, particularly those with phialidic Aspergillus and
Penicillium asexual stages. Most eurotialean fungi are
saprotrophic and represent some of the most
catabolically and anabolically diverse microorganisms
known. Some species are capable of growing at
extremely low water activities (i.e. xerotolerant and/
or osmotolerant), low temperatures (psychrotolerant)
and high temperatures (thermotolerant). These
properties, combined with the ability to produce
diverse sets of toxic secondary metabolites such as
aflatoxins, ochratoxins and patulins, make these fungi
important agents of food spoilage. Other secondary
metabolites produced by eurotialean fungi are useful
as pharmaceuticals, including antibiotics such as
penicillin and the anticholesterolemic agent lovastatin. The aggressively saprotrophic nature of some
species also makes them ideal industrial fungi because
they produce copious and diverse enzymes that
degrade a wide variety of complex biomolecules,
secrete them efficiently, and work well in fermentation systems. The broad importance of these fungi,
coupled with their ease of manipulation in the
laboratory, has led to a long standing interest in their
genetics, and more recently, to complete-genome
sequencing of several Aspergillus and Penicillium
species. Aspergillus nidulans, with its homothallic
Emericella sexual stage, has been used in classical
and molecular genetic studies for nearly 70 y.
Chaetothyriomycetidae.—This (FIGS. 8–12) is the second major clade of Eurotiomycetes. This subclass and
its three resident orders received consistently high
support across all analyses (FIG. 1).
Verrucariales. The order Verrucariales includes
mainly taxa living with autotrophic organisms to form
lichen symbioses. The majority of their photosynthetic
partners belong to the Chlorophyta, but heterokont
(phaeophyte, xanthophyte) and rhodophyte partners
also are known (Friedl and Büdel 1996, Kohlmeyer
and Volkmann-Kohlmeyer 1998). This large phylogenetic diversity of photosynthetic symbionts in the
Verrucariales differs from the largest group of lichens
(Lecanoromycetes), probably because of the exceptionally broad habitat preference across members of
this order, ranging from dry to aquatic conditions,
including freshwater and marine habitats. The two
partners of these symbioses usually share a mutualistic
relationship, but some of these fungi depart from this
‘‘reciprocal benefit’’ principle and act as parasites on
other lichens. Some of the parasites are still associated
with a photobiont, but they complement their nutrient
uptake by invading and parasitizing thalli of other
lichens (lichenicolous lichens, FIG. 8). Others have lost
their association with the photobiont and live as
commensals or parasites on other lichens (lichenicolous fungi). Therefore, although most of the Verrucariales are mutualists, living strategies in this order are
diverse, including commensalism and parasitism.
Verrucariales are cosmopolitan and include mostly
saxicolous species, which colonize rocks ranging from
small pebbles in rivers or glades to boulders and
entire cliffs but also manufactured substrates such as
concrete or stone walls (FIG. 8). They are particularly
diverse on calcareous substrates, where they grow
either as epiliths (over the surface of the rock) or
endoliths (within a superficial layer of the rock).
Although members of the Verrucariales are saxicolous, a significant number of taxa grow on other
substrates, such as soil, bark or wood, mosses or other
lichens. Verruclariales constitute the largest group of
maritime lichens and are present on rocky shores
worldwide.
Species of Verrucariales are diverse in thallus
morphology, including foliose-umbilicate, squamulose, crustose and granulose forms. Consistent with
their narrow range of thallus coloration, these fungi
lack the secondary metabolite diversity so characteristic of Lecanoromycetes. However some species of
Verrucariales are rich in a dark pigment probably
related to melanin, possibly an ancestral character
shared with Chaetothyriales. Similar to the situation
among members of Pyrenulales, vegetative propagules such as isidia or soredia are rare in the
Verrucariales, but asexual reproduction is still possible because squamulose and crustose-areolate thalli
are prone to fragmentation. Sexual reproductive
structures certainly play a major role in dispersal in
this group. Verrucariales is characterized by perithecial ascomata ranging from superficial to entirely
immersed in the thallus. The hamathecium is often
absent or when present formed by an evanescent
tissue of gelatinized pseudoparaphyses. The ostiole is
distinctively covered by periphyses (FIG. 9). Asci are
described as bitunicate with a mode of dehiscence
that is fissitunicate to evanescent (Eriksson 1982,
Janex-Favre 1971). Spores are highly variable, from
colorless to brown, and simple to muriform.
Chaetothyriales. This order includes nonlichenized
ascomycetes divided in two different families, the
Chaetothyriaceae and the Herpotrichiellaceae. The
members of Chaetothyriaceae are known as epiphytes
(Batista and Ciferri 1962) but it is still unclear whether
many of these species are saprophytic or biotrophic
(Barr 1987). Species of the Herpotrichiellaceae are
known either from their sexually reproducing state
(teleomorph), their clonally reproducing state (ana-
GEISER ET AL: EUROTIOMYCETES
morph) or both. Teleomorphs include small inconspicuous saprophytes, mainly growing on dead plants
and wood (Barr 1987; Untereiner and Naveau 1999)
whereas anamorphs also are found as animal and
human pathogens. These parasites, often called black
yeasts, can induce skin and nervous system infections
in healthy or immunocompromised patients (de Hoog
et al 2000 and references therein) and their addition
to the Eurotiomycetes places them with most other
animal pathogens in the Pezizomycotina. Most of these
species are known only by their anamorphs, and it is
only through recent molecular analyses that anamorph-teleomorph connections have been made
(Untereiner 2000 and references therein).
Sexual stages in Chaetothyriaceae are found mainly
in the tropics where they occur on the leaves and bark
of plants (Batista and Ciferri 1962). The sexually
reproducing Herpotrichiellaceae grow on dead plants
or wood, but their anamorphs are cosmopolitan and
can be isolated from a large variety of substrates
including bathwater, plants and soil (de Hoog et al
2000 and references therein). Their ubiquitous
presence in nature indicates that they are mainly
opportunistic pathogens, although the recent diversification of some species and their narrow range
of host specialization suggest that they can be systemic
pathogens (de Hoog et al 2000, Haase et al 1999).
Recent studies showed that some slow growing
melanized fungi inhabiting rocks in harsh environments belong to the Chaetothyriales (Ruibal 2004,
Sterflinger et al 1999).
The order Chaetothyriales is characterized by a dark
mycelium, growing as a loose net of hyphae (mycelial
pellicle) over the substrate in the Chaetothyriaceae
(Batista and Ciferri 1962), or as inconspicuous
immersed mycelium in the teleomorphs of Herpotrichiellaceae (Untereiner 2000). Anamorphic Chaetothyriales are characterized primarily by melanized
torulose hyphae, but they also can exhibit yeast-like,
meristematic and filamentous forms. Production of
asexual spores is also pleiomorphic in this order, with
annellidic (e.g. Exophiala), phialidic (e.g. Phialophora, FIG. 10), and blastic conidiogeneses (e.g.
Ramichloridium anceps) (de Hoog et al 2000). The
dark coloration of the mycelium is due to the
production of a melanin pigment, which was shown
to contribute to the resistance of these fungi to host
immune responses (Schnitzler et al 1999). However
the presence of melanin alone is not sufficient to
explain pathogenicity, and additional factors must be
involved to explain the virulence of these fungi (de
Hoog et al 2000). The perithecial ascomata of
Chaetothyriales are erumpent or superficial, sometimes setose, with or without a periphysate ostiole
(Kirk et al 2001). The excipulum pigmentation is
1061
variable, and the wall is thin and pseudoparenchymatous. The hamathecium consists of short apical
periphysoids. Asci are clavate, with a fissitunicate
mode of dehiscence and a thickening of the apical
region (FIG. 11). Spores are hyaline to pale gray and
transversally septate to muriform.
Pyrenulales. Pyrenulales includes mostly lichenized
taxa, the majority of them belonging to Anisomeridium
and Pyrenula, both with more than 100 accepted
species. These lichenized Pyrenulales are associated
with green algae belonging exclusively to the Trentepohliaceae, a family characterized by its orange
carotenoid pigments. This order also includes some
saprophytic nonlichenized taxa mostly found in the
family Requienellaceae (Aptroot 1991). Recent molecular studies showed that the family Trypetheliaceae did
not cluster with the family Pyrenulaceae but is nested
with the Dothideomycetes (Lutzoni et al 2004, del
Prado et al 2006).
The great majority of the lichenized Pyrenulales
colonize trees, where they occur exclusively on bark.
One notable exception on leaf surfaces, however, are
species of Strigula, associated with the orangepigmented green alga, Cephaleuros parasiticus; the
alga has been described mistakenly as a fungus on
numerous occasions (Holcomb and Henk 1994,
Reynolds and Dunn 1984). The nonlichenized taxa
are found on bark, leaves or wood. Some Pyrenulales
occur in temperate climates where they often are
confined to ancient woodlands, but this group is
predominantly tropical, where members are diverse as
epiphytes in rainforests. Although many recent
collecting efforts have been carried out in the tropics,
many regions are still understudied, and the species
diversity of this order is probably greatly underestimated (Aptroot 2001, Aptroot and Sipman 1997).
Lichenized Pyrenulales species are characterized by
a thin thallus, either immersed in the substrate or
superficial (FIG. 12). The structure of their thalli is
never as complex as in some other lichens, and they
never form foliose or fruticose thalli (Aptroot 1991).
Vegetative propagules such as soredia and isidia,
typically found in lichens from the Lecanoromycetes,
are absent. Similarly, secondary metabolites, so informative for species identification within the Lecanoromycetes, are rare in this order. Pyrenulales are
characterized by perithecial ascomata that are ostiolate, often papillate and sometimes aggregated. The
hamathecium generally consists of narrow trabeculate
pseudoparaphyses, subsequently replaced by unbranched paraphyses in the family Pyrenulaceae (Kirk
et al 2001). In the Requiellenaceae, the hamathecium
differs by having unbranched and sparsely septate
paraphyses (Boise, 1986). Asci are functionally bitunicate and they have ascohymenial origins (Janex-
1062
MYCOLOGIA
Favre 1971). Spores are colorless or brown and
transversally septate to muriform.
Mycocaliciales. Mycocaliciales showed a sister relationship with the Eurotiomycetidae + Chaetothyriomycetidae clade that was strongly supported by ML, BP
and Bayesian PP, but not by MP or WP (FIG. 1). This
relationship suggests possible inclusion of Mycocaliciales in Eurotiomycetes as a third subclass, but we
postpone including it because it is based only on SSU
and LSU data from Mycocaliciales. A number of
morphological characters, however, unite this order
with taxa in both Eurotiomycetidae and Chaetothyriomycetidae, which might reflect common ancestry.
The mazaedial ascomata in this group are reminiscent
of the stalked ascomata produced by Onygena (Onygenales) and Pseudotulostoma (Eurotiales), and asci in
some taxa within Sphinctrinaceae are evanescent,
providing a general connection to Eurotiomycetidae.
Their parasitic and/or commensal associations with
other fungi, particularly lichens, provide an ecological
connection with many taxa in Chaetothyriomycetidae.
The spotty distribution of these characters in Mycocaliciales and Eurotiomycetes does not necessarily
compel the hypothesis that they are ancestral but
perhaps indicates an evolutionary plasticity toward
them within these groups.
ACKNOWLEDGMENTS
We thank Meredith Blackwell and two anonymous reviewers
for their comments on the manuscript. Individuals who
provided cultures and other materials that contributed to the
AFTOL effort are gratefully acknowledged. This work would
not have been possible without the support of NSF grant
0090301, Research Coordination Network: A phylogeny for
kingdom Fungi to M. Blackwell, J.W. Spatafora and J.W.
Taylor, as well as NSF grant DEB-0228668, Assembling the
Fungal Tree of Life (AFTOL) to F. Lutzoni and R. Vilgalys,
and NSF CAREER award DEB-0133891 to F. Lutzoni.
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