Multigene phylogeny and taxonomic revision of yeasts and related fungi in the Ustilaginomycotina

Abstract

The subphylum Ustilaginomycotina (Basidiomycota, Fungi) comprises mainly plant pathogenic fungi (smuts). Some of the lineages possess cultivable unicellular stages that are usually classified as yeast or yeast-like species in a largely artificial taxonomic system which is independent from and largely incompatible with that of the smut fungi. Here we performed phylogenetic analyses based on seven genes including three nuclear ribosomal RNA genes and four protein coding genes to address the molecular phylogeny of the ustilaginomycetous yeast species and their filamentous counterparts. Taxonomic revisions were proposed to reflect this phylogeny and to implement the ‘One Fungus = One Name’ principle. The results confirmed that the yeast-containing classes Malasseziomycetes, Moniliellomycetes and Ustilaginomycetes are monophyletic, whereas Exobasidiomycetes in the current sense remains paraphyletic. Four new genera, namely Dirkmeia gen. nov., Kalmanozyma gen. nov., Golubevia gen. nov. and Robbauera gen. nov. are proposed to accommodate Pseudozyma and Tilletiopsis species that are distinct from the other smut taxa and belong to clades that are separate from those containing type species of the hitherto described genera. Accordingly, new orders Golubeviales ord. nov. with Golubeviaceae fam. nov. and Robbauerales ord. nov. with Robbaueraceae fam. nov. are proposed to accommodate the sisterhood of Golubevia gen. nov. and Robbauera gen. nov. with other orders of Exobasidiomycetes. The majority of the remaining anamorphic yeast species are transferred to corresponding teleomorphic genera based on strongly supported phylogenetic affinities, resulting in the proposal of 28 new combinations. The taxonomic status of a few Pseudozyma species remains to be determined because of their uncertain phylogenetic positions. We propose to use the term pro tempore or pro tem. in abbreviation to indicate the single-species lineages that are temporarily maintained.

Pattersoniomyces tillandsiae gen. et comb. nov.: linking sexual and asexual morphs of the only known smut fungus associated with Bromeliaceae

“…Ustilaginomycotinous yeasts are commonly detected from very diverse habitats, using both culture dependent and culture-independent methods (e.g., Boekhout et al 2003;Inácio et al 2008;Sipiczki and Kajdacsi 2009;Bourret et al 2013;Nasr et al 2014;Nasanit et al 2015Nasanit et al , 2016Tantirungkij et al 2015;Wang et al 2015;Kijpornyongpan and Aime 2017;Kruse et al 2017). The links between asexual and sexual morphs were demonstrated only for a few species, for example between Pseudozyma prolifica Bandoni and Mycosarcoma maydis (DC.)…”

“…Bref. (Sampaio 2004;Wang et al 2015), Rhodotorula acheniorum 2017). The identical LSU sequences of Pattersoniomyces tillandsiae from Honduras and yeast strains from Brazil suggest that both stages represent the same species and this finding constitutes another link of asexual and sexual morphs within Ustilaginomycotina.…”

“…The heterogeneity of the genus Ustilago was discussed by several researchers (e.g., Lindeberg 1959); however, only ultrastructural and molecular phylogenetic analyses (Bauer et al , 2001Begerow et al 1997Begerow et al , 2006Begerow et al , 2014 made a significant step towards resolving its generic boundaries. Currently, Ustilago is restricted to species parasitic on Poaceae having single spores germinating with phragmobasidia and lacking both columellae and sterile cells (McTaggart et al 2012a) and to some associated pseudozyma-like anamorphic species (Wang et al 2015). Many species originally classified in Ustilago have been reallocated to other genera placed in diverse families and orders of the Ustilaginomycotina and even in a different subphylum, the Pucciniomycotina Vánky 1998;Ershad 2000;Vánky 2002;Bauer et al 2007Bauer et al , 2008Vánky et al 2008;Lutz et al 2012;McTaggart et al 2012b;Piątek et al 2013).…”

Paraphyly and (yeast) classification

“…This situation is changing, however, as exemplified in a recent study of yeasts in the subphylum Ustilaginomycotina (Wang et al, 2015), where certain genera are slated for revision because of paraphyly. In the broader field of mