Diversity and phylogeny of basidiomycetous yeasts from plant leaves and soil: Proposal of two new orders, three new families, eight new genera and one hundred and seven new species

A-H Li; F-X Yuan; M Groenewald; K Bensch; A M Yurkov; K Li; P-J Han; L-D Guo; M C Aime; J P Sampaio; S Jindamorakot; B Turchetti; J Inacio; B Fungsin; Q-M Wang; F-Y Bai

doi:10.1016/j.simyco.2020.01.002

Diversity and phylogeny of basidiomycetous yeasts from plant leaves and soil: Proposal of two new orders, three new families, eight new genera and one hundred and seven new species

Stud Mycol. 2020 Jan 28:96:17-140. doi: 10.1016/j.simyco.2020.01.002. eCollection 2020 Jun.

Authors

A-H Li^{1

2}, F-X Yuan^{1

3}, M Groenewald⁴, K Bensch⁴, A M Yurkov⁵, K Li¹, P-J Han¹, L-D Guo¹, M C Aime⁶, J P Sampaio^{7

8}, S Jindamorakot⁹, B Turchetti¹⁰, J Inacio¹¹, B Fungsin¹², Q-M Wang^{1

13}, F-Y Bai¹

Affiliations

¹ State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China.
² China General Microbiological Culture Collection Center and State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China.
³ North Minzu University, Yinchuan, Ningxia, 750030, China.
⁴ Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, Utrecht, 3584 CT, The Netherlands.
⁵ Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, 38124, Germany.
⁶ Purdue University, Department of Botany and Plant Pathology, West Lafayette, IN, 47901, USA.
⁷ UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal.
⁸ PYCC - Portuguese Yeast Culture Collection, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal.
⁹ National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathum Thani, 12120, Thailand.
¹⁰ Department of Agriculture, Food and Environmental Sciences & Industrial Yeasts Collection DBVPG, University of Perugia, Perugia, 74 - I-06121, Italy.
¹¹ School of Pharmacy and Biomolecular Sciences, University of Brighton, Brighton, BN2 4GJ, UK.
¹² TISTR Culture Collection, Thailand Institute of Scientific and Technological Research (TISTR), 35 M 3, Technopolis, Khlong Ha, Khlong Luang, Pathum Thani, 12120, Thailand.
¹³ College of Life Sciences, Hebei University, Baoding, Hebei Province, 071002, China.

Abstract

Nearly 500 basidiomycetous yeast species were accepted in the latest edition of The Yeasts: A Taxonomic Study published in 2011. However, this number presents only the tip of the iceberg of yeast species diversity in nature. Possibly more than 99 % of yeast species, as is true for many groups of fungi, are yet unknown and await discovery. Over the past two decades nearly 200 unidentified isolates were obtained during a series of environmental surveys of yeasts in phyllosphere and soils, mainly from China. Among these isolates, 107 new species were identified based on the phylogenetic analyses of nuclear ribosomal DNA (rDNA) [D1/D2 domains of the large subunit (LSU), the small subunit (SSU), and the internal transcribed spacer region including the 5.8S rDNA (ITS)] and protein-coding genes [both subunits of DNA polymerase II (RPB1 and RPB2), the translation elongation factor 1-α (TEF1) and the mitochondrial gene cytochrome b (CYTB)], and physiological comparisons. Forty-six of these belong to 16 genera in the Tremellomycetes (Agaricomycotina). The other 61 are distributed in 26 genera in the Pucciniomycotina. Here we circumscribe eight new genera, three new families and two new orders based on the multi-locus phylogenetic analyses combined with the clustering optimisation analysis and the predicted similarity thresholds for yeasts and filamentous fungal delimitation at genus and higher ranks. Additionally, as a result of these analyses, three new combinations are proposed and 66 taxa are validated.

Keywords: Apiotrichum xylopini S.O. Suh, C.F. Lee, Gujjari & J.J. Zhou ex Kachalkin, Yurkov & Boekhout; Bannozyma arctica Vishniac & M. Takash. ex Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout; Basidiomycetous yeasts; Begerowomyces Q.M. Wang & F.Y. Bai; Begerowomyces foliicola Q.M. Wang, F.Y. Bai & A.H. Li; Bensingtonia pseudorectispora Q.M. Wang, F.Y. Bai & A.H. Li; Bensingtonia wuzhishanensis Q.M. Wang, F.Y. Bai & A.H. Li; Boekhoutia Q.M. Wang & F.Y. Bai; Boekhoutia sterigmata Q.M. Wang, F.Y. Bai & A.H. Li; Bulleribasidium cremeum Q.M. Wang, F.Y. Bai & A.H. Li; Bulleribasidium elongatum Q.M. Wang, F.Y. Bai & A.H. Li; Bulleribasidium panici Fungsin, M. Takash. & Nakase ex Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Bulleribasidium phyllophilum Q.M. Wang, F.Y. Bai & A.H. Li; Bulleribasidium phyllostachydis Q.M. Wang, F.Y. Bai & A.H. Li; Bulleribasidium pseudopanici Q.M. Wang, F.Y. Bai & A.H. Li; Bulleribasidium siamense Fungsin, M. Takash. & Nakase ex Q.M. Wang, F.Y. Bai, Boekhout & Nakase; Carcinomyces arundinariae Fungsin, M. Takash. & Nakase ex Yurkov; Carlosrosaea foliicola Q.M. Wang, F.Y. Bai & A.H. Li; Carlosrosaea simaoensis Q.M. Wang, F.Y. Bai & A.H. Li; Chrysozyma cylindrica Q.M. Wang, F.Y. Bai & A.H. Li; Chrysozyma flava Q.M. Wang, F.Y. Bai & A.H. Li; Chrysozyma fusiformis Q.M. Wang, F.Y. Bai & A.H. Li; Chrysozyma iridis Q.M. Wang, F.Y. Bai & A.H. Li; Chrysozyma pseudogriseoflava Q.M. Wang, F.Y. Bai & A.H. Li; Chrysozyma rhododendri Q.M. Wang, F.Y. Bai & A.H. Li; Chrysozyma sambuci Q.M. Wang, F.Y. Bai & A.H. Li; Chrysozyma sorbariae Q.M. Wang, F.Y. Bai & A.H. Li; Colacogloea aletridis Q.M. Wang, F.Y. Bai & A.H. Li; Colacogloea hydrangeae Q.M. Wang, F.Y. Bai & A.H. Li; Colacogloea rhododendri Q.M. Wang, F.Y. Bai & A.H. Li; Colacogloea subericola (Belloch, Villa-Carv., Á;lv.-Rodríg. & Coque) Q.M. Wang, & F.Y. Bai; Cystobasidium alpinum Turchetti, Selbmann, Onofri & Buzzini; Cystobasidium portillonense Laich, Vaca & R. Chávez ex Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout; Cystobasidium raffinophilum Q.M. Wang, F.Y. Bai & A.H. Li; Cystobasidium terricola Q.M. Wang, F.Y. Bai & A.H. Li; Derxomyces bifurcus Q.M. Wang, F.Y. Bai & A.H. Li; Derxomyces cylindricus F.Y. Bai, Q.M. Wang & M. Takash. ex F.Y. Bai & Q.M. Wang; Derxomyces elongatus Q.M. Wang, F.Y. Bai & A.H. Li; Derxomyces hubeiensis F.Y. Bai, Q.M. Wang & M. Takash. ex F.Y. Bai & Q.M. Wang; Derxomyces longicylindricus Q.M. Wang, F.Y. Bai & A.H. Li; Derxomyces longiovatus Q.M. Wang, F.Y. Bai & A.H. Li; Derxomyces melastomatis Q.M. Wang, F.Y. Bai & A.H. Li; Derxomyces nakasei F.Y. Bai, Q.M. Wang & M. Takash. ex F.Y. Bai & Q.M. Wang; Derxomyces napiformis Q.M. Wang, F.Y. Bai & A.H. Li; Derxomyces ovatus Q.M. Wang, F.Y. Bai & A.H. Li; Derxomyces polymorphus Q.M. Wang, F.Y. Bai & A.H. Li; Derxomyces pseudoboekhoutii Q.M. Wang, F.Y. Bai & A.H. Li; Derxomyces pseudoyunnanensis Q.M. Wang, F.Y. Bai & A.H. Li; Derxomyces taiwanicus Q.M. Wang, F.Y. Bai & A.H. Li; Derxomyces xingshanicus Q.M. Wang, F.Y. Bai & A.H. Li; Dioszegia heilongjiangensis Q.M. Wang, F.Y. Bai & A.H. Li; Dioszegia kandeliae Q.M. Wang, F.Y. Bai, L.D. Guo & A.H. Li; Dioszegia maotaiensis Q.M. Wang, F.Y. Bai & A.H. Li; Dioszegia milinica Q.M. Wang, F.Y. Bai & A.H. Li; Dioszegia ovata Q.M. Wang, F.Y. Bai & A.H. Li; Dioszegia zsoltii F.Y. Bai, M. Takash. & Nakase; F.Y. Bai, M. Groenew. & Boekhout; Filobasidium dingjieense Q.M. Wang, F.Y. Bai & A.H. Li; Filobasidium globosum Q.M. Wang, F.Y. Bai & A.H. Li; Filobasidium mali Q.M. Wang, F.Y. Bai & A.H. Li; Filobasidium mucilaginum Q.M. Wang, F.Y. Bai & A.H. Li; Genolevuria bromeliarum Landell & P. Valente ex Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Genolevuria pseudoamylolytica Q.M. Wang, F.Y. Bai & A.H. Li; Glaciozyma Turchetti, Connell, Thomas-Hall & Boekhout ex M. Groenew. & Q.M. Wang; Glaciozyma antarctica (Fell, Statzell, I.L. Hunter & Phaff) M. Groenew. & Q.M. Wang; Glaciozyma martinii Turchetti, Connell, Thomas-Hall & Boekhout; Glaciozyma watsonii Turchetti, Connell, Thomas-Hall & Boekhout; Heitmania cylindrica Q.M. Wang, F.Y. Bai & A.H. Li; Heitmania tridentata Q.M. Wang, F.Y. Bai & A.H. Li; Heitmaniaceae Q.M. Wang & F.Y. Bai; Heitmaniales Q.M. Wang & F.Y. Bai; Holtermannia saccardoi Q.M. Wang, F.Y. Bai & A.H. Li; Jianyuniaceae Q.M. Wang & F.Y. Bai; Kockovaella haikouensis Q.M. Wang, F.Y. Bai & A.H. Li; Kockovaella ischaemi Q.M. Wang, F.Y. Bai & A.H. Li; Kockovaella mexicana Lopandić, O. Molnár & Prillinger ex Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Kockovaella nitrophila Q.M. Wang, F.Y. Bai & A.H. Li; Kondoa arboricola Q.M. Wang, F.Y. Bai & A.H. Li; Kondoa chamaenerii Q.M. Wang, F.Y. Bai & A.H. Li; Kondoa cylindrica Q.M. Wang, F.Y. Bai & A.H. Li; Kondoa daliangziensis Q.M. Wang, F.Y. Bai & A.H. Li; Kondoa foliicola Q.M. Wang, F.Y. Bai & A.H. Li; Kondoa lulangica Q.M. Wang, F.Y. Bai & A.H. Li; Kondoa myxariophila Q.M. Wang, F.Y. Bai & A.H. Li; Kondoa rhododendri Q.M. Wang, F.Y. Bai & A.H. Li; Kondoa ribitophobia Q.M. Wang, F.Y. Bai & A.H. Li; Kondoa thailandica Fungsin, Hamam. & Nakase ex Q.M. Wang, M. Groenew., F.Y. Bai & Boekhout; Kwoniella newhampshirensis K. Sylvester, Q.M. Wang & C.T. Hittinger; Kwoniella ovata Q.M. Wang, F.Y. Bai & A.H. Li; Kwoniella shandongensis R. Chen, Y.M. Jiang & S.C. Wei ex M. Groenew. & Q.M. Wang; Leucosporidium creatinivorum (Golubev) M. Groenew. & Q.M. Wang; Leucosporidium fragarium (J.A. Barnett & Buhagiar) M. Groenew. & Q.M. Wang; Leucosporidium intermedium (Nakase & M. Suzuki) M. Groenew. & Q.M. Wang; Leucosporidium muscorum (Di Menna) M. Groenew. & Q.M. Wang; Leucosporidium yakuticum (Golubev) M. Groenew. & Q.M. Wang; Meniscomyces Q.M. Wang & F.Y. Bai; Meniscomyces layueensis Q.M. Wang, F.Y. Bai & A.H. Li; Microbotryozyma swertiae Q.M. Wang, F.Y. Bai & A.H. Li; Microsporomyces ellipsoideus Q.M. Wang, F.Y. Bai & A.H. Li; Microsporomyces pseudomagnisporus Q.M. Wang, F.Y. Bai & A.H. Li; Microsporomyces rubellus Q.M. Wang, F.Y. Bai & A.H. Li; Molecular phylogeny; Naganishia onofrii Turchetti, Selbmann & Zucconi ex Yurkov; Naganishia vaughanmartiniae Turchetti, Blanchette & Arenz ex Yurkov; Nielozyma Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Nielozyma formosana Nakase, Tsuzuki, F.L. Lee & M. Takash. ex Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Nielozyma melastomatis Nakase, Tsuzuki, F.L. Lee & M. Takash. ex Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Oberwinklerozyma dicranopteridis Q.M. Wang, F.Y. Bai & A.H. Li; Oberwinklerozyma nepetae Q.M. Wang, F.Y. Bai & A.H. Li; Oberwinklerozyma silvestris Golubev & Scorzetti ex Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout; Oberwinklerozyma straminea Golubev & Scorzetti ex Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout; Papiliotrema aspenensis (Ferreira-Paim, et al.) Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Papiliotrema baii Yurkov, M.A. Guerreiro & Á;. Fonseca ex Yurkov; Papiliotrema frias V. de García, Zalar, Brizzio, Gunde-Cim. & Van Broock ex Yurkov; Papiliotrema hoabinhensis D.T. Luong, M. Takash., Ty, Dung & Nakase ex Yurkov; Papiliotrema japonica J.P. Samp., Fonseca & Fell ex Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Papiliotrema terrestris Crestani, Landell, Faganello, Vainstein, Vishniac & P. Valente ex Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Papiliotrema wisconsinensis K. Sylvester, Q.M. Wang & Hittinger ex Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Phaeotremella lactea Q.M. Wang, F.Y. Bai & A.H. Li; Phaeotremella ovata Q.M. Wang, F.Y. Bai & A.H. Li; Phaffia aurantiaca Q.M. Wang, F.Y. Bai & A.H. Li; Phyllozyma aceris Q.M. Wang, F.Y. Bai & A.H. Li; Phyllozyma jiayinensis Q.M. Wang, F.Y. Bai & A.H. Li; Piskurozyma fildesensis T.T. Zhang & Li Y. Yu ex Yurkov; Piskurozyma taiwanensis Nakase, Tsuzuki & M. Takash. ex Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Pseudobensingtonia fusiformis Q.M. Wang, F.Y. Bai & A.H. Li; Pseudohyphozyma hydrangeae Q.M. Wang, F.Y. Bai & A.H. Li; Pseudohyphozyma lulangensis Q.M. Wang, F.Y. Bai & A.H. Li; Pseudoleucosporidium V. de García, et al. ex M. Groenew. & Q.M. Wang; Pseudoleucosporidium fasciculatum (Babeva & Lisichk.) M. Groenew. & Q.M. Wang; Pseudosterigmatospora Q.M. Wang & F.Y. Bai; Pseudosterigmatospora motuoensis Q.M. Wang, F.Y. Bai & A.H. Li; Pseudotremella lacticolour Satoh & Makimura ex Yurkov; Rhodosporidiobolus fuzhouensis Q.M. Wang, F.Y. Bai & A.H. Li; Rhodosporidiobolus jianfalingensis Q.M. Wang, F.Y. Bai & A.H. Li; Rhodosporidiobolus platycladi Q.M. Wang, F.Y. Bai & A.H. Li; Rhynchogastrema complexa (Landell, et al.) Xin Zhan Liu, F.Y. Bai, M. Groenew., Boekhout & Yurkov; Rhynchogastrema fermentans (C.F. Lee) Xin Zhan Liu, F.Y. Bai, M. Groenew., Boekhout & Yurkov; Rhynchogastrema glucofermentans (S.O. Suh & M. Blackw.) Xin Zhan Liu, F.Y. Bai, M. Groenew., Boekhout & Yurkov; Rhynchogastrema nanyangensis F.L. Hui & Q.H. Niu ex Xin Zhan Liu, F.Y. Bai, M. Groenew., Boekhout & Yurkov; Rhynchogastrema tunnelae (Boekhout, Fell, Scorzetti & Theelen) Xin Zhan Liu, F.Y. Bai, M. Groenew., Boekhout & Yurkov; Rhynchogastrema visegradensis (G. Péter & Dlauchy) Xin Zhan Liu, F.Y. Bai, M. Groenew., Boekhout &Yurkov; Robertozyma Q.M. Wang & F.Y. Bai; Robertozyma ningxiaensis Q.M. Wang, F.Y. Bai & A.H. Li; Rosettozyma Q.M. Wang & F.Y. Bai; Rosettozyma cystopteridis Q.M. Wang, F.Y. Bai & A.H. Li; Rosettozyma motuoensis Q.M. Wang, F.Y. Bai & A.H. Li; Rosettozyma petaloides Q.M. Wang, F.Y. Bai & A.H. Li; Rosettozymaceae Q.M. Wang & F.Y. Bai; Rosettozymales Q.M. Wang & F.Y. Bai; Ruinenia bangxiensis Q.M. Wang, F.Y. Bai & A.H. Li; Ruinenia diospyri Nakase, Tsuzuki, F.L. Lee, Jindam. & M. Takash. ex Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout; Ruinenia fanjingshanensis Q.M. Wang, F.Y. Bai & A.H. Li; Ruinenia lunata Q.M. Wang, F.Y. Bai & A.H. Li; Ruinenia pyrrosiae Nakase, Tsuzuki, F.L. Lee, Jindam. & M. Takash. ex Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout; Saitozyma ninhbinhensis (D.T. Luong, M. Takash., Dung & Nakase)Yurkov; Saitozyma paraflava Golubev & J.P. Samp. ex Xin Zhan Liu; Saitozyma pseudoflava Q.M. Wang, F.Y. Bai & A.H. Li; Sakaguchia melibiophila M. Groenew., Q.M. Wang & F.Y. Bai; Slooffia globosa Q.M. Wang, F.Y. Bai & A.H. Li; Solicoccozyma gelidoterrea Q.M. Wang, F.Y. Bai & A.H. Li; Species diversity; Sporobolomyces cellobiolyticus Q.M. Wang, F.Y. Bai & A.H. Li; Sporobolomyces ellipsoideus Q.M. Wang, F.Y. Bai & A.H. Li; Sporobolomyces primogenomicus Q.M. Wang & F.Y. Bai; Sporobolomyces reniformis Q.M. Wang, F.Y. Bai & A.H. Li; Sterigmatospora Q.M. Wang & F.Y. Bai; Sterigmatospora layueensis Q.M. Wang, F.Y. Bai & A.H. Li; Symmetrospora oryzicola (Nakase & M. Suzuki) Q.M. Wang & F.Y. Bai; Symmetrospora rhododendri Q.M. Wang, F.Y. Bai & A.H. Li; Taxonomy; Teunia Q.M. Wang & F.Y. Bai; Teunia betulae K. Sylvester, Q.M. Wang & Hittinger ex Q.M. Wang, F.Y. Bai & A.H. Li; Teunia cuniculi (K.S. Shin & Y.H. Park) Q.M. Wang, F.Y. Bai & A.H. Li; Teunia globosa Q.M. Wang, F.Y. Bai & A.H. Li; Teunia helanensis Q.M. Wang, F.Y. Bai & A.H. Li; Teunia korlaensis Q.M. Wang, F.Y. Bai & A.H. Li; Teunia tronadorensis V. de Garcia, Zalar, Brizzio, Gunde-Cim. & van Brook ex Q.M. Wang, F.Y. Bai & A.H. Li; Tremella basidiomaticola Xin Zhan Liu & F.Y. Bai; Tremella shuangheensis Q.M. Wang, F.Y. Bai & A.H. Li; Trimorphomyces sakaeraticus Fungsin, M. Takash. & Nakase ex Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Vanrija meifongana C.F. Lee ex Kachalkin Yurkov & Boekhout; Vanrija nantouana C.F. Lee ex Kachalkin Yurkov & Boekhout; Vanrija thermophila Vogelmann, S. Chaves & C. Hertel ex Kachalkin Yurkov & Boekhout; Vishniacozyma europaea Q.M. Wang, F.Y. Bai & A.H. Li; Vishniacozyma foliicola Q.M. Wang & F.Y. Bai ex Yurkov; Vishniacozyma heimaeyensis Vishniac ex Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Vishniacozyma melezitolytica Q.M. Wang, F.Y. Bai & A.H. Li; Vishniacozyma pseudopenaeus Q.M. Wang, F.Y. Bai & A.H. Li; Vishniacozyma psychrotolerans V. de García, Zalar, Brizzio, Gunde-Cim. & Van Broock ex Yurkov; Vishniacozyma taibaiensis Q.M. Wang & F.Y. Bai ex Yurkov; Vishniacozyma tephrensis Vishniac ex Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout; Yamadamyces Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout; Yamadamyces rosulatus Golubev & Scorzetti ex Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout; Yamadamyces terricola Q.M. Wang, F.Y. Bai & A.H. Li; Yurkovia longicylindrica Q.M. Wang, F.Y. Bai & A.H. Li.