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Towards an integrated phylogenetic classification of the Tremellomycetes

Authors:
  • Institute of Microbiology, Chinese Academy of Sciences

Abstract and Figures

Families and genera assigned to Tremellomycetes have been mainly circumscribed by morphology and for the yeasts also by biochemical and physiological characteristics. This phenotype-based classification is largely in conflict with molecular phylogenetic analyses. Here a phylogenetic classification framework for the Tremellomycetes is proposed based on the results of phylogenetic analyses from a seven-genes dataset covering the majority of tremellomycetous yeasts and closely related filamentous taxa. Circumscriptions of the taxonomic units at the order, family and genus levels recognised were quantitatively assessed using the phylogenetic rank boundary optimisation (PRBO) and modified general mixed Yule coalescent (GMYC) tests. In addition, a comprehensive phylogenetic analysis on an expanded LSU rRNA (D1/D2 domains) gene sequence dataset covering as many as available teleomorphic and filamentous taxa within Tremellomycetes was performed to investigate the relationships between yeasts and filamentous taxa and to examine the stability of undersampled clades. Based on the results inferred from molecular data and morphological and physiochemical features, we propose an updated classification for the Tremellomycetes. We accept five orders, 17 families and 54 genera, including seven new families and 18 new genera. In addition, seven families and 17 genera are emended and one new species name and 185 new combinations are proposed. We propose to use the term pro tempore or pro tem. in abbreviation to indicate the species names that are temporarily maintained.
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Towards an integrated phylogenetic classication of the
Tremellomycetes
X.-Z. Liu
1
,
2
, Q.-M. Wang
1
,
2
, M. Göker
3
, M. Groenewald
2
, A.V. Kachalkin
4
, H.T. Lumbsch
5
, A.M. Millanes
6
, M. Wedin
7
, A.M. Yurkov
3
,
T. Boekhout
1
,
2
,
8*
, and F.-Y. Bai
1
,
2*
1
State Key Laboratory for Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, PR China;
2
CBS Fungal Biodiversity Centre (CBS-KNAW),
Uppsalalaan 8, Utrecht, The Netherlands;
3
Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig 38124, Germany;
4
Faculty of
Soil Science, Lomonosov Moscow State University, Moscow 119991, Russia;
5
Science & Education, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL 60605,
USA;
6
Departamento de Biología y Geología, Física y Química Inorg
anica, Universidad Rey Juan Carlos, E-28933 M
ostoles, Spain;
7
Department of Botany, Swedish
Museum of Natural History, P.O. Box 50007, SE-10405 Stockholm, Sweden;
8
Shanghai Key Laboratory of Molecular Medical Mycology, Changzheng Hospital, Second
Military Medical University, Shanghai, PR China
*Correspondence: F.-Y. Bai,
baify@im.ac.cn; T. Boekhout, t.boekhout@cbs.knaw.nl
Abstract: Families and genera assigned to Tremellomycetes have been mainly circumscribed by morphology and for the yeasts also by biochemical and physiological
characteristics. This phenotype-based classication is largely in conict with molecular phylogenetic analyses. Here a phylogenetic classication framework for the
Tremellomycetes is proposed based on the results of phylogenetic analyses from a seven-genes dataset covering the majority of tremellomycetous yeasts and closely
related lamentous taxa. Circumscriptions of the taxonomic units at the order, family and genus levels recognised were quantitatively assessed using the phylogenetic
rank boundary optimisation (PRBO) and modied general mixed Yule coalescent (GMYC) tests. In addition, a comprehensive phylogenetic analysis on an expanded LSU
rRNA (D1/D2 domains) gene sequence dataset covering as many as available teleomorphic and lamentous taxa within Tremellomycetes was performed to investigate
the relationships between yeasts and lamentous taxa and to examine the stability of undersampled clades. Based on the results inferred from molecular data and
morphological and physiochemical features, we propose an updated classication for the Tremellomycetes. We accept ve orders, 17 families and 54 genera, including
seven new families and 18 new genera. In addition, seven families and 17 genera are emended and one new species name and 185 new combinations are proposed.
We propose to use the term pro tempore or pro tem. in abbreviation to indicate the species names that are temporarily maintained.
Key words: Jelly fungi, Morphology, Multigene phylogeny, Ranks, Taxonomy, Tremellomycetes, Yeasts.
Taxonomic novelties: New families: Bulleraceae X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Bulleribasidiaceae X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout,
Mrakiaceae X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Naemateliaceae X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Phaeotremellaceae A.M. Yurkov &
Boekhout, Piskurozymaceae X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Trimorphomycetaceae X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout; New genera:
Bandonia A.M. Yurkov, X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Carlosrosaea A.M. Yurkov, X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout,
Cutaneotrichosporon X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Dimennazyma X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Effuseotrichosporon A.M. Yurkov,
X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Fonsecazyma X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Gelidatrema A.M. Yurkov, X.Z. Liu, F.Y. Bai, M. Groenew.
& Boekhout, Genolevuria X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Goffeauzyma X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Haglerozyma X.Z. Liu, F.Y. Bai,
M. Groenew. & Boekhout, Krasilnikovozyma X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Nielozyma X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Piskurozyma
X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Pseudotremella X.Z. Liu, F.Y. Bai, A.M. Yurkov, M. Groenew. & Boekhout, Saitozyma X.Z. Liu, F.Y. Bai, M. Groenew.
& Boekhout, Sugitazyma A.M. Yurkov, X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Solicoccozyma X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Vishniacozyma
X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout; New species: Kockovaella prillingeri (Prillinger, G. Kraep. & Lopandic) X.Z. Liu, F.Y. Bai, M. Groenew. &
Boekhout; New combinations: Apiotrichum brassicae (Nakase) A.M. Yurkov & Boekhout, A. cacaoliposimilis (J.L. Zhou, S.O. Suh & Gujjari) Kachalkin, A.M.
Yurkov & Boekhout, A. dehoogii (Middelhoven, Scorzetti & Fell) A.M. Yurkov & Boekhout, A. domesticum (Sugita, A. Nishikawa & Shinoda) A.M. Yurkov &
Boekhout, A. dulcitum (Berkhout) A.M. Yurkov & Boekhout, A. gamsii (Middelhoven, Scorzetti, Sigler & Fell) A.M. Yurkov & Boekhout, A. gracile (Weigmann & A.
Wolff) A.M. Yurkov & Boekhout, A. laibachii (Windisch) A.M. Yurkov & Boekhout, A. lignicola (Diddens) A.M. Yurkov & Boekhout, A. loubieri (Morenz) A.M. Yurkov
& Boekhout, A. montevideense (L.A. Queiroz) A.M. Yurkov & Boekhout, A. mycotoxinivorans (O. Moln
ar, Schatzm. & Prillinger) A.M. Yurkov & Boekhout,
A. scarabaeorum (Middelhoven, Scorzetti & Fell) A.M. Yurkov & Boekhout, A. siamense (Nakase, Jindam., Sugita & H. Kawas.) Kachalkin, A.M. Yurkov &
Boekhout, A. sporotrichoides (van Oorschot) A.M. Yurkov & Boekhout, A. vadense (Middelhoven, Scorzetti & Fell) A.M. Yurkov & Boekhout, A. veenhuisii
(Middelhoven, Scorzetti & Fell) A.M. Yurkov & Boekhout, A. wieringae (Middelhoven) A.M. Yurkov & Boekhout, A. xylopini (S.O. Suh, Lee, Gujjari & Zhou)
Kachalkin, A.M. Yurkov & Boekhout, Bandonia marina (van Uden & Zobell) A.M. Yurkov, X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Bulleribasidium begoniae
(Nakase, Tsuzuki, F.L. Lee & M. Takash.) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Bu. foliicola (Q.M. Wang, F.Y. Bai, Boekhout & Nakase) X.Z. Liu, F.Y. Bai,
M. Groenew. & Boekhout, Bu. hainanense (Q.M. Wang, F.Y. Bai, Boekhout & Nakase) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Bu. panici (Fungsin, M. Takash.
& Nakase) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Bu. pseudovariabile (F.Y. Bai, M. Takash. & Nakase) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Bu.
sanyaense (Q.M. Wang, F.Y. Bai, Boekhout & Nakase) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Bu. setariae (Nakase, Tsuzuki, F.L. Lee & M. Takash.) X.Z.
Liu, F.Y. Bai, M. Groenew. & Boekhout, Bu. siamense (Fungsin, M. Takash. & Nakase) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Bu. variabile (Nakase & M.
Suzuki) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Bu. wuzhishanense (Q.M. Wang, F.Y. Bai, Boekhout & Nakase) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout,
Carcinomyces arundinariae (Fungsin, M. Takash. & Nakase) A.M. Yurkov, Carc. polyporina (D.A. Reid) A.M. Yurkov, Carlosrosaea vrieseae (Landell, Brand~
ao,
Safar, Gomes, F
elix, Santos, Pagani, Ramos, Broetto, Mott, Valente & Rosa) A.M. Yurkov, X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Cryptococcus
depauperatus (Petch) Boekhout, Liu, Bai & M. Groenew., Cr. luteus (Roberts) Boekhout, Liu, Bai & M. Groenew., Cutaneotrichosporon arboriformis (Sugita, M.
Takash., Sano, Nishim., Kinebuchi, S. Yamag. & Osanai) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Cu. curvatus (Diddens & Lodder) A.M. Yurkov, X.Z. Liu, F.Y.
Bai, M. Groenew. & Boekhout, Cu. cutaneum (de Beurmann, Gougerot & Vaucher) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Cu. cyanovorans (Motaung,
Albertyn, J.L.F. Kock et Pohl) A.M. Yurkov, X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Cu. daszewskae (Takash., Sugita, Shinoda & Nakase) A.M. Yurkov, X.Z.
Liu, F.Y. Bai, M. Groenew. & Boekhout, Cu. debeurmannianum (Sugita, Takash., Nakase & Shinoda) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Cu. dermatis
(Sugita, Takash., Nakase, Ichikawa, Ikeda & Shinoda) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Cu. guehoae (Middelhoven, Scorzettii & Fell) A.M. Yurkov, X.Z.
Liu, F.Y. Bai, M. Groenew. & Boekhout, Cu. haglerorum (Middelhoven,
A. Fonseca, S.C. Carreiro, Pagnocca & O.C. Bueno) X.Z. Liu, F.Y. Bai, M. Groenew. &
Peer review under responsibility of CBS-KNAW Fungal Biodiversity Centre.
Copyright © 2016, CBS-KNAW Fungal Biodiversity Centre. Production and hosting by ELSEVIER B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/
licenses/by-nc-nd/4.0/).
available online at www.studiesinmycology.org STUDIES IN MYCOLOGY 81: 85147.
Studies in Mycology
85
Boekhout, Cu. jirovecii (Fr
agner) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Cu. moniliiforme (Weigmann & A. Wolff) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Cu.
mucoides (E. Gu
eho & M.T. Smith) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Cu. oleaginosus (J.J. Zhou, S.O. Suh & Gujjari) X.Z. Liu, F.Y. Bai, M. Groenew. &
Boekhout, Cu. smithiae (Middelhoven, Scorzetti, Sugita & Fell) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Cu. terricola (Sugita, M. Takash. & Nakase) X.Z. Liu,
F.Y. Bai, M. Groenew. & Boekhout, Dimennazyma cistialbidi (
A. Fonseca, J. In
acio & Spenc.-Mart.) A.M. Yurkov, X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout,
Effuseotrichosporon vanderwaltii (Motaung, Albertyn, Kock, C.F. Lee, S.O. Suh, M. Blackwell & C.H. Pohl) A.M. Yurkov, X.Z. Liu, F.Y. Bai, M. Groenew. &
Boekhout, Filobasidium chernovii (
A. Fonseca, Scorzetti & Fell) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Fil. magnum (Lodder & Kreger-van Rij) X.Z. Liu, F.Y.
Bai, M. Groenew. & Boekhout, Fil. oeirense (
A. Fonseca, Scorzetti & Fell) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Fil. stepposum (Golubev & J.P. Samp.) X.Z.
Liu, F.Y. Bai, M. Groenew. & Boekhout, Fil. wieringae (
A. Fonseca, Scorzetti & Fell) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Fonsecazyma betulae (K.
Sylvester, Q.M. Wang, C. T. Hittinger) A.M. Yurkov, A.V. Kachalkin & Boekhout, Fon. mujuensis (K.S. Shin & Y.H. Park) X.Z. Liu, F.Y. Bai, M. Groenew. &
Boekhout, Fon. tronadorensis (V. De Garcia, Zalar, Brizzio, Gunde-Cim. & van Brook) A.M. Yurkov, Gelidatrema spencermartinsiae (Garcia, Brizzio, Boekhout,
Theelen, Libkind & van Broock) A.M. Yurkov, X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Genolevuria amylolytica (
A. Fonseca, J. In
acio & Spenc.-Mart.) X.Z.
Liu, F.Y. Bai, M. Groenew. & Boekhout, Gen. armeniaca (
A. Fonseca & J. In
acio) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Gen. bromeliarum (Landell & P.
Valente) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Gen. tibetensis (F.Y. Bai & Q.M. Wang) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Goffeauzyma
aciditolerans (Gadanho & J.P. Samp.) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Gof. agrionensis (Russo, Libkind, Samp. & van Broock) X.Z. Liu, F.Y. Bai, M.
Groenew. & Boekhout, Gof. gastrica (Reiersöl & di Menna) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Gof. gilvescens (Chernov & Babeva) X.Z. Liu, F.Y. Bai, M.
Groenew. & Boekhout, Gof. iberica (Gadanho & J.P. Samp.) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Gof. metallitolerans (Gadanho & J.P. Samp.) X.Z. Liu, F.Y.
Bai, M. Groenew. & Boekhout, Haglerozyma chiarellii (Pagnocca, Legaspe, Rodrigues & Ruivo) A. M. Yurkov, X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout,
Heterocephalacria arrabidensis (
A. Fonseca, Scorzetti & Fell) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Het. bachmannii (Diederich & M.S. Christ.) Millanes &
Wedin, Het. physciacearum (Diederich) Millanes & Wedin, Itersonilia pannonica (Niwata, Takash., Tornai-Lehoczki, T. De
ak & Nakase) X.Z. Liu, F.Y. Bai, M.
Groenew. & Boekhout, Kockovaella chinensis (Prillinger, G. Kraep. & Lopandic) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Ko. distylii (Hamam., Kuroy. &
Nakase) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Ko. fuzhouensis (J.Z. Yue) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Ko. lichenicola (Prillinger, G. Kraep.
& Lopandic) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Ko. mexicana (Lopandic, O. Moln
ar & Prillinger) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Ko.
ogasawarensis (Hamam., Kuroy. & Nakase) X.Z. Liu, F.Y. Bai, Groenew. & Boekhout, Ko. sichuanensis (Prillinger, G. Kraep. & Lopandic) X.Z. Liu, F.Y. Bai, M.
Groenew. & Boekhout, Krasilnikovozyma huempii (C. Ramírez & A. E. Gonz
alez) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Kr. tahquamenonensis (Wang,
Hulfachor, Sylvester and Hittinger) A.M. Yurkov, Kwoniella bestiolae (Thanh, Hai & Lachance) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Kw. dejecticola (Thanh,
Hai & Lachance) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Kw. dendrophila (Van der Walt & D.B. Scott) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Kw. pini
(Golubev & Pfeiffer) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Kw. shivajii (S.R. Ravella, S.A. James, C.J. Bond, I.N. Roberts, K. Cross, Retter & P.J. Hobbs)
X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Mrakia aquatica (E.B.G. Jones & Slooff) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, M. cryoconiti (Margesin & Fell)
X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, M. niccombsii (Thomas-Hall) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Naematelia aurantialba (Bandoni & M.
Zang) Millanes & Wedin, Naem. microspora (Lloyd) Millanes & Wedin, Naganishia adeliensis (Scorzetti, I. Petrescu, Yarrow & Fell) X.Z. Liu, F.Y. Bai, M. Groenew.
& Boekhout, Nag. albida (Saito) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Nag. albidosimilis (Vishniac & Kurtzman) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout,
Nag. antarctica (Vishniac & Kurtzman) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Nag. bhutanensis (Goto & Sugiy.) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout,
Nag. cerealis (Passoth, A.-C. Andersson, Olstorpe, Theelen, Boekhout & Schnürer) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Nag. difuens (Zach) X.Z. Liu, F.Y.
Bai, M. Groenew. & Boekhout, Nag. friedmannii (Vishniac) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Nag. liquefaciens (Saito & M. Ota) X.Z. Liu, F.Y. Bai, M.
Groenew. & Boekhout, Nag. onofrii (Turchetti, Selbmann & Zucconi) A.M. Yurkov, Nag. randhawae (Z.U. Khan, S.O. Suh. Ahmad, F. Hagen, Fell, Kowshik, Chandy
& Boekhout) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Nag. uzbekistanensis (
A. Fonseca, Scorzetti & Fell) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Nag.
vaughanmartiniae (Turchetti, Blanchette & Arenz) A.M. Yurkov, Nag. vishniacii (Vishniac & Hemping) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Nielozyma
formosana (Nakase, Tsuzuki, F.L. Lee & M. Takash.) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Niel. melastomae (Nakase, Tsuzuki, F.L. Lee & M. Takash.) X.Z.
Liu, F.Y. Bai, M. Groenew. & Boekhout, Papiliotrema anemochoreius (C.H. Pohl, Kock, P.W.J. van Wyk & Albertyn) F.Y. Bai, M. Groenew. & Boekhout, Pap.
aspenensis (K. Ferreira-Paim, T.B. Ferreira, L. Andrade-Silva, D.J. Mora, D.J. Springer, J. Heitman, F.M. Fonseca, D. Matos, M.S.C. Melhem & M.L. Silva-Vergara)
X.Z. Liu, F.Y. Bai, A.M. Yurkov & Boekhout, Pap. aurea (Saito) M. Takash., Sugita, Shinoda & Nakase) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Pap. baii (A.M.
Yurkov, M.A. Guerreiro &
A. Fonseca) A.M. Yurkov, Pap. avescens (Saito) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Pap. fonsecae (V. de García, Zalar,
Braizzio, Gunde-Cim. & van Brollck) A.M. Yurkov, Pap. frias (V. de García, Zalar, Braizzio, Gunde-Cim. & van Brollck) A.M. Yurkov, Pap. fuscus (J.P. Samp., J.
In
acio, Fonseca & Fell) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Pap. hoabinhensis (D.T. Luong, M. Takash., Ty. Dung & Nakase) A.M. Yurkov, Pap. japonica
(J.P. Samp., Fonseca & Fell) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Pap. laurentii (Kuff.) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Pap. mangalensis (Fell,
Statzell & Scorzett) A.M. Yurkov, Pap. nemorosus (Golubev, Gadanho, J.P. Samp. & N.W. Golubev) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Pap. perniciosus
(Golubev, Gadanho, J.P. Samp. & N.W. Golubev) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Pap. pseudoalba (Nakase & M. Suzuki) X.Z. Liu, F.Y. Bai, M.
Groenew. & Boekhout, Pap. rajasthanensis (Saluja & G.S. Prasad) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Pap. ruineniae (A.M. Yurkov, M.A. Guerreiro &
A.
Fonseca) A.M. Yurkov, Pap. taeanensis (K.S. Shin & Y.H. Park) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Pap. terrestris (Crestani, Landell, Faganello, Vainstein,
Vishniac & P. Valente) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Pap. wisconsinensis (Crestani, Landell, Faganello, Vainstein, Vishniac & P. Valente) X.Z. Liu,
F.Y. Bai, M. Groenew. & Boekhout, Phaeotremella fagi (Middelhoven & Scorzetti) A.M. Yurkov & Boekhout, Ph. mycetophiloides (Kobayasi) Millanes & Wedin,
P. mycophaga (G.W. Martin) Millanes & Wedin, Ph. neofoliacea (Chee J. Chen) Millanes & Wedin, Ph. simplex (H.S. Jacks. & G.W. Martin) Millanes & Wedin, Ph.
skinneri (Phaff & Carmo Souza) A.M. Yurkov & Boekhout, Pseudotremella allantoinivorans (Middelhoven) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Ps.
lacticolor (Satoh & Makimura) A.M. Yurkov, Ps. moriformis (Berk.) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Ps. nivalis (Chee J. Chen) X.Z. Liu, F.Y. Bai, M.
Groenew. & Boekhout, Piskurozyma capsuligena (Fell, Statzell, I.L. Hunter & Phaff) A.M. Yurkov, Pis. cylindrica (
A. Fonseca, Scorzetti & Fell) X.Z. Liu, F.Y. Bai,
M. Groenew. & Boekhout, Pis. ldesensis (T. Zhang & L.-Y. Yu) A.M. Yurkov, Pis. licatus (Golubev & J.P. Samp.) Kachalkin, Pis. silvicola (Golubev & J.P. Samp.)
X.Z. Liu, F.Y. Bai, Groenew. & Boekhout, Pis. sorana (Hauerslev) A.M. Yurkov, Pis. taiwanensis (Nakase, Tsuzuki & M. Takash.) X.Z. Liu, F.Y. Bai, M. Groenew. &
Boekhout, Rhynchogastrema aquatica (Brandao, Valente, Pimenta & Rosa) X.Z. Liu, F.Y. Bai, M. Groenew., Boekhout & A.M. Yurkov, R. complexa (Landell,
Pagnocca, Sette, Passarini, Garcia, Ribeiro, Lee, Brandao, Rosa & Valente) X.Z. Liu, F.Y. Bai, M. Groenew., Boekhout & A.M. Yurkov, R. fermentans (Lee) X.Z.
Liu, F.Y. Bai, M. Groenew., Boekhout & A.M. Yurkov, R. glucofermentans (S.O. Suh & Blackwell) X.Z. Liu, F.Y. Bai, M. Groenew., Boekhout & A.M. Yurkov,
R. nanyangensis (F.L. Hui & Q.H. Niu) X.Z. Liu, F.Y. Bai, M. Groenew., Boekhout & A.M. Yurkov, R. noutii (Boekhout, Fell, Scorzett & Theelen) X.Z. Liu, F.Y. Bai,
M. Groenew., Boekhout & A.M. Yurkov, R. tunnelae (Boekhout, Fell, Scorzetti & Theelen) X.Z. Liu, F.Y. Bai, M. Groenew., Boekhout & A.M. Yurkov,
R. visegradensis (Peter & Dlauchy) X.Z. Liu, F.Y. Bai, M. Groenew., Boekhout & A.M. Yurkov, Saitozyma ava (Saito) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout,
Sait. ninhbinhensis (Luong, Takash., Dung & Nakase) A.M. Yurkov, Sait. paraava (Golubev & J.P. Samp.) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Sait.
podzolica (Babeva & Reshetova) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Solicoccozyma aeria (Saito) A.M. Yurkov, Sol. fuscescens (Golubev) A.M. Yurkov,
Sol. keelungensis (C.F. Chang & S.M. Liu) A.M. Yurkov, Sol. phenolicus (
A. Fonseca, Scorzetti & Fell) A.M. Yurkov, Sol. terreus (Di Menna) A.M. Yurkov, Sol.
terricola (T.A. Pedersen) A.M. Yurkov, Sugitazyma miyagiana (Nakase, Itoh, Takem. & Bandoni) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Tausonia pullulans
(Lindner) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Tremella yokohamensis (Alshahni, Satoh & Makimura) A.M. Yurkov, Trimorphomyces sakaeraticus
(Fungsin, M. Takash. & Nakase) X.Z. Liu, F.Y. Bai, M. Groenew., Boekhout & A.M. Yurkov, Vanrija fragicola (M. Takash., Sugita, Shinoda & Nakase) X.Z. Liu, F.Y.
Bai, M. Groenew. & Boekhout, Van. meifongana (C.F. Lee) Kachalkin, A.M. Yurkov & Boekhout, Van. nantouana (C.F. Lee) Kachalkin, A.M. Yurkov & Boekhout,
Van. thermophila (Vogelmann, Chaves & Hertel) Kachalkin, A.M. Yurkov & Boekhout, Vishniacozyma carnescens (Verona & Luchetti) X.Z. Liu, F.Y. Bai, M.
Groenew. & Boekhout, Vis. dimennae (Fell & Phaff) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Vis. foliicola (Q.M. Wang & F.Y. Bai) A.M. Yurkov, Vis. globispora
(B.N. Johri & Bandoni) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Vis. heimaeyensis (Vishniac) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Vis. nebularis
LIU ET AL.
86
(Vishniac) A.M. Yurkov, Vis. peneaus (Phaff, Mrak & O.B. Williams) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Vis. psychrotolerans (V. de García, Zalar, Brizzio, Gunde-
Cim. & van Broock) A.M. Yurkov, Vis. taibaiensis (Q.M. Wang & F.Y. Bai) A.M. Yurkov, Vis. tephrensis (Vishniac) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout, Vis.
victoriae (M.J. Montes, Belloch, Galiana, M.D. García, C. Andr
es, S. Ferrer, Torr.-Rodr. & J. Guinea) X.Z. Liu, F.Y. Bai, M. Groenew. & Boekhout.
Available online xxx; http://dx.doi.org/10.1016/j.simyco.2015.12.001. Hard copy: xxx.
INTRODUCTION
Tremellomycetes is a class of Agaricomycotina (Hibbett et al.
2007, Boekhout et al. 2011a) and encompasses yeasts, dimor-
phic taxa and species that form hyphae and/or complex fruiting
bodies. Five orders, namely Cystolobasidiales,Filobasidiales,
Holtermanniales,Tremellales and Trichosporonales, are
currently recognised in Tremellomycetes based on phenotypic
and phylogenetic properties (Fell et al. 2000, Scorzetti et al.
2002, Boekhout et al. 2011a, Wuczkowski et al. 2011, Weiss
et al. 2014, Liu et al. 2015). However, the separation of Tri-
chosporonales from Tremellales remains a matter of debate
(Hibbett et al. 2007, Millanes et al. 2011).
Basidiomycetous yeasts, like ascomycetous yeasts, were
conventionally classied based on morphological features,
including sexual and asexual reproductive structures and
morphology; chemotaxonomic criteria, including cell-wall
composition data and ubiquinone types; and physiological
properties characterised by standardised tests on the assimila-
tion and fermentation of carbon and nitrogen compounds, pro-
duction of starch-like compounds, and other growth tests (Lodder
& Kreger-van Rij 1952, Van der Walt 1970, Van der Walt &
Yarrow 1984, Boekhout et al. 1993, 2011a, Kurtzman et al.
2011b, Prillinger et al. 1993, McLaughlin et al. 1995, Sampaio &
Fonseca 1995, Nguyen et al. 1998, Yarrow 1998, Takashima
et al. 2000, Bauer et al. 2006, Celio et al. 2006). Basidiocarp-
forming Tremellomycetes were mainly classied using morpho-
logical features, such as form and consistency of the fruiting
bodies, and details of hyphae, basidia, basidiospores etc. The
classication based on these phenotypical features, however,
was in many cases not consistent with the results obtained from
molecular phylogenetic analyses. This non-concordance is one
of the most prominent problems in the classication of this group
of fungi, as illustrated by the polyphyletic nature of many
currently recognised genera. Bullera and Cryptococcus are just
two examples of genera that are highly polyphyletic with species
belonging to more than one order of Tremellomycetes (Boekhout
et al. 2011b, Fonseca et al. 2011). Further discovery of new
species belonging to these genera not only worsened the
problem of systematics of Tremellomycetes, but also impeded
the communication of researchers from different elds. For
instance, a large number of environmental sequences have been
obtained by microbial ecologists and were identied to species
belonging to these polyphyletic genera. The NCBI GenBank
database (http://www.ncbi.nlm.nih.gov/) is the most widely used
tool to identify these molecular reads, but the taxon names
presented in the results from GenBank searches are often
confusing because they refer to such non-monophyletic groups
or genera.
Molecular phylogenetic analyses of multiple genes have
become an effective approach to reconstruct fungal phylogenies.
As the result of the Assembling the Fungal Tree of Life (AFTOL)
project, James et al. (2006) used a six-gene dataset to resolve a
kingdom-wide fungal phylogeny and Hibbett et al. (2007) pro-
posed a comprehensive phylogenetic re-classication of the
fungi down to the ordinal level. Yeast species formed only a small
part of the nearly 200 fungal species involved in the AFTOL
project. The majority of teleomorphic ascomycetous yeast taxa
have independently been reclassied based on results obtained
from multigene phylogenetic studies (Kurtzman 2003, Kurtzman
& Robnett, 2003, 2007, Kurtzman et al. 2007, 2008), but most
basidiomycetous yeast taxa remain to be studied. In the fth
edition of The Yeasts, a Taxonomic Study(Kurtzman et al.
2011a) many of the basidiomycetous yeast genera included
are still highly polyphyletic.
The recent changes in the dual nomenclature for pleomorphic
fungi prompted us to modify the classication of Trem-
ellomycetes to full the One Fungus = One Nameprinciple
(McNeill et al. 2012). As is the case in other groups of fungi,
many species of this class have separate teleomorphic and
anamorphic names. A further change in the new nomenclature is
that electronic publication of new taxa and their names is
permitted from 1 January 2012 in the absence of a printed hard
copy (Knapp et al. 2011). So far, approximately 190 new fungal
species have been e-published in Index Fungorum since then
(http://www.indexfungorum.org/). The e-publication rule will
accelerate the description of new fungal species, and this further
urges us to revise the taxonomy of the Tremellomycetes in order
to provide a stable taxonomic framework that reects our
knowledge of the phylogenetic diversity and relationships of
these fungi.
Several studies across the eukaryotic tree of life have shown
that there is poor equivalence of taxonomic ranks across the
groups studied (Johns & Avise 1998, Avise & Johns 1999,
Castresana 2001, Lumbsch 2002, Avise & Liu 2011, Talavera
et al. 2013). Clades of the same rank often show high vari-
ance with regard to genetic distances and temporal aspects.
Despite the arbitrary nature of taxonomic ranks above the spe-
cies level, they have importance in an evolutionary framework for
cataloguing and communicating about biological diversity and,
hence, taxonomic decisions should be made on a consistent
basis (Holt & Jonsson 2014). Different methods have been
suggested to level off ranks within taxonomic groups, including a
temporal approach (Hennig 1966, Farris 1976, Avise & Johns
1999, Holt & Jonsson 2014), but they have not commonly
been applied in botany, mycology and zoology (Vences et al.
2013). In bacteriology, a quantitative interpretation of ranks is
much more common, particularly by means of traditional (Tindall
et al. 2010) or digital (Meier-Kolthoff et al. 2013) DNA:DNA
hybridisation thresholds for species and 16S rRNA gene
thresholds for higher ranks (Yarza et al. 2014). However,
thresholds for pairwise (dis-)similarities are not a phylogenetic
criterion (Wiley & Lieberman 2011) and can yield inconsistencies
(Meier-Kolthoff et al. 2014). Moreover, the method used by Yarza
et al. (2014) to estimate similarity thresholds does not guarantee
maximum agreement with the existing assignment to ranks,
which could be obtained using clustering optimisation (Göker
et al. 2009, 2010, Stielow et al. 2011). Another question
regarding Linnaean classication is whether higher taxa are real;
this has usually been denied in the literature (Wiley & Lieberman
PHYLOGENETIC CLASSIFICATION OF THE TREMELLOMYCETES
www.studiesinmycology.org 87
2011, Vences et al. 2013), but recent studies found statistical
tests to identify evolutionary signicant units above the species
level (Humphreys & Barraclough 2014, Barraclough &
Humphreys 2015).
Recently, we reconstructed the phylogeny of trem-
ellomycetous yeasts and related dimorphic and lamentous
Tremellomycetes by analysing sequences from seven genes (Liu
et al. 2015), resulting in a relatively robust framework that allows
us to update the taxonomic system of the Tremellomycetes.
Here, we employed two quantitative methods, namely a phylo-
genetic variant of clustering optimisation (Göker et al. 2009,
2010, Stielow et al. 2011) and the iterative application of a
modied general mixed Yule coalescent (GMYC) (Humphreys &
Barraclough 2014), to test and circumscribe the taxonomic units
at the order, family and genus levels recognised from this mul-
tigene phylogeny. Results of either method were not followed
strictly, however, but were modied where necessary to
decrease the number of new taxa to be introduced. Moreover, a
comprehensively sampled LSU rRNA gene phylogeny, including
taxa that were not studied in the seven-gene phylogeny, was
constructed for Tremellomycetes integrating both yeasts and
lamentous fungi, incorporating information from the seven-gene
phylogeny by using backbone constraints. An updated taxonomic
system for Tremellomycetes is consequently proposed based on
the integrated phylogenetic evidence combined with morpho-
logical and physiological criteria.
MATERIALS AND METHODS
Organisms
A total of 294 tremellomycetous yeast strains, including the type
strains of 286 currently recognised species and varieties as listed
in Table 1 of Liu et al. (2015), were employed in this study. In
addition, 47 tremellomycetous yeast species which were pub-
lished too late to be included in the study of Liu et al. (2015) and
47 more fruiting body forming species from the genera Tremella,
Syzygospora,Rhynchogastrema,Tetragoniomyces and Trimor-
phomyces were employed in this study (Table 1). Additionally, 23
novel but undescribed species retrieved from the public dataset
were also included. Five Cryptococcus species recently
described by Hagen et al. (2015) were listed in Table 1 of
accepted species names but not included in the phylogenetic
analyses. Large ribosomal subunit (LSU) rRNA gene sequences
were additionally sampled specically from related and la-
mentous taxa in Tremellomycetes, for which no culture material
or other nucleotide data are available. All together, a total of 435
taxa were compared in this study.
Phylogenetic analysis
The phylogenetic analysis used for the taxonomic backbone in
this study was presented in Liu et al. (2015). The phylogeny was
inferred from a seven-gene dataset comprising nucleotide se-
quences of the internal transcribed spacer region (ITS) rRNA
gene, the D1/D2 domains of the large subunit (LSU or 26S)
rRNA gene, the small subunit (SSU or 18S) rRNA gene, two
subunits of RNA polymerase II (RPB1 and RPB2), translation
elongation factor 1-α(TEF1) and cytochrome b(CYTB), using
Bayesian inference, maximum likelihood (ML) and neighbour-
joining (NJ) analyses (Liu et al. 2015). The supplementary LSU
rRNA gene (D1/D2 domains) sequence dataset containing newly
published tremellomycetous yeast species and additional la-
mentous teleomorphic taxa was constructed and subjected to
constrained maximum likelihood (ML) and maximum parsimony
(MP) analyses based on the topology of a seven-genes dataset
taken from Liu et al. (2015). The LSU sequences were aligned
with MAFFT version 7 and the G-INS-i option. Constrained
phylogenetic analyses were only inforced for species previously
analysed using seven DNA loci. Only bipartitions that received at
least 85 % bootstrap support during fast bootstrapping of the
seven-genes dataset (Liu et al. 2015) conducted with Pthreads-
parallelised RAxML version 8.1.24 (Stamatakis 2014) were used
as a backbone constraint for LSU phylogenetic inference. Fast
bootstrapping in conjunction with the autoMRE bootstopping
criterion (Pattengale et al. 2009) and subsequent search for the
best tree (Stamatakis et al. 2008) were conducted using the
GTRCAT model approximation. MP bootstrapping with 1 000
replicates was conducted with TNT version 1.1/June 2015
(Goloboff et al. 2008).
Quantitative assessment of taxonomic ranks
Two methods were used for the assessment of taxonomic ranks
on the basis of the maximum likelihood tree obtained from the
concatenated sequences of the seven genes (Liu et al. 2015).
Firstly, we used a phylogeny-based variant of clustering optimi-
sation called phylogenetic rank boundary optimisation (PRBO).
The goal of clustering optimisation (Göker et al. 2009, 2010,
Stielow et al. 2011) is to detect distance thresholds (and clus-
tering parameters) that yield non-hierarchical clusterings that are
in maximal agreement with a given reference clustering (such as
a classication into taxa of a single rank). The limitations of the
approach are that it is rather a clustering method than a phylo-
genetic approach, even though the resulting clusters