12 Tremellomycetes and Related Groups

1 1 2 1 MICHAEL WEIß ,ROBERT BAUER ,JOSE´ PAULO SAMPAIO ,FRANZ OBERWINKLER

CONTENTS I. Introduction I. Introduction ...... 00 A. Historical Concepts...... 00 Tremellomycetes is a fungal group full of con- B. Modern View ...... 00 II. Morphology and Anatomy ...... 00 trasts. It includes jelly fungi with conspicuous A. Basidiocarps ...... 00 macroscopic basidiomes, such as some species B. Micromorphology ...... 00 of Tremella, as well as macroscopically invisible C. Ultrastructure...... 00 inhabitants of other fungal fruiting bodies and III. Life Cycles...... 00 a plethora of species known so far only as A. Dimorphism ...... 00 B. Deviance from Dimorphism ...... 00 asexual yeasts. Tremellomycetes may be benefi- IV. Ecology ...... 00 cial to humans, as exemplified by the produc- A. Mycoparasitism...... 00 tion of edible Tremella fruiting bodies whose B. Tremellomycetous Yeasts ...... 00 production increased in China alone from 100 C. Animal and Human Pathogens ...... 00 MT in 1998 to more than 250,000 MT in 2007 V. Biotechnological Applications ...... 00 VI. Phylogenetic Relationships ...... 00 (Chang and Wasser 2012), or extremely harm- VII. Taxonomy...... 00 ful, such as the systemic human pathogen Cryp- A. Taxonomy in Flow ...... 00 tococcus neoformans. The systematics and B. Taxonomic Synopsis...... 00 taxonomy of many species now contained in C. Key Groups ...... 00 Tremellomycetes have significantly changed 1. Cystofilobasidiales ...... 00 2. Filobasidiales ...... 00 during the past three decades and are about to 3. Holtermanniales...... 00 change again as a result of changes in the taxo- 4. Trichosporonales...... 00 nomic treatment of anamorph forms in the 5. Tremellales ...... 00 International Code of Nomenclature for algae, D. Possibly Related Taxa Incertae Sedis ... 00 fungi, and plants (McNeill et al. 2012). An 1. Bartheletia...... 00 2. Wallemia ...... 00 integrated systematic view of the Tremellomy- VIII. Conclusions ...... 00 cetes has been hampered by the fact that the References...... 00 anamorphic taxa, i.e., yeasts, and the basidiome-forming dimorphic taxa have tradi- tionally been studied by different scientific communities. Recently, the group has been dis- cussed in more integrative treatments (e.g., Boekhout et al. 2011; Millanes et al. 2011; Sam- Dedicated to the memory of Robert Joseph Bandoni paio 2004). (1926–2009) Since the last edition of The Mycota,key 1Fachbereich Biologie, Eberhard-Karls-Universita¨tTu¨bingen, Auf der Morgenstelle 1, 72076 Tu¨bingen, Germany; e-mail: systematic concepts in the Basidiomycota have [email protected];; changed conspicuously. While the tremello- 2Centro de Recursos Microbiolo´gicos, Departamento de Cieˆn- mycetous groups were then treated in a sepa- cias da Vida, Universidade Nova de Lisboa, 2829-516 Caparica, rate Heterobasidiomycetes chapter (Wells and Portugal

Systematics and Evolution, 2nd Edition The Mycota VII Part A D.J. McLaughlin and J.W. Spatafora (Eds.) © Springer-Verlag Berlin Heidelberg 2014 M. Weiß et al.

Bandoni 2001), Heterobasidiomycetes is no B. Modern View longer considered a monophyletic group (Weiß et al. 2004); for the present edition its This concept was challenged by Bandoni members are discussed in this chapter, in (1984), who redefined Tremellales and Auricu- Agaricomycetes (Tulasnella, Ceratobasidium lariales based on ultrastructural characters, the and relatives, Auriculariales, Sebacinales; see nature of the haploid states, and trophic strate- Hibbettetal.2014), and in Dacrymycetes (see gies, rather than on basidial morphology. This Oberwinkler 2014). alternative concept has been largely confirmed In this overview we provide an introduction by molecular data (e.g., Swann and Taylor 1995; to the taxonomy, morphology, ecology, and Weiß and Oberwinkler 2001) and is currently phylogenetic relationships of the Tremellomy- widely accepted (Hibbett et al. 2007). cetes, including a phylogenetic tree that covers Particular taxonomic problems in the Tre- the vast majority of species of this group for mellomycetes to be solved in the future include which molecular data [nuclear rDNA coding for the obvious nonmonophyly of established mor- the D1/D2 regions of the large ribosomal sub- phogenera, such as Tremella, and the question unit (LSU)] are available, using type or ex-type of how to best treat originally anamorphic sequences wherever possible. It illustrates both genera, such as Bullera and Cryptococcus,ina the phylogenetic resolution presently available modern nomenclature that no longer gives pri- in the Tremellomycetes and the degree to which ority to generic names based on teleomorphs current taxonomy matches the phylogenetic (Hawksworth 2011; McNeill et al. 2012). Since it relationships in this group. Considering the is too early to solve these questions in this text, impressive progress in genome sequencing here we still adopt some widely used names that and phylogenomics we anticipate that at least are likely to change in the near future. the higher-level relationships will be much bet- ter resolved in the near future. II. Morphology and Anatomy

A. Historical Concepts A. Basidiocarps

The genus Tremella was validly described by Basidiocarps (Fig. 12.1) are known from species Persoon (1794). Some years later (Fries 1821) of Tremellales, Holtermanniales, and Filobasi- thegenuswasthebasisforthefamilyTremel- diales (Syzygospora). In species of Tremellales, laceae (as Tremellini, including also Dacry- basidiocarps are mostly of a gelatinous consis- myces), and for the order Tremellales (as tency. Many species can undergo prolonged Tremellinae)—one of the six orders that Fries phases of exsiccation, reviving when rehy- described in his Hymenomycetes—which drated, with renewed growth and production roughly corresponds to what today are called of conidia or basidiospores (Wells and Bandoni jelly fungi. Since the acceptance of basidial 2001). They are thus well adapted to habitats on morphology as a key character in the system- dead wood, on which the more exposed species, atics of the basidiomycetes (Brefeld 1888; for example, Tremella, are often found. Basi- Patouillard 1887;Tulasne1853), Tremella- diocarp forms vary from pustulate, for exam- ceae/Tremellales have often been used as the ple, Tremella spp., Tetragoniomyces,or taxon containing all hymenomycetes with Sirobasidium,tocushion-shaped, lobose-cere- longitudinally septate basidia—as opposed briform, for example, Tremella mesenterica to the Auriculariaceae/Auriculariales, which (Fig. 12.1a, b), to foliose, for example, Tremella according to these concepts included taxa foliacea (Fig. 12.1g) and Tremella fuciformis with transversely septate basidia [see Bandoni (Fig. 12.1h). Often they originate from a host (1984) for a systematic treatment of the fungus that they obviously parasitize (see taxonomic history]. below). Mature basidiocarps may even show a Tremellomycetes and Related Groups

Fig. 12.1 (a–e) Tremella mesenterica.(a) Young basi- fuciformis, bar¼3 cm. (i) Tremella aurantia, bar¼ diocarps on Peniophora laeta growing on Carpinus 3 cm. (j) Sirobasidium magnum, bar 3 cm. (k–m) Syzy- betulus, bar¼2 mm. (b) Mature basidiocarp, bar¼ gospora pallida.(k) Pustular basidiocarps emerging 5 mm. (c) Part of hymenium with basidia, bar¼ from host Phanerochaete cremea, bar¼2 mm. (l) Basid- 10 mm. (d) Yeast budding, bar¼10 mm. (e) Basidio- ium and conidiophores, bar¼10 mm. (m) Budding spore with secondary spore, bar¼5 mm. (f) Tremella yeasts, bar¼10 mm. (n, o) Tetragoniomyces uliginosus. encephala showing whitish core with hyphal mixture of (n) Basidiocarps in culture, bar¼1 mm. (o) Germinat- host Stereum sanguinolentum and mycoparasite, bar¼ ing basidium, bar¼10 mm 1 cm. (g) Tremella foliacea, bar¼2 cm. (h) Tremella M. Weiß et al. central core composed of hyphae of host and order, with transverse or oblique basidial mycoparasite, as in Tremella encephala septa,asinAuriculibuller, Bulleromyces, and (Fig. 12.1f). Basidiocarps in the Holterman- Papiliotrema (Fig. 12.2b). Development of the niales are tough-gelatinous, with a clavarioid basidial compartments is often strongly desyn- appearance. chronized (Wells and Bandoni 2001), and basi- Numerous teleomorphic species in the Tre- dial compartments may detach in some species, mellomycetes apparently lack basidiocarps. for example in Sirobasidium (Fig. 12.2h), before Such species grow intrahymenially in their fun- giving rise to a ballistospore (Bandoni 1984). gal hosts, either without causing any macro- Basidial septation may also be lacking, resulting scopic symptoms, such as Tremella giraffa, in holobasidia,asinCarcinomyces (Fig. 12.3d) Tremella obscura, and Tremella penetrans,or and Filobasidiella (Fig. 12.3a) (Tremellales); inducing galls on their hosts, for example, Filobasidium (Fig. 12.3b) and Syzygospora lichenicolous species of Tremella or Biatoropsis (Fig. 12.3e, f) (Filobasidiales); Cystofilobasi- usnearum. Sexual stages in some species of dium (Fig. 12.3c); and Xanthophyllomyces Tremellales, for example, Bulleribasidium (Cystofilobasidiales). In some species a partial (Fig. 12.2e), Filobasidiella (Fig. 12.3a), Kwo- apical septation in holobasidia has been niella, and Rhynchogastrema (Fig. 12.2f), as reported, for example in Rhynchogastrema well as all known sexual stages in Cystofiloba- (Fig. 12.2f) and Syzygospora (Metzler et al. sidiales, are known only from pure cultures. 1989; Oberwinkler and Lowy 1981). Obviously, a transition from phragmobasidia to holobasi- dia has occurred independently several times in B. Micromorphology the Tremellomycetes (Millanes et al. 2011). Second, there are also exceptions Most species in the Tremellomycetes grow as concerning the development and arrangement yeasts in their haploid stages (Figs. 12.2 and of basidia. While basidia usually appear singly 12.3). Such yeast stages may proliferate by bud- or in clusters proliferating from subbasidial ding, but they may also produce ballistoconidia clamps, for example in basidiomes of Tremella, that are morphologically and functionally simi- basidial chains can be observed in species of lar to basidiospores. Yeast cells are generally Sirobasidium (Fig. 12.2h) and, to a lesser globoid to ellipsoid but may also be elongate, degree, in Sirotrema. In these species, basidia as in Carcinomyces. Diploid stages are generally proliferate basipetally, starting from an apical filamentous, with clamped hyphae. basidium. In Cystofilobasidiales basidia arise There is conspicuous variation in basidial from teliospores (Fig. 12.3c). morphology, which has been one of the most Third, Tremellomycete species differ important characters used in traditional mor- concerning the release and functioning of basi- phogeneric concepts. The basidia of the species diospores. In most teleomorphic species basi- of Tremella are usually longitudinally septate diospores are actively discharged from (so-called tremelloid basidia), with the basidial sterigmata. In Sirobasidium, on the other compartments protruding into elongated tubes, hand, basidia give rise to passively released designated as epibasidia by some authors (Wells fusoid basidiospores (Fig. 12.2h) [alternatively and Bandoni 2001), that pervade the often gelat- designated as epibasidia (Wells and Bandoni inous matrix of their own or the host basidiome 2001)] that may proliferate by budding or by and, finally, apically bear a sterigma, from the formation of secondary spores (Bandoni which the mostly globular basidiospores are 1984). Some other species in the Tremellomy- actively discharged into the air (Fig. 12.4). cetes, such as the phragmobasidiate species of There are, however, numerous variations. Kwoniella and the holobasidiate species of Car- First, tremelloid basidia are only known in cinomyces, produce sessile basidiospores. the Tremellales and in Holtermannia. In some A feasible concept uniting the heterogene- other species of Tremellales the basidial com- ity in basidial morphology observed in the Tre- partments may be arranged in a more linear mellomycetes has been proposed by Bandoni Tremellomycetes and Related Groups

10 µm 10 µm 20 µm d g a

20 µm 10 µm

f e

b

10 µm 20 µm

c h

Fig. 12.2 Basidial characters in Tremellomycetes. (a) and Bandoni 1983). (e) Bulleribasidium oberjochense Cuniculitrema polymorpha (Kirschner et al. 2001). (b) (Sampaio et al. 2001). (f) Rhynchogastrema coronata Papiliotrema bandonii (Sampaio et al. 2001). (c) Tetra- (Metzler et al. 1989). (g) Phragmoxenidium mycophi- AU1 goniomyces uliginosus (Oberwinkler and Bandoni lum (Oberwinkler et al. 1990). (h) Sirobasidium mag- 1981). (d) Trimorphomyces papilionaceus (Oberwinkler num (Chen 1998)

(1984), who suggested that the basidial “com- These structures provide an eloquent example partments” themselves may actually be meiotic of convergent evolution as they are present in products (endospores) that in most species various distantly related groups of basidiomy- form a germtube (the so-called epibasidium) cetes, such as the rust and the smut fungi. to produce a secondary spore (basidiospore in Many presumably mycoparasitic species of common terminology). Longitudinal, trans- Tremellomycetes feature a characteristic tre- verse, or oblique septation of the basidium melloid haustorial type in their filamentous then may simply result from a varying arrange- stages (e.g., Chen 1998; Oberwinkler and Ban- ment of the primary spores (endospores) doni 1981; Zugmaier et al. 1994) (Fig. 12.2c, f, within the basidium. g). Tremelloid haustoria arise from clamp con- Teliospores, i.e., one-celled conidia that nections and consist of single cells that are give rise to basidia after a resting period, are globular or short clavate at the base and extend only known from species of Cystofilobasidiales. into one or more narrow filaments (Fig. 12.4). M. Weiß et al.

20 µm

10 µm

20 µm a e

c

20 µm

20 µm

20 µm b d f

Fig. 12.3 Basidial characters in Tremellomycetes. (a) 1983). (d) Carcinomyes effibulatus (Oberwinkler and Filobasidiella neoformans (Oberwinkler et al. 1983). Bandoni 1982). (e) Syzygospora alba (Oberwinkler (b) Filobasidium floriforme (Oberwinkler et al. 1983). and Lowy 1981). (f) Syzygospora pallida (Oberwinkler (c) Cystofilobasidium capitatum (Oberwinkler et al. et al. 1984)

In an established mycoparasitic interaction the genera Cryptococcus, Bullera, Fellomyces,and apex of the filaments is in contact with a host Kockovaella. Meanwhile, molecular phylogenetic hypha (see subsequent discussion for ultra- studies have shown that this character is not structural details). useful for circumscribing monophyletic genera Several types of conidia have been observed (Boekhout et al. 2011). Consequently, genera in the Tremellomycetes. Globular blastoconidia such as Derxomyces, Dioszegia,andHannaella are occasionally found in Tremellales fruiting have been proposed for monophyletic groups bodies [e.g., in T. mesenterica (Fig. 12.4), where that contain both species with or without the ample production of blastoconidia creates the formation of ballistoconidia. However, the foot- characteristic orange color of the fruiting bod- prints of the old classification marker “presence/ ies], before or synchronously with the produc- absence of ballistoconida” are still visible in the tion of basidia and basidiospores. Production current tree of the Tremellomycetes (Fig. 12.7). of blastoconidia on elongated stalks is known Zygoconidia, i.e., dikaryotic H-shaped con- from species of Fellomyces and Cuniculitrema. idia, are known from several distantly related Arthroconidia are typical of most Trichosporo- taxa, such as Carcinomyces, Papiliotrema, and nales species but can also be found in other Trimorphomyces (Fig. 12.2d) (Tremellales), as species, for example, in Guehomyces and Tau- well as from Syzygospora (Filobasidiales) (e.g., sonia (Cystofilobasidiales). Many species in the Oberwinkler and Bandoni 1983; Oberwinkler Tremellomycetes also form ballistoconidia. and Lowy 1981; Sampaio et al. 2002). The formation or absence of ballistoconidia Finally, four-spined asteroconidia have was used in earlier classifications to separate the been observed in some lichenicolous species Tremellomycetes and Related Groups

yeast conjugation of yeast cells

basidio- spores

saprotrophic basidia hyphae

mycoparasitic

basidiocarp conidia tremelloid haustoria

Fig. 12.4 Life cycle of Tremella mesenterica of Tremella (Diederich 1996; Millanes et al. ever, be missing in some pores of a studied 2011). specimen (R. Bauer, unpublished; Padamsee et al. 2012), which may help to explain some inconsistencies documented in the literature. Spindle pole bodies of the studied species C. Ultrastructure in Tremellales are biglobular during prophase Septal pores in the Tremellomycetes are doli- (Berbee and Wells 1988), a character state that pores that, except for members of Cystofiloba- supports the inclusion of the Tremellomycetes sidiales (Oberwinkler et al. 1983; Wells 1994;R. in Agaricomycotina. Bauer, unpublished), are surrounded at both The cellular interaction between species of sides by sacculate caps arranged in hemispher- the Tremellomycetes and their presumed host ical outlines (Fig. 12.5) (Berbee and Wells fungi occurs via the formation of tremelloid 1988). In three-dimensional configurations haustoria (Figs. 12.2c, f, g and 12.4; see previous these saccules represent fingerlike extensions discussion). The haustorial filaments are capa- of the endoplasmic reticulum surrounding the ble of fusing with host cells via pores of roughly pore on either side (as is visible in one saccule 15 nm in diameter, where plasma membranes of illustrated in Fig. 12.5b), in which the intracis- both fungi are continuous with each other ternal surface of the membrane is accompanied (Fig. 12.6). This yields a direct cytoplasmic con- by an additional electron-opaque nonmembra- tact; however, the size of these fusion channels nous layer (Fig. 12.5b). In cross or oblique sec- prevents an exchange of organelles, including tions, these fingerlike extensions are mapped as ribosomes, between the interacting organisms saccules with abseptal openings (Fig. 12.5b, c). (Bauer and Oberwinkler 1990a; Oberwinkler Saccular parenthesomal elements may, how- et al. 1984; Zugmaier et al. 1994). While in M. Weiß et al.

Fig. 12.5 Septal pore architecture in Tremellomycetes. ments, representative for Tremellomycetes [except for Bar¼0.1 mmin(a–c), 0.2 mmin(d). (a) Dolipore of Cystofilobasidiales; see (a)] and Wallemia.(b, c) Tre- Cystofilobasidium ferigula without specialized multila- mella sp. Cupulate cap elements are sectioned longitu- mellate caps, representative of Cystofilobasidiales. Note dinally in (b), transversally in (c). Continuity between that pore is surrounded at each side by a more or less ER and saccules is visible for one of upper saccules in dome-shaped ER cisterna. (b–d) Dolipores surrounded (b). (d) Wallemia sebi at each side by many multilamellate cupulate cap ele- most studied species of the Tremellomycetes characteristic trait in most species of the Tre- a haustorial filament forms only one fusion mellomycetes for which a teleomorph is channel (Fig. 12.6a, b), in Syzygospora pallida known. A typical life cycle of a Tremella spe- a single haustorial filament may form several cies is illustrated in Fig. 12.4. In these species, protrusions into the host cytoplasm, resulting basidiospores germinate by budding to estab- in numerous fusion channels per filament lish a haploid yeast stage.Sincethisstagecan (Fig. 12.6c, d) (Bauer 2004; Bauer and Ober- easily be maintained in pure culture in stan- winkler 1990b; Oberwinkler et al. 1984). dard media,itisassumedthattheyeaststageis AU2 saprotrophic. Conjugation of compatible yeast cells initi- III. Life Cycles ates a dikaryotic hyphal stage, which is consid- ered mycoparasitic in many species based on two lines of evidence. First, axenic cultivation A. Dimorphism of this stage has seldom been reported (Zugma- Dimorphism, i.e., differing morphological ier and Oberwinkler 1995; Zugmaier et al. organization of different life stages, is a 1994). Second, tremelloid haustoria attached Tremellomycetes and Related Groups

Fig. 12.6 Mycoparasitic interaction stages of some Tre- with plasma membranes of both cells. (c, d) Haustorial mellomycetes. Bars¼0.2 mmin(a, c) and 0.1 mmin(b, filament of Syzygospora pallida penetrating a cell of d). (a, b) Haustorial filament of Tetragoniomyces uligi- Phanerochaete cremea.(c) One of several micropores nosus (upper cell) attached to cell of Rhizoctonia sp. (a) connecting haustorial filament with host cell is medi- Note medianly sectioned micropore (arrow) connect- anly sectioned (arrow). (d) Detail from (c). Note that ing haustorial apex with host cell. (b) Detail from (a) pore membrane (arrowheads) is continuous with Note that pore membrane (arrowheads) is continuous plasma membranes of both cells to hyphae of other fungal speciesare often a teleomorph is possibly induced in the pres- observed microscopically (see previous discus- ence of a particular fungal host. sion). Dikaryotic hyphae may constitute a fruiting body that ultimately produces basidia and basidiospores or conidiogenous hyphae, B. Deviance from Dimorphism giving rise to conidia. In species lacking a fruit- ing body, dikaryotic hyphae grow inside a host The designation of a species of the Tremello- fruiting body and finally sporulate at its sur- mycetes (typically a yeast) as monomorphic face. should always be considered as being prelimi- Holtermanniella mycelialis has been nary. There are instances where a filamentous reported to be dimorphic and haploid (Golubev stage is obtained by mating compatible strains and Golubev 2003). In this species, after some long after the first description of the yeast stage, days of cultivation, yeast colonies build for example, in Bullera/Bulleromyces, Crypto- clamped hyphae with tremelloid haustoria and coccus/Filobasidiella, and Cryptococcus/Kwo- release blastoconidia. Basidia have not been niella. More recently, genomic methods have observed in this species, which may represent been used to predict and ultimately demon- an anamorph of a Holtermannia species, where strate sexuality in fungi that were previously M. Weiß et al. considered asexual (Metin et al. 2010; O’Gor- previous discussion; Bandoni 1984; Bauer and man et al. 2009). Consequently, many other Oberwinkler 1990a; Zugmaier et al. 1994). How- inconspicuous teleomorphs may still await ever, a flux of carbon compounds or other detection and description (Metin et al. 2010). nutrients from a fungal host species to a trem- Some species lack a yeast stage. In Tetra- ellomycete has not yet been demonstrated. goniomyces uliginosus (Fig. 12.2c) basidia do Apparently, the mycoparasitic potential is not produce external basidiospores. Instead, initiated with the transition from the monokar- the thick-walled basidia themselves detach, yotic to the dikaryotic life stage. Molecular and compatible basidial compartments either mechanisms, such as host recognition, are still mate directly or produce germination tubes unknown. that mate (Oberwinkler and Bandoni 1981), That hyphal stages of some phylogeneti- inducing the next hyphal generation. Yeast cally close species of the Tremellomycetes are stages are also unknown for many species of associated with fungi that are closely related Trichosporonales and in Filobasidiella depau- inter se (Fig. 12.7: 22) may be taken as an perata. additional piece of evidence in favor of a myco- Trimorphomyces papilionaceus (Tremel- parasitic lifestyle. Here, strongly dependent tre- lales) is the only known species of the Tremel- mellomycetous mycoparasites may have lomycetes that has a dikaryotic yeast stage in coevolved together with their fungal hosts. addition to the usual haploid yeast stage, which While for the majority of Tremellomycetes arises from budding basidiospores. Here, the species studied to date the axenic cultivation of dikaryotic yeast cells initiate from dikaryotic the dikaryotic stage has not been achieved [but zygoconidia borne on two-tipped conidiogen- see Zugmaier and Oberwinkler (1995)], a suc- ous cells located in either conidiomata or fruit- cessful induction of the teleomorph by mating ing bodies in which the conidiogenous cells compatible yeast cells has been reported for occur together with basidia (Fig. 12.2d). In the some species for which only the haploid stage, presence of a suitable fungal host, zygoconidia i.e., the yeast in most cases, was known previ- alternatively germinate with hyphae that form ously. These include Filobasidiella neoformans, clamps and tremelloid haustoria. Bulleromyces and Kwoniella (Tremellales), and The life cycle of Itersonilia perplexans com- Cystofilobasidium (Cystofilobasidiales). prises clamped dikaryotic hyphae, short unclamped monokaryotic hyphae, monokaryo- tic yeast cells, chlamydosporelike resting cells, B. Tremellomycetous Yeasts and ballistoconidia (Boekhout 2011; F. Ober- winkler, unpublished). Apparently, all of the known yeast stages in the Tremellomycetes can be cultured axenically in standard media. Tremellomycetous yeasts are IV. Ecology ubiquitous elements of terrestrial and aquatic ecosystems and have been reported from Ant- A. Mycoparasitism arctic soils as well as from hydrothermal oce- anic vents. They have been isolated from That a mycoparasitic lifestyle is a distinctive sources as diverse as the surface of land plants, feature of the teleomorphic stages for many, if including flowers and tree bark, from freshwa- not all, members of the Tremellomycetes has ter and seawater samples, from clinical speci- been deduced from obvious host specificity, mens, and from animals or their excrements from morphological evidence, such as the pres- [see Kurtzman et al. (2011)]. Some species ence of hyphae of putative host fungi growing seem to occupy rather diverse niches, for exam- inside fruiting bodies of Tremellomycetes, or ple, Cryptococcus curvatus has been reported from the presence of tremelloid haustoria, mainly from medical sources and from food which may attach to host hyphae and establish products but was also shown to be the domi- minute cytoplasm-to-cytoplasm contacts (see nant microbial eukaryote in sediments of a Tremellomycetes and Related Groups

94 Cryptococcus diffluens AF075502 Cryptococcus liquefaciens AF181515 94 Cryptococcus socialis AF181503 Cryptococcus vishniacii AF189841 59 Cryptococcus albidosimilis AF137606 Cryptococcus adeliensis AF137603 0.1 76 Cryptococcus albidus AF075474 Cryptococcus uzbekistanensis AF181508 99 Cryptococcus saitoi AF181540 82 68 Cryptococcus friedmannii AF075478 Cryptococcus randhawii AJ876599 100 100 Cryptococcus antarcticus AF075488 Cryptococcus bhutanensis AF137599 Filobasidium uniguttulatum HM769334 100 Cryptococcus aciditolerans AY731790 100 Cryptococcus metallitolerans AY731789 Cryptococcus ibericus AY731791 99 Cryptococcus gilvescens AF181547 Cryptococcus gastricus AF137600 100 Syzygospora physciacearum JN043614 Syzygospora bachmannii JN043613 Cryptococcus arrabidensis AF181535 Filobasidium floriforme AF075498 10 Cryptococcus magnus AF181851 57 Filobasidium elegans AF181548 Cryptococcus oeirensis AF181519 Cryptococcus chernovii AF181530 49 Cryptococcus stepposus DQ222456 Filobasidium globisporum AF075495 Cryptococcus wieringae AF181541 100 Syzygospora pallida AJ406403 Syzygospora alba JN043616 9 88 Cryptococcus filicatus EU433983 100 Bullera taiwanensis AB079065 Cryptococcus cylindricus AF181534 48 Syzygospora sorana EU541305 Filobasidium capsuligenum AF363642 44 Cryptococcus terricola AF181520 96 Cryptococcus himalayensis AF181502 88 Cryptococcus terreus AF075479 77 Cryptococcus phenolicus AF181523 50 Cryptococcus fuscescens AF075472 Cryptococcus aerius AF075486 Tremellales 81 Mrakiella niccombsii AY029345 70 Mrakiella aquatica AF075470 Mrakiella cryoconiti AJ866978 8 Mrakia frigida AF075463 7 100 Mrakia gelida AF189831 Mrakia robertii AY038811 Mrakia blollopis AY038814 55 79 Mrakia psychrophila EU224266 96 Udeniomyces pyricola AF075507 6 Trichosporonales 66 Udeniomyces pseudopyricola AY841862 Holtermanniales 98 Udeniomyces megalosporus AF075510 51 Udeniomyces puniceus AF075519 Itersonilia pyriformis DQ441474 5 99 Itersonilia perplexans AJ235274 74 66 Udeniomyces pannonicus AB077382 Filobasidiales 99 Guehomyces pullulans AF257275 4 Tausonia pamirica EF118825 3 Mrakia curviuscula EF118826 100 Cystofilobasidiales 100 Cryptococcus huempii AF189844 79 Cystofilobasidium macerans AF189848 Cystofilobasidium infirmominiatum AF075505 100 Cystofilobasidium bisporidii AF189832 98 Cystofilobasidium ferigula AF075487 Cystofilobasidium capitatum AF075465 2 Xanthophyllomyces dendrorhous AF075496 1

Fig. 12.7 (continued) M. Weiß et al.

100 Trichosporon xylopini HQ005757 41 Trichosporon porosum AF189833 Trichosporon sporotrichoides AF189885 Trichosporon coprophilum AB180199 66 0.1 Trichosporon wieringae AY315666 Trichosporon lignicola AF363658 Trichosporon loubieri AF075522 Trichosporon mycotoxinivorans AJ601388 Trichosporon multisporum AF139984 Trichosporon veenhuisii AF105400 Trichosporon laibachii AF075514 Trichosporon akiyoshidainum AB180200 Trichosporon vadense AY093426 88 Trichosporon gracile AF105399 Trichosporon dulcitum AF075517 Trichosporon chiropterorum AB180197 48 Trichosporon cacaoliposimilis HM802134 Trichosporon dulcitum GQ222351 56 99 Trichosporon domesticum AF075512 73 Trichosporon montevideense AF105397 69 Trichosporon brassicae AF075521 62 Trichosporon otae AB180196 Trichosporon scarabaeorum AF444710 Trichosporon guehoae AF105401 81 Trichosporon shinodae AB180201 Trichosporon cavernicola AB180195 Trichosporon jirovecii AB492270 59 Trichosporon oleaginosus HM802135 54 Trichosporon cutaneum AF075483 Trichosporon debeurmannianum AB044568 89 64 Trichosporon middelhovenii AB180198 Trichosporon terricola AB086382 Trichosporon moniliiforme AF105392 Trichosporon mucoides AB492276 57 64 Trichosporon dermatis AB044569 Cryptococcus haglerorum AF407276 Cryptococcus arboriformis AB260936 Cryptococcus daszewskae AB126588 Trichosporon chiarellii EU030272 48 Trichosporon japonicum AF308657 Trichosporon insectorum AY520383 77 Trichosporon asahii AB492277 92 69 Trichosporon asteroides AF075513 Trichosporon faecale AF105395 60 49 71 Trichosporon lactis AJ319756 Trichosporon caseorum AJ319757 Trichosporon ovoides AF075523 55 100 Trichosporon inkin AF105396 Trichosporon coremiiforme AF139983 Trichosporon aquatile AF075520 Tremellales 83 Cryptococcus cyanovorans JF680899 Cryptococcus curvatus AF189834 99 Vanrija pseudolonga AB126587 55 Vanrija longa AB126589 70 Vanrija humicola AF189836 15 72 86 Vanrija albidus AB126584 Vanrija musci AB126586 Cryptococcus fragicola AB126585 Trichosporonales Bullera koratensis AY313006 92 Bullera formosensis AB090946 Holtermanniales Bullera lagerstroemiae AY313010 45 Tetragoniomyces uliginosus JN043621 14 Cryptotrichosporon anacardii AY550002 13 Cryptococcus marinus AF189846 98 Holtermanniella mycelialis AJ311450 Filobasidiales 71 Holtermanniella nyarrowii AY006480 96 Holtermanniella takashimae FM242574 12 60 Holtermanniella festucosa AY462119 Cystofilobasidiales 100 Holtermanniella watticus AY138478 Holtermannia corniformis AF189843 11

Fig. 12.7 (continued) Tremellomycetes and Related Groups

63 Dioszegia fristingensis AY562146 Dioszegia statzelliae AY029341 Dioszegia changbaiensis AY242819 Dioszegia butyracea EU070929 0.1 78 Dioszegia aurantiaca AB104689 Dioszegia crocea AF075508 Dioszegia xingshanensis EU070928 51 Dioszegia hungarica AF075503 94 Dioszegia buhagiarii AY562151 Dioszegia rishiriensis AB545810 Dioszegia takashimae AY562149 98 Dioszegia zsoltii AF544245 20 Dioszegia athyri EU070931 80 Dioszegia catarinonii AY562142 96 Bullera formosana AB119465 Bullera melastomatis AB119464 74 Derxomyces pseudohuiaensis AF544250 Derxomyces qinlingensis EU517060 44 Derxomyces wuzhishanensis EU517063 Derxomyces cylindrica AY487563 Derxomyces mrakii AB118871 19 62 Derxomyces boninensis AY487568 47 Derxomyces huiaensis AB118870 93 Derxomyces waltii AY487569 Derxomyces nakasei AY487564 Derxomyces boekhoutii EU517057 Derxomyces hainanensis EU517056 Derxomyces pseudocylindrica EU517059 47 77 Derxomyces pseudoschimicola AF544248 Tremellales Derxomyces schimicola AY487570 Derxomyces komagatae AF544249 43 Derxomyces simaoensis EU517062 Derxomyces hubeiensis AY487566 Derxomyces linzhiensis EU517058 58 55 Hannaella coprosmaensis AF363660 Hannaella kunmingensis AB109558 Hannaella luteola AF075482 Trichosporonales 42 Hannaella zeae AJ965480 93 Hannaella sinensis AF189884 18 Holtermanniales Hannaella oryzae AF075511 Hannaella surugaensis AB100440 Cryptococcus podzolicus AF075481 Cryptococcus neoformans var. neoformans AF189845 17 Cryptococcus gattii AF075526 Filobasidiales 78 Cryptococcus neoformans var. grubii FJ534909 100 Filobasidiella depauperata AF487884 Cryptococcus amylolentus AF105391 Cystofilobasidiales 59 Carcinomyces effibulatus JN043605 16 49 Tremella polyporina JN043607 Bullera arundinariae AF547661 Fig. 12.7 (continued) methane seep at a water depth of 640 m in the Some species of Fellomyces have only been Pacific Ocean (Takishita et al. 2006). For some found on lichen thalli (Lopandic et al. 2011). species ecological trends are visible. Psychro- For many, if not most, of the known spe- philic species, such as members of Mrakia, have cies, however, data are still too sparse to esti- been isolated in Antarctica or Greenland or mate distribution and ecology with confidence. from glaciers but were also reported from Additionally, it may be problematic to integrate refrigerated food (Fell 2011). Bullera alba is data based on morphological and physiological frequently isolated from the phylloplane (Sam- species determination with data based on paio 2004). Xanthophyllomyces dendrorhous is sequence-based identification. Since all known known from the sap of various tree species tremellomycetous yeast species have been (David-Palma et al. 2014; Fell et al. 2011). DNA-barcoded, analysis of environmental M. Weiß et al.

91 Tremella tropica AF042251 54 Tremella mesenterica AF075518 26 69 Tremella taiwanensis AF042230 0.1 48 Tremella brasiliensis AF189864 Tremella globispora AF189869 100 Tremella flava AF042221 40 51 Tremella cinnabarina AF189866 97 Cryptococcus yokohamensis HM222927 Tremella fuciformis AF075476 Tremella resupinata AF042239 49 Cryptococcus dejecticola AY917102 Bullera dendrophila AF189870 99 Cryptococcus bestiolae FJ534903 Kwoniella mangrovensis AF444742 25 58 Kwoniella heveanensis AF075467 Cryptococcus cuniculi DQ333885 67 Cryptococcus carnescens DQ516975 Cryptococcus victoriae AF363647 Cryptococcus tephrensis DQ000318 Cryptococcus laurentii DQ644575 63 Cryptococcus foliicola AY557599 Tremellales 93 Cryptococcus heimaeyensis DQ000317 98 Cryptococcus taibaiensis AY557601 100 Bullera globispora AF075509 96 Cryptococcus dimennae AF075489 Trimorphomyces nebularis EU266921 24 Tremella parmeliarum JN043618 86 Bullera sakaeratica AY211546 23 Trimorphomyces papilionaceus AF416645 Trichosporonales 62 Tremella tuckerae JN043588 Tremella coppinsii JN043601 Holtermanniales Tremella wirthii JN043598 Tremella pertusariae JN043600 Tremella lichenicola JN043611 22 Bullera miyagiana AF189858 Filobasidiales Tremella cetrariicola JN043596 Biatoropsis usnearum JN043592 21 Tremella everniae JN043599 46 Tremella hypogymniae JN043590 Cystofilobasidiales Tremella giraffa AF042271 Fig. 12.7 (continued) high-throughput sequencing data should refine of the leading pathogens worldwide that can be our estimates about biogeography and ecology grown from cerebrospinal fluid (Perfect 2005). in the future. Each year cryptococcal meningoencephalitis is diagnosed in nearly a million individuals and accounts for more than 600,000 deaths (Park et al. 2009). Even if treated with state-of-the-art C. Animal and Human Pathogens therapy, cryptococcosis is fatal in ca. 20 % of C. neoformans, the yeast stage of F. neoformans, cases (Desnos-Ollivier et al. 2010). As the is an opportunistic pathogen in immunocom- closely related Cryptococcus gattii (anamorph promised humans and animals around the of Filobasidiella bacillispora), C. neoformans world. The fungus is able to infest immuno- apparently has a wide spectrum of potential competent individuals without causing notice- host taxa, including both vertebrate and inver- able disease symptoms. However, in tebrate species and even protozoans [see Kwon- immunocompromised individuals, for exam- Chung (2011)]. ple, those with an HIV infection, it may dissem- The genus Trichosporon contains many inate from a local infection to any organ of a known pathogens of animals and humans, and patient and in particular invade the central more than 30 % of Trichosporon species were nervous system. Today, C. neoformans is one found to be correlated with human infections Tremellomycetes and Related Groups

Cryptococcus nemorosus AF472625 59 Cryptococcus perniciosus AF472624 40 Papiliotrema bandonii AF416642 37 Cryptococcus anemochorus DQ384929 0.1 98 Cryptococcus flavescens AB035042 89 Cryptococcus terrestris EF370393 Cryptococcus aureus AB035041 Auriculibuller fuscus AF444762 36 63 Cryptococcus amylolyticus AY562134 98 Cryptococcus armeniacus AY562140 Cryptococcus bromeliarum DQ784566 Bullera pseudoalba AF075504 Cryptococcus rajasthanensis AM262324 Rhynchogastrema coronatum KJ170152 35 Tremella candelariellae JN043575 100 Tremella dendrographae JN043576 75 Tremella christiansenii JN043577 Tremella caloplacae JN043573 92 Tremella exigua AF042248 Sirobasidium intermedium AF075492 34 Cryptococcus mujuensis DQ333884 94 Tremella moriformis AF075493 89 Tremella nivalis AF042232 58 Cryptococcus allantoinivorans AY315662 Tremella indecorata AF042250 97 Bullera unica AF075524 Bulleromyces albus AF416643 33 Tremella haematommatis JN043617 Kockovaella litseae AB292850 Kockovaella calophylli AB292852 72 Kockovaella cucphuongensis AB292853 Kockovaella vietnamensis AB292851 47 Kockovaella asplenii AB189066 44 Fellomyces sichuanensis AF189879 81 Fellomyces thailandicus AF363644 Fellomyces mexicanus AJ627906 Fellomyces chinensis AF189878 Kockovaella barringtoniae AB292854 Fellomyces horovitziae AF189856 53 Fellomyces fuzhouensis AF363659 99 Kockovaella thailandica AF075516 32 Kockovaella imperatae AF189862 96 Cuniculitrema polymorpha AY032662 31 74 Fellomyces polyborus AF189859 30 99 Fellomyces penicillatus AF177405 Fellomyces borneensis AF189877 96 Tremella microspora AF042253 85 Tremella aurantia AF189842 59 Tremella aurantialba EF010939 88 Tremella encephala AF189867 Cryptococcus cistialbidi AY562135 44 66 Tremella lobariacearum JN043579 69 Tremella nephromatis JN043581 Tremellales 100 Tremella cladoniae JN043583 Tremella leptogii JN043582 56 Tremella phaeophysciae JN043585 Bulleribasidium oberjochense AF416646 29 100 Bullera pseudovariabilis AF544247 Bullera variabilis AF189855 62 72 Bullera begoniae AB119462 100 87 Bullera panici AY188387 Trichosporonales Bullera siamensis AY188388 Holtermanniales Bullera setariae AB119463 99 Cryptococcus flavus AF075497 Cryptococcus paraflavus AY395799 Tremella simplex AF042246 45 Tremella mycophaga AF042249 Filobasidiales Tremella mycetophiloides JN043608 46 Tremella neofoliacea AF042236 Cryptococcus skinneri AF189835 93 Tremella foliacea AF189868 Cystofilobasidiales Cryptococcus fagi DQ054535 56 Fibulobasidium murrhardtense AF416648 100 Fibulobasidium sirobasidioides AF416644 59 Fibulobasidium inconspicuum AF363641 28 Sirobasidium magnum AF075475 27

Fig. 12.7 (continued) M. Weiß et al.

or allergies. Trichosporon infections are partic- even in cold environments (Bergauer et al. 2005). ularly threatening for immunodeficient patients Other species can be used as sources of enzymes suffering from leukemia or lymphoma. Species with particular characteristics, for example, often seen associated with patients with a deep- cold- and high-pressure-tolerant polygalacturo- seated, and potentially fatal, trichosporonosis nases from the deep-sea yeast C. liquefaciens include T. asahii, T. asterioides, T. debeurman- (Abe et al. 2006). Tremellomycetous yeasts, for nianum, T. inkin, T. loubieri, and T. mucoides example C. albidus and C. laurentii, may be used [see Sugita (2011)]. Trichosporon species have in the biocontrol of plant-pathogenic fungi, for also been shown to be involved in summer-type example Botrytis, and to reduce postharvesting hypersensitivity pneumonitis (SHP), an allergic decay of fruits (Fonseca et al. 2011). C. curvatus disease occurring in hot and humid seasons in can use celluloses and hemicelluloses to produce Asia that is caused by inhalation of Trichos- triglycerides and accumulates these lipids at poron arthroconidia. Causative species include levels of 60 % cell dry weight [see Fonseca et al. T. dermatis (Sugita 2011), a taxon that has also (2011) for detailed references], which makes this been isolated from hydrothermal fields in the species interesting for biomass conversion. Mid-Atlantic Ridge (Gadanho and Sampaio X. dendrorhous is cultured industrially for 2005). Finally, Trichosporon species can cause its ability to produce carotenoids, predomi- infections on skin and hair, for example, white nantly astaxanthin, which can be used, for piedra. example, as a dietary additive for mariculture A prerequisite for a fungal species that is of crustaceans or salmonids to enhance these potentially pathogenic for humans is its ability animals pigmentation. to grow at 37 C. This criterion is used as a routine test in classical yeast taxonomy. That growth at 37 C is not sufficient to prove path- VI. Phylogenetic Relationships ogenicity may be illustrated by Trichosporon louberi, a species not known as a pathogen, which is able to grow even at 42 C but that Based on morphological, ultrastructural, chem- has been reported from soils in Antarctic Dry ical, and ecological data, the monophyly of Tre- Valleys (Fell et al. 2006). mellomycetes as conceived here has been suggested by various authors, for example, Wells (1994, as Tremellales) and Wells and Bandoni (2001, as Tremellomycetidae). Molec- V. Biotechnological Applications ular phylogenetic analyses have supported this hypothesis, for example, Matheny et al. (2006) Biotechnological applications have been repor- and Weiß and Oberwinkler (2001). However, ted for a number of tremellomycetous yeasts. some molecular studies based on nrDNA have Some examples are provided here. Cryptococcus yielded alternative topologies, in which tremel- terreus and Cryptococcus terricola may be useful lomycetous taxa form a grade, with a more in the biodegradation of phenolic compounds, basal Cystofilobasidiales separated from the ◂ Fig. 12.7 Phylogenetic relationships in Tremellomy- v7.3.2 (Stamatakis et al. 2008) in a parallelized version cetes, as estimated from nuclear rDNA sequences cod- at Bioportal (Kumar et al. 2009) using GTR+CAT ing for 50 terminal domain of ribosomal large subunit model of DNA substitution and with heuristic searches (nLSU). Sequence sampling based on comprehensive starting from bootstrap trees (Stamatakis et al. 2008). search of GenBank nucleotide collection (http://www. Branch support was calculated from 1,000 bootstrap ncbi.nlm.nih.gov/), yielding preliminary set of ca. 1,700 replicates; values below 40 % omitted. The tree was sequences, which was gradually pruned by eliminating rooted with Cystofilobasidiales. Branch lengths are in duplicate and dubious sequences after preliminary terms of number of expected substitutions per align- phylogenetic analyses. Sequences were aligned with ment site (see bar); intersected branches were reduced MAFFT v7.045b (Katoh and Standley 2013), a in length by half for graphical presentation. Numbers in maximum-likelihood tree was derived with RAxML circles referenced in text Tremellomycetes and Related Groups remainig taxa (Bauer et al. 2006; Matheny et al. 2012) has abandoned taxonomic priority for 2006; Millanes et al. 2011). Within Agaricomy- teleomorphic stages, principally rendering cotina, Tremellomycetes obtains a basal posi- obsolete taxa that had been established for tele- tion (Floudas et al. 2012; James et al. 2006; Weiß omorphic stages detected in groups that for- et al. 2004). merly only contained anamorphic species, for The phylogenetic tree derived for this example, Bulleromyces, Bulleribasidium, and review from a comprehensive sampling of Cuniculitrema. Likewise, it is no longer neces- nrLSU data is shown in Fig. 12.7. We did not sary to keep genera for anamorphs in originally test whether or not Cystofilobasidiales is part of solely teleomorphic groups, for example, Hol- a monophyletic Tremellomycetes and so did termanniella and Mrakiella. Some of these not include any outgroup sequences, which more recently created names for teleomorphic increased alignment quality. Consistent with or anamorphic genera may be used to define the current literature, our tree was rooted with appropriate monophyletic subgroups in the Cystofilobasidiales. Filobasidiales branches future. Ongoing discussions in the mycological next, followed by Holtermanniales, which is community will yield proposals about consistent with Millanes et al. (2011) and which of the competing names to conserve or Wuczkowski et al. (2011), but in contrast to abandon. the analysis by Boekhout et al. (2011), where a sister-group relationship of Holtermanniales and Filobasidiales received high bootstrap sup- port. The most basal branch in the remaining B. Taxonomic Synopsis subtree is occupied by Cryptococcus marinus,a What follows is a synopsis of generic names in the species that was found in an isolated position in Tremellomycetes that are currently in use. As of this several studies, for example, Boekhout et al. writing, questions regarding the taxonomic priority of (2011) and Scorzetti et al. (2002). Trichospor- names versus names to be conserved that have emerged onales and Tremellales appear as sister groups, as a result of the ICN (McNeill et al. 2012) (see the consistent with Boekhout et al. (2011) but in discussion in the previous section) have not been resolved. Therefore, we include both anamorph- and contrast to other analyses where Trichosporo- teleomorph-derived names for groups in which one or nales cluster nested within Tremellales (Mill- the other will probably be eliminated in the future. anes et al. 2011; Sampaio 2004). Taxa typified with a teleomorph are designated by an asterisk (*).

VII. Taxonomy Cystofilobasidiales Fell, Roeijmans & Boekhout 1999

A. Taxonomy in Flow Cryptococcus Vuill. 1901 p.pte (type C. neoformans) (Fig. 12.7: 17) Among all groups of Agaricomycotina, Tremel- Cystofilobasidium* Oberw. & Bandoni 1983 (type C. capitatum) (Fig. 12.7:2) lomycetes is particularly prone to future taxo- Guehomyces Fell & Scorzetti 2004 (type G. pullulans) nomic changes. First, molecular phylogenetic (Fig. 12.7:4) studies strongly suggest that Tremella, the larg- Itersonilia Derx 1948 (type I. perplexans) (Fig. 12.7:5) est teleomorphic genus in this group, is non- Mrakia* Y. Yamada & Komag. 1987 (type M. frigida) monophyletic (Fig. 12.7) (Boekhout et al. 2011; (Fig. 12.7:7) Mrakiella Margesin & Fell 2008 (type M. cryoconiti) Millanes et al. 2011). The same is true for the (Fig. 12.7:8) main anamorphic genera, Bullera and Crypto- Phaffia M.W. Mill., Yoney. & Soneda 1976 (type P. coccus (Fig. 12.7). Accordingly, segregation of rhodozyma) (Fig. 12.7:1) subgroups of these catch-all genera is being or Tausonia Babeva 1998 (type M. pamirica) (Fig. 12.7:3) already has been implemented (e.g., Derxo- Udeniomyces Nakase & Takem. 1992 (type U. pyricola) (Fig. 12.7:6) myces, Dioszegia, Hannaella, Vanrija). Second, Xanthophyllomyces* Golubev 1995 (type X. dendrorhous; the International Code of Nomenclature for teleomorph of Phaffia rhodozyma)(Fig.12.7:1) algae, fungi, and plants (ICN) (McNeill et al. M. Weiß et al.

Filobasidiales Ju¨lich 1981 Filobasidiella* Kwon-Chung 1976 (type F. neoformans, teleomorph of Cryptococcus neoformans) (Fig. 12.7: 17) Bullera Derx 1930 p.pte (type B. alba) (Fig. 12.7: 33) Hannaella F.Y. Bai & Q.M. Wang 2008 (type H. sinensis) Cryptococcus Vuill. 1901 p.pte (type C. neoformans) (Fig. 12.7: 18) (Fig. 12.7: 17) Kockovaella Nakase, I. Banno & Y. Yamada 1991 (type Filobasidium* L.S. Olive 1968 (type F. floriforme) K. thailandica) (Fig. 12.7: 32) (Fig. 12.7: 10) Kwoniella* Statzell-Tallman, Belloch & J.W. Fell 2008 Syzygospora* G.W. Martin 1937 (type S. alba) (type K. mangrovensis) (Fig. 12.7: 25) (Fig. 12.7:9) Papiliotrema* J.P. Samp., M. Weiß & R. Bauer 2002 (type P. bandonii) (Fig. 12.7: 37) Holtermanniales Phragmoxenidium* Oberw. 1990 (type Phragmoxeni- dium mycophilum; no DNA data available) Phyllogloea* Lowy 1961 (type P. singeri; no DNA data Holtermannia* Sacc. & Traverso 1910 (type H. pinguis) available) (Fig. 12.7: 11) Rhynchogastrema* B. Metzler & Oberw. 1989 (type R. Holtermanniella Libkind, Wuczkowski, Turchetti & coronatum) (Fig. 12.7: 35) Boekhout 2010 (type H. takashimae) (Fig. 12.7: 12) Sigmogloea* Bandoni & J.C. Krug 2000 (type S. tremel- loidea; no DNA data available) Trichosporonales Boekhout & Fell 2001 Sirobasidium* Lagerh. & Pat. 1892 (type S. sangui- neum) (Fig. 12.7: 27, 34) Sirotrema* Bandoni 1986 (type S. pusilla; no DNA data Bullera Derx 1930 p.pte (type B. alba) (Fig. 12.7: 33) available) Cryptococcus Vuill. 1901 pro parte (type C. neoformans) Sterigmatosporidium G. Kraep. & U. Schulze 1983 (type (Fig. 12.7: 17) S. polymorphum, the anamorph of Cuniculitrema p.) Cryptotrichosporon Okoli & Boekhout 2007 (type C. (Fig. 12.7: 31) anacardii) (Fig. 12.7: 13) Tremella* Pers. 1794 (type T. mesenterica) (Fig. 12.7: Tetragoniomyces* Oberw. & Bandoni 1981 (type T. 26) uliginosus) (Fig. 12.7: 14) Tremellina Bandoni 1986 (type T. pyrenophila; no DNA Trichosporon Behrend 1890 (type T. beigelii) data available) Vanrija R.T. Moore 1980 (type V. humicola)(Fig.12.7:15) Trimorphomyces* Bandoni & Oberw. 1983 (type T. papilionaceus) (Fig. 12.7: 23, 24) Tremellales Fr. 1821 Xenolachne* D.P. Rogers 1947 (type X. flagellifera;no DNA data available) Auriculibuller* J.P. Samp. & Fonseca 2004 (type A. fuscus) (Fig. 12.7: 36) Incertae sedis Bandoniozyma P. Valente, Pagnocca, C.A. Rosa, C.F. ´ Lee, S.O. Suh, M. Blackw., G. Peter & Fell 2012 (type Dictyotremella Kobayashi 1971 (type Dictyotremella B. noutii) novoguineensis; no DNA data available) Biatoropsis* Ra¨sa¨nen 1934 (type B. usnearum) Heteromycophaga P. Roberts 1997 (type H. glandulo- (Fig. 12.7: 21) sae; no DNA data available) Bullera Derx 1930 p.pte (type B. alba) (Fig. 12.7: 33) Hyalococcus Schroeter 1889 Bulleribasidium* J.P. Samp., M. Weiß & R. Bauer 2002 Neotremella Lowy 1979 (type N. guzmanii; no DNA (type B. oberjochense) (Fig. 12.7: 29) ´ data available) Bulleromyces* Boekhout & A. Fonseca 1991 (type B. Bartheletia (type B. paradoxa) albus) (Fig. 12.7: 33) Wallemia (type W. ichthyophaga) Carcinomyces* Oberw. & Bandoni 1982 (type C. myce- tophilus) (Fig. 12.7: 16) Cryptococcus Vuill. 1901 p.pte (type C. neoformans) (Fig. 12.7: 17) Cuniculitrema* J.P. Samp. & R. Kirschner 2001 (type C. C. Key Groups polymorpha; teleomorph of Sterigmatosporidium polymorphum) (Fig. 12.7: 31) 1. Cystofilobasidiales Derxomyces F.Y. Bai & Q.M. Wang 2008 (type D. mra- kii) (Fig. 12.7: 19) Whether this is the most basal group in the Dioszegia Zsolt 1957 (type D. hungarica) (Fig. 12.7: 20) Tremellomycetes or whether Cystofilobasi- Fellomyces Y. Yamada & I. Banno 1984 (type F. poly- borus) (Fig. 12.7: 30) diales should be excluded from Tremellomy- Fibulobasidium* Bandoni 1979 (type F. inconspicuum) cetes in order to assure its monophyly has not (Fig. 12.7: 28) yet been answered with certainty (see preceding Tremellomycetes and Related Groups

Sect. VI). According to molecular phylogenetic 3. Holtermanniales analyses [e.g., Boekhout et al. (2011); this study, Fig. 12.7] the order splits into Cystofilobasi- Holtermanniales is the most understudied dium, Xanthophyllomyces (both with slender order in the Tremellomycetes. It currently con- holobasidia), and a clade containing Mrakia/ tains the teleomorphic species of Holtermannia Mrakiella and several anamorphic species of and some yeast species, for which the genus Tausonia/Guehomyces, Itersonilia, and Udenio- Holtermanniella was recently established myces. A characteristic trait of the order, which (Wuczkowski et al. 2011). The only Holterman- is absent in all other groups of the Tremello- nia species that has been cultured and mycetes, is the formation of teliospores, which sequenced is Holtermannia corniformis, with can be observed in species of Cystofilobasidium small clavarioid and anatomically complex and Mrakia. Teleomorphs are holobasidiate basidiomes reminiscent of Calocera (Bandoni producing sessile basidiospores. Dolipores et al. 2011) and tremelloid basidia. Since H. lack parenthesomes (Fig. 12.5a); basidiomes corniformis grows on ascomycetous stromata are not known in this group. Species of Cysto- on dead wood and possesses tremelloid haus- filobasidium and Xanthophyllomyces produce toria, it is probably a mycoparasitic species. carotenoids, a trait that is commercially used Based on the available morphological data the in X. dendrorhous, where the carotenoid astax- other six described species of Holtermannia do anthin produced by an optimized strain is used not seem to be closely related to H. corniformis in industrial mariculture (Johnson and Schroe- (Bandoni et al. 2011); thus, detailed morpho- der 1995). Biogeographically, some species of logical studies and analyses of sequence data the Cystofilobasidiales, for example, Cystofilo- are needed to clarify their phylogenetic posi- basidium bisporidii, and the species of Mrakia/ tion. While species of Holtermannia are only Mrakiella are clearly cold-adapted and have known from Southeast Asia and Brazil (Kirk been found in Arctic environments. et al. 2008), Holtermanniella species have been reported from Europe and North America.

2. Filobasidiales 4. Trichosporonales Filobasidiales contains a taxonomically hetero- This order nearly exclusively comprises ana- geneous assemblage of species. Teleomorphic morphic species, most of which are character- species have been assigned to the morphogenera ized by the formation of hyphae and Filobasidium and Syzygospora, neither of which arthroconidia (Trichosporon) and the lack of a seems to represent monophyletic taxa in their yeast stage. If merged with some yeast species current circumscription (Fig. 12.7) (Boekhout that probably secondarily lost the ability to et al. 2011; Millanes et al. 2011). Teleomorphic form arthroconidia and are still classified in species have holobasidia; spores are sessile in Cryptococcus, Trichosporon may represent a most species. Species of Filobasidium have char- monophyletic group (Fig. 12.7). Roughly one- acteristically elongate slender basidia bearing third of all described Trichosporon species are apically a whorl of sessile basidiospores associated with human infections or allergic (Fig. 12.2b). Macroscopically visible fruiting diseases (Sugita 2011). bodies may be present (Syzygospora alba, Syzy- Following Fonseca et al. (2011) and Sugita (2011)we gospora pallida)(Fig.12.1k) or absent. Parenthe- give Vanrija (Moore 1980) nomenclatural priority over somes are lacking in S. pallida (Oberwinkler et al. Asterotremella (Prillinger et al. 2007) for a monophy- 1984). Species of Syzygospora parasitize fruiting letic group of yeasts closely related to Trichosporon that lack arthroconidia and formerly were classified in Cryp- bodies of asco- or basidiomycetes or lichen thalli tococcus (humicola group) (Fig. 12.7: 15). Thus, we (Diederich 1996; Oberwinkler et al. 1984). The restrict the original concept of Vanrija (Moore 1980, ecology of most other Filobasidiales species is 1987) to the humicola clade of the Trichosporonales not known; strains have been isolated from dif- and add some species that were described later. Our ferent sources such as plants, animals, or soils. emended concept includes the new combinations Van- M. Weiß et al. rija albida (C. Ramı´rez) M. Weiß, Vanrija longa (M. since most described species of Tremella are Takash., Sugita, Shinoda & Nakase) M. Weiß, Vanrija still without sequence data, this may be a pre- musci (M. Takash., Sugita, Shinoda & Nakase) M. Weiß, liminary observation. and Vanrija pseudolonga (M. Takash., Sugita, Shinoda & Nakase) M. Weiß based on Sporobolomyces albidus Other teleomorphic genera of the Tremel- C. Ramı´rez (Ramı´rez Go´mez 1957, p. 238), Cryptococcus lales with sequenced members include longus M. Takash., Sugita, Shinoda & Nakase (Taka- Auriculibuller, Biatoropsis, Bulleribasidium, shima et al. 2001, p. 2207), Cryptococcus musci M. Bulleromyces, Carcinomyces, Cuniculitrema, Takash., Sugita, Shinoda & Nakase (Takashima et al. Fibulobasidium, Filobasidiella, Kwoniella, Papi- 2001, p. 2207), and Cryptococcus pseudolongus M. Takash., Sugita, Shinoda & Nakase (Takashima et al. liotrema, Rhynchogastrema, Sirobasidium,and 2001, p. 2208), respectively. Trimorphomyces. In current molecular phyloge- netic analyses (e.g., Boekhout et al. 2011;Mill- Interestingly, in our molecular phyloge- anes et al. 2011; this study) (Fig. 12.7), these taxa netic analysis, as well as in Millanes et al. appear scattered over the Tremellales tree. Since (2011), Tetragoniomyces uliginosus (Fig. 12.7: backbone resolution is still poor, we will not 14) seems to be a basal member of the Trichos- speculate about phylogenetic relationships poronales. If this position is verified in future here. Basidial morphology in these taxa varies analyses, this species would be the only mem- from longitudinally to obliquely to transversely ber of this order for which a sexual stage is or irregularly septate to nonseptate (see Micro- known. Like most species of Trichosporon, but morphology in Sect. II). Species of Carcinomyces in contrast to the majority of species in Tremel- and Filobasidiella have holobasidia; basidia in lomycetes, Tetragoniomyces lacks a yeast stage. Rhynchogastrema are apically partially septate. Tetragoniomyces basidia detach, and compati- In many instances teleomorphic species appear ble basidial compartments fuse either directly closely related to yeast species for which teleo- or via germination tubes to establish a new morphic stages have not yet been observed. dikaryotic hyphal cell (Fig. 12.2c). Some parts of the tree contain monophy- letic clades that are currently exclusively com- posed of yeast species. Some of these have 5. Tremellales recently been transferred from Cryptococcus or Bullera into genera of their own, for exam- Tremellales is the largest group in the Tremel- ple, Dioszegia and Hannaella. lomycetes and shows a high diversity of fea- Of the various families that have been pro- tures regarding life cycles and morphology. posed in Tremellales in the past, only two, Within the Tremellomycetes, Tremellales har- Cuniculitremaceae and Sirobasidiaceae, seem bors most of the teleomorphs with conspicuous to represent monophyletic groups. A typical basidiocarps, most of which are still classified feature present in Cuniculitremaceae (Fello- in the genus Tremella [ca. 90 species; Kirk et al. myces, Kockovaella, Cuniculitrema) is the (2008)]. However, according to molecular production of ballistoconidia on elongate con- phylogenetic analyses (e.g., Boekhout et al. idiophores. Members of Sirobasidiaceae (Fibu- 2011; Millanes et al. 2011; this study) lobasidium, Sirobasidium) form cylindrical to (Fig. 12.7), Tremella seems to be polyphyletic fusiform and passively released basidiospores and, consequently, will have to be split into that are possibly homologous to the epibasidial monophyletic subgroups in future classifica- tubes in Tremella (Wells and Bandoni 2001). tions. Obviously it will also be necessary to The production of basidiospores in chains include anamorphic yeast species (in current is a unique feature of the species of Filobasi- taxonomy mostly still assigned to Cryptococcus diella. Teleomorphs of this genus have never or Bullera) in most of these subgroups to ren- been reported from natural environments and der them monophyletic. Judging from pub- are only known from in vitro fusion of compat- lished sequence data, yeast stages of ible yeast strains. Since C. neoformans, the sequenced Tremella species have not yet been most virulent pathogen in the Tremellomycetes isolated from environmental samples; however, (see Animal and Human Pathogens in Sect. IV), Tremellomycetes and Related Groups is the type species of its genus, Cryptococcus stress and are hence regularly detected as con- may in the future be restricted to species now taminants of low-moisture foods (Zalar et al. known as Filobasidiella. 2005). Ultrastructural data have shown the basid- In recent molecular phylogenetic studies iomycetous nature of Wallemia sebi (Moore (Millanes et al. 2011; this study) (Fig. 12.7: 16), 1986). However, molecular phylogenetic analyses Carcinomyces effibulatus, a holobasidiate spe- could not unambiguously assign it to any of the cies parasitizing the agaric Gymnopus dryophi- major basidiomycetous clades (Matheny et al. lus and inducing the formation of characteristic 2006). Recent phylogenomic studies with limited tumors in the host basidiomes, was found to be taxon sampling placed Wallemia in a basal posi- included in Tremellales. Preliminary sequence tion within the Agaricomycotina (Padamsee et al. data (M. Weiß, unpublished) suggest that this 2012;Zajcetal.2013). The septal pore apparatus taxon is conspecific with Carcinomyces myceto- of W. sebi resembles that of Tremellales philus and Carcinomyces tumefaciens. We thus (Fig. 12.5d) (Padamsee et al. 2012). reinstall Carcinomyces (Oberwinkler and Ban- doni 1982), a genus apparently well separated from species of Syzygospora (Filobasidiales) VIII. Conclusions (Fig. 12.7, part 1), with which Carcinomyces had been merged earlier (Ginns 1986). We have provided an overview of Tremellomy- cetes, a basal group in the Agaricomycotina. Incertae Sedis For most of its species, knowledge of ecology D. Possibly Related Taxa and phylogeography is still sparse. A particular 1. Bartheletia problem for the taxonomy of this group is the fact that teleomorphs and anamorphs have In molecular phylogenetic analyses Scheuer mostly been studied by different scientific com- et al. (2008) found that Bartheletia paradoxa, munities using different taxonomic methods. the only species of Bartheletia, is a member of Polymerase chain reaction–based advances in the Agaricomycotina, but they were unable to molecular biology have triggered an integration assign it to any particular subgroup of this of these two taxonomic approaches into a con- subphylum. B. paradoxa is a dimorphic fungus sistent classification system, yet a sound phylo- that rapidly develops on fallen Ginkgo biloba genetic classification is only just emerging. We leaves in its filamentous conidiogenous ana- expect that most of the open systematic ques- morphic state in autumn. Later, resting telios- tions will be solved in the near future by phy- pores are formed that germinate a year later logenomic analyses, when more genomes in the into longitudinally septate basidia. Since all Tremellomycetes will be available (as of writing other teliospore-generating taxa in the Agarico- this chapter, genome data are only available for mycotina belong to the Cystofilobasidiales, C. neoformans and T. mesenterica). We hope Scheuer et al. (2008) speculated about a possi- that, along with the progress in molecular tech- ble relationship of Bartheletia to the Tremello- niques and data, a rising number of mycolo- mycetes. However, unlike most members of the gists will be interested in and capable of Tremellomycetes, B. paradoxa lacks a yeast studying these fascinating fungi in the field, to stage. In addition, that fungus differs from all shed light on the biodiversity still unknown. other known members of the Agaricomycotina by the absence of dolipores. Instead, Barthele- tia has multiple plasmodesmalike perforations in its hyphal septa (Scheuer et al. 2008). References

Abe F, Minegishi H, Miura T, Nagahama T, Usami R, 2. Wallemia Horikoshi K (2006) Characterization of cold- and high-pressure-active polygalacturonases from a The hyphomycete genus Wallemia includes deep-sea yeast, Cryptococcus liquefaciens strain N6. Biosci Biotechnol Biochem 70:296–299 three described species that can tolerate osmotic M. Weiß et al.

Bandoni RJ (1984) The Tremellales and Auriculariales: Fell JW (2011) Mrakia Y. Yamada & Komagata (1987). an alternative classification. Trans Mycol Soc Jpn In: Kurtzman CP, Fell JW, Boekhout T (eds) The 25:489–530 yeasts: a taxonomic study. Elsevier, Amsterdam, Bandoni RJ, Boekhout T, Sampaio JP (2011) Holter- pp 1503–1510 mannia (Saccardo & Traverso 1910). In: Kurtzman Fell JW, Scorzetti G, Connell L, Craig S (2006) Biodiver- CP, Fell JW, Boekhout T (eds) The yeasts: a taxo- sity of micro-eukaryotes in Antarctic dry valley nomic study. Elsevier, Amsterdam, pp 1467–1470 soils with<5 % soil moisture. Soil Biol Biochem Bauer R (2004) Basidiomycetous interfungal cellular 38:3107–3119 interactions—a synopsis. In: Agerer R, Piepenbr- Fell JW, Johnson EA, Scorzetti G (2011) Xanthophyllo- ing M, Blanz P (eds) Frontiers in basidiomycote myces Golubev (1995). In: Kurtzman CP, Fell JW, mycology. IHW, Eching, pp 325–337 Boekhout T (eds) The yeasts: a taxonomic study. Bauer R, Oberwinkler F (1990a) Direct cytoplasm- Elsevier, Amsterdam, pp 1595–1599 cytoplasm connection: an unusual host-parasite Floudas D, Binder M, Riley R, Barry K, Blanchette RA, interaction of the tremelloid mycoparasite Tetra- Henrissat B, Martinez AT, Otillar R, Spatafora JW, goniomyces uliginosus. Protoplasma 154:157–160 Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Bauer R, Oberwinkler F (1990b) Haustoria of the myco- Copeland A, Coutinho PM, de Vries RP, Ferreira P, parasitic heterobasidiomycete Christiansenia pal- Findley K, Foster B, Gaskell J, Glotzer D, Gorecki lida. Cytologia 55:419–424 P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens Bauer R, Begerow D, Sampaio JP, Weiß M, Oberwinkler JA, Kallen N, Kersten P, Kohler A, Kues U, Kumar F (2006) The simple-septate basidiomycetes: a syn- TKA, Kuo A, LaButti K, Larrondo LF, Lindquist E, opsis. Mycol Prog 5:41–66 Ling A, Lombard V, Lucas S, Lundell T, Martin R, Berbee ML, Wells K (1988) Ultrastructural studies of McLaughlin DJ, Morgenstern I, Morin E, Murat C, mitosis and the septal pore apparatus in Tremella Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, globospora. Mycologia 80:479–492 Rokas A, Ruiz-Duenas FJ, Sabat G, Salamov A, Bergauer P, Fonteyne PA, Nolard N, Schinner F, Mar- Samejima M, Schmutz J, Slot JC, John FS, Stenlid gesin R (2005) Biodegradation of phenol and J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, phenol-related compounds by psychrophilic and Young D, Pisabarro A, Eastwood DC, Martin F, cold-tolerant alpine yeasts. Chemosphere 59:909– Cullen D, Grigoriev IV, Hibbett DS (2012) The 918 paleozoic origin of enzymatic lignin decomposi- Boekhout T (2011) Itersonilia Derx (1948). In: Kurtz- tion reconstructed from 31 fungal genomes. Sci- man CP, Fell JW, Boekhout T (eds) The yeasts: a ence 336:1715–1719 taxonomic study. Elsevier, Amsterdam, pp 1777– Fonseca A´ , Boekhout T, Fell JW (2011) Cryptococcus 1780 Vuillemin (1901). In: Kurtzman CP, Fell JW, Boekhout T, Fonseca A´ , Sampaio JP, Bandoni RJ, Fell Boekhout T (eds) The yeasts: a taxonomic study. JW, Kwon-Chung KJ (2011) Discussion of teleo- Elsevier, Amsterdam, pp 1661–1737 morphic and anamorphic basidiomycetous yeasts. Fries EM (1821) Systema mycologicum I. Lundae AU3 In: Kurtzman CP, Fell JW, Boekhout T (eds) The Gadanho M, Sampaio JP (2005) Occurrence and diver- yeasts: a taxonomic study. Elsevier, Amsterdam, sity of yeasts in the mid-atlantic ridge hydrother- pp 1339–1372 mal fields near the Azores Archipelago. Microb Brefeld O (1888) Basidiomyceten II. Protobasidiomyce- Ecol 50:408–417 ten, vol VII. Untersuchungen aus dem Gesammt- Ginns J (1986) The genus Syzygospora (Heterobasidio- gebiete der Mykologie. Arthur Felix, Leipzig mycetes: Syzygosporaceae). Mycologia 78:619–636 Chang ST, Wasser SP (2012) The role of culinary- Golubev WI, Golubev NW (2003) A new basidiomyce- medicinal mushrooms on human welfare with a tous yeast species, Cryptococcus mycelialis, related pyramid model for human health. Int J Med Mush- to Holtermannia Saccardo et Traverso. Microbiol- rooms 14:95–134 ogy (Moscow) 72:728–732 Chen C-J (1998) Morphological and molecular studies Hawksworth DL (2011) A new dawn for the naming of in the genus Tremella. Bibl Mycol 174:1–225 fungi: impacts of decisions made in Melbourne in David-Palma M, Libkind D, Sampaio JP (2014) Global July 2011 on the future publication and regulation distribution, diversity hot spots and niche transi- of fungal names. IMA Fungus 2:155–162 tions of an astaxanthin-producing eukaryotic Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon microbe. Mol Ecol 23:921–932 PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Desnos-Ollivier M, Patel S, Spaulding AR, Charlier C, Lu¨cking R, Lumbsch T, Lutzoni F, Matheny PB, Garcia-Hermoso D, Nielsen K, Dromer F (2010) McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Mixed infections and in vivo evolution in the Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, human fungal pathogen Cryptococcus neoformans. Aptroot A, Bauer R, Begerow D, Benny GL, Castle- mBio 1:e00091-10 bury LA, Crous PW, Dai Y-C, Gams W, Geiser DM, Diederich P (1996) The lichenicolous heterobasidiomy- Griffith GW, Gueidan C, Hawksworth DL, Hestmark cetes. Bibl Lichenol 61:1–198 G, Hosaka K, Humber RA, Hyde K, Ironside JE, Tremellomycetes and Related Groups

Ko˜ljalg U, Kurtzman CP, Larsson K-H, Lichtwardt (eds) The yeasts: a taxonomic study. Elsevier, R, Longcore J, Miadlikowska J, Miller A, Moncalvo Amsterdam, pp 1443–1455 J-M, Mozley-Standridge S, Oberwinkler F, Parmasto Lopandic K, Prillinger H, Wuczkowski M (2011) Fel- E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio lomyces Y. Yamada & Banno (1984). In: Kurtzman JP, Schu¨ssler A, Sugiyama J, Thorn RG, Tibell L, CP, Fell JW, Boekhout T (eds) The yeasts: a taxo- Untereiner W, Walker C, Wang Z, Weir A, Weiß nomic study. Elsevier, Amsterdam, pp 1759–1772 M, White MM, Winka K, Yao Y-J, Zhang N (2007) A Matheny PB, Gossmann JA, Zalar P, Arun Kumar TK, higher-level phylogenetic classification of the Fungi. Hibbett DS (2006) Resolving the phylogenetic posi- Mycol Res 111:509–547 tion of the Wallemiomycetes: an enigmatic major Hibbett DS, Bauer R, Binder M, Giachini AJ, Hosaka K, lineage of Basidiomycota. Can J Bot 84:1794–1805 Justo A, Larsson E, Larsson KH, Lawrey JD, Miet- McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter tinen O, Nagy L, Nilsson RH, Weiß M, Thorn RG W, Hawksworth DL, Herendeen PS, Knapp S, Mar- (2014) Agaricomycetes, chapter 14. In: McLaugh- hold K, Prado J, Prud’homme van Reine WF, lin DJ, Spatafora JW (eds) Systematics and evolu- Smith GF, Wiersema JH, Turland NJ (2012) Inter- tion. Springer, Heidelberg national code of nomenclature for algae, fungi, and James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter plants (Melbourne Code). Regnum Vegetabile, vol V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadli- 154. Koeltz Scientific Books kowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold Metin B, Findley K, Heitman J (2010) The mating type AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, locus (MAT) and sexual reproduction of Crypto- Johnson D, O’Rourke B, Crockett M, Binder M, coccus heveanensis: insights into the evolution of Curtis JM, Slot JC, Wang Z, Wilson AW, Schussler sex and sex-determining chromosomal regions in A, Longcore JE, O‘Donnell K, Mozley-Standridge Fungi. PLoS Genet 6:e1000961 S, Porter D, Letcher PM, Powell MJ, Taylor JW, Metzler B, Oberwinkler F, Petzold H (1989) Rhynchogas- White MM, Griffith GW, Davies DR, Humber RA, trema gen. nov. and Rhynchogastremaceae fam. Morton JB, Sugiyama J, Rossman AY, Rogers JD, nov. (Tremellales). Syst Appl Microbiol 12:280–287 Pfister DH, Hewitt D, Hansen K, Hambleton S, Millanes AM, Diederich P, Ekman S, Wedin M (2011) Shoemaker RA, Kohlmeyer J, Volkmann- Phylogeny and character evolution in the jelly Kohlmeyer B, Spotts RA, Serdani M, Crous PW, fungi (Tremellomycetes, Basidiomycota, Fungi). Hughes KW, Matsuura K, Langer E, Langer G, Mol Phylogenet Evol 61:12–28 Untereiner WA, Lucking R, Budel B, Geiser DM, Moore RT (1980) Taxonomic proposals for the classifi- Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr cation of marine yeasts and other yeast-like fungi R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spata- including the smuts. Bot Mar 23:361–374 fora JW, Vilgalys R (2006) Reconstructing the Moore RT (1986) A note on Wallemia sebi. Antonie early evolution of Fungi using a six-gene phylog- Van Leeuwenhoek 52:183–187 eny. Nature 443:818–822 Moore RT (1987) Additions to the genus Vanrija. Bibl Johnson EA, Schroeder W (1995) Astaxanthin from the Mycol 108:167–173 yeast Phaffia rhodozyma. Stud Mycol 38:81–90 O’Gorman CM, Fuller HT, Dyer PS (2009) Discovery of Katoh K, Standley DM (2013) MAFFT multiple a sexual cycle in the opportunistic fungal pathogen sequence alignment software Version 7: improve- Aspergillus fumigatus. Nature 457:471–474 ments in performance and usability. Mol Biol Evol Oberwinkler F (2014) Dacrymycetes, chapter 13. In: 30:772–780 McLaughlin DJ, Spatafora JW (eds) Systematics Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) and evolution. Springer, Heidelberg Dictionary of the Fungi, 10th edn. CAB Interna- Oberwinkler F, Bandoni RJ (1981) Tetragoniomyces tional, Wallingford gen. nov. and Tetragoniomycetaceae fam. nov. Kirschner R, Sampaio JP, Gadanho M, Weiß M, Ober- (Tremellales). Can J Bot 59:1034–1040 winkler F (2001) Cuniculitrema polymorpha Oberwinkler F, Bandoni R (1982) Carcinomycetaceae: a (Tremellales, gen. nov. and sp. nov.), a heteroba- new family in the Heterobasidiomycetes. Nord J sidiomycete vectored by bark beetles, which is the Bot 2:501–516 teleomorph of Sterigmatosporidium polymor- Oberwinkler F, Bandoni RJ (1983) Trimorphomyces:a phum. Antonie Van Leeuwenhoek 80:149–161 new genus in the Tremellaceae. Syst Appl Micro- Kumar S, Skjaeveland A, Orr RJS, Enger P, Ruden T, biol 4:105–113 Mevik BH, Burki F, Botnen A, Shalchian-Tabrizi K Oberwinkler F, Lowy B (1981) Syzygospora alba,a (2009) AIR: a batch-oriented web program package mycoparasitic heterobasidiomycete. Mycologia for construction of supermatrices ready for phylo- 73:1108–1115 genomic analyses. BMC Bioinformatics 10:357 Oberwinkler F, Bandoni R, Blanz P, Kisimova-Horovitz Kurtzman CP, Fell JW, Boekhout T (eds) (2011) The L (1983) Cystofilobasidium: a new genus in the yeasts: a taxonomic study. Elsevier, Amsterdam Filobasidiaceae. Syst Appl Microbiol 4:114–122 Kwon-Chung KJ (2011) Filobasidiella Kwon-Chung Oberwinkler F, Bandoni RJ, Bauer R, Deml G, (1975). In: Kurtzman CP, Fell JW, Boekhout T Kisimova-Horovitz L (1984) The life-history of M. Weiß et al.

Christiansenia pallida, a dimorphic, mycoparasitic Sugita T (2011) Trichosporon Behrend 1890. In: Kurtzman heterobasidiomycete. Mycologia 76:9–22 CP, Fell JW, Boekhout T (eds) The yeasts: a taxo- Oberwinkler F, Bauer R, Schneller J (1990) Phragmox- nomic study. Elsevier, Amsterdam, pp 2015–2061 enidium mycophilum sp. nov., an unusual myco- Swann EC, Taylor JW (1995) Phylogenetic perspectives parasitic heterobasidiomycete. Syst Appl on basidiomycete systematics: evidence from the Microbiol 13:186–191 18S rRNA gene. Can J Bot 73:S862–S868 Padamsee M, Kumar TKA, Riley R, Binder M, Boyd A, Takashima M, Sugita T, Shinoda T, Nakase T (2001) Calvo AM, Furukawa K, Hesse C, Hohmann S, Reclassification of the Cryptococcus humicola James TY, LaButti K, Lapidus A, Lindquist E, complex. Int J Syst Evol Microbiol 51:2199–2210 Lucas S, Miller K, Shantappa S, Grigoriev IV, Hib- Takishita K, Tsuchiya M, Reimer JD, Maruyama T bett DS, McLaughlin DJ, Spatafora JW, Aime MC (2006) Molecular evidence demonstrating the (2012) The genome of the xerotolerant mold Wal- basidiomycetous fungus Cryptococcus curvatus is lemia sebi reveals adaptations to osmotic stress the dominant microbial eukaryote in sediment at and suggests cryptic sexual reproduction. Fungal the Kuroshima Knoll methane seep. Extremo- Genet Biol 49:217–226 philes 10:165–169 Park BJ, Wannemuehler KA, Marston BJ, Govender N, Tulasne LR (1853) Observations sur l’organisation des Pappas PG, Chiller TA (2009) Estimation of the Tre´melline´es. Ann Sci Nat Bot 19:193–231 current global burden of cryptococcal meningitis Weiß M, Oberwinkler F (2001) Phylogenetic relation- among persons living with HIV/AIDS. AIDS ships in Auriculariales and related groups— 23:525–530 hypotheses derived from nuclear ribosomal DNA Patouillard N (1887) Les Hyme´nomyce`tes d’Europe. sequences. Mycol Res 105:403–415 Paris Weiß M, Bauer R, Begerow D (2004) Spotlights on Perfect JR (2005) Cryptococcus neoformans: a sugar- heterobasidiomycetes. In: Agerer R, Piepenbring coated killer with designer genes. FEMS Immunol M, Blanz P (eds) Frontiers in basidiomycote Med Microbiol 45:395–404 mycology. IHW, Eching, pp 7–48 Persoon CH (1794) Dispositio methodica fungorum. Wells K (1994) Jelly fungi, then and now! Mycologia Neues Magazin fu¨r die Botanik 1:81–128 86:18–48 Prillinger H, Lopandic K, Sugita T, Wuczkowski M Wells K, Bandoni R (2001) Heterobasidiomycetes. In: (2007) Asterotremella gen. nov albida, an anamor- McLaughlin DJ, McLaughlin EG, Lemke PA (eds) phic tremelloid yeast isolated from the agarics The mycota, Vol. VII, Part B: systematics and Asterophora lycoperdoides and Asterophora para- evolution. Springer, Berlin, pp 85–120 sitica. J Gen Appl Microbiol 53:167–175 Wuczkowski M, Passoth V, Turchetti B, Andersson AC, Ramı´rez Go´mez C (1957) Contribucio´n al estudio de la Olstorpe M, Laitila A, Theelen B, van Broock M, ecologı´a de las levaduras. I. Estudio de levaduras Buzzini P, Prillinger H, Sterflinger K, Schnurer J, aisladas de hongos carnosos. Microbiol Esp Boekhout T, Libkind D (2011) Description of Hol- 10:215–247 termanniella gen. nov., including Holtermanniella Sampaio JP (2004) Diversity, phylogeny and classifica- takashimae sp. nov. and four new combinations, tion of basidiomycetous yeasts. In: Agerer R, Pie- and proposal of the order Holtermanniales to penbring M, Blanz P (eds) Frontiers in accommodate tremellomycetous yeasts of the Hol- basidiomycote mycology. IHW, Eching, pp 49–80 termannia clade. Int J Syst Evol Microbiol 61:680– Sampaio JP, Weiß M, Gadanho M, Bauer R (2002) New 689 taxa in the Tremellales: Bulleribasidium oberjo- Zajc J, Liu Y, Dai W, Yang Z, Hu J, Constincˇar C, chense gen. et sp. nov., Papiliotrema bandonii Gunde-Cimerman N (2013) Genome and tran- gen. et sp. nov. and Fibulobasidium murrhard- scriptome sequencing of the halophilic fungus tense sp. nov. Mycologia 94:873–887 Wallemia ichthyophaga: haloadaptations present Scheuer C, Bauer R, Lutz M, Stabentheiner E, Mel’nikd and absent. BMC Genomics 14:617 VA, Grube M (2008) Bartheletia paradoxa is a Zalar P, de Hoog GS, Schroers H-J, Frank JM, Gunde- living fossil on Ginkgo leaf litter with a unique Cimerman N (2005) Taxonomy and phylogeny of septal structure in the Basidiomycota. Mycol Res the xerophilic genus Wallemia (Wallemiomycetes 112:1265–1279 and Wallemiales, cl. et ord. nov.). Antonie Van Scorzetti G, Fell JW, Fonseca A, Statzell-Tallman A Leeuwenhoek 87:311–328 (2002) Systematics of basidiomycetous yeasts: a Zugmaier W, Oberwinkler F (1995) Tremelloid hausto- comparison of large subunit D1/D2 and internal rial cells with haustorial filaments and potential transcribed spacer rDNA regions. FEMS Yeast Res host-range of Tremella mesenterica. Nord J Bot 2:495–517 15:207–213 Stamatakis A, Hoover P, Rougemont J (2008) A rapid Zugmaier W, Bauer R, Oberwinkler F (1994) Mycopar- bootstrap algorithm for the RAxML web servers. asitism of some Tremella species. Mycologia Syst Biol 57:758–771 86:49–56 Author Queries

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AU1 “Sampaio et al. 2001” is cited in text but not given in the reference list. Please provide details in the list or delete the citation from the text. AU2 In "maintained in pure culture in standard media," changed "on" to "in" before "standard." This change (from "on" to "in" before "medium/ media") will be made globally. Please confirm. AU3 Please provide complete details for the reference "Fries 1821".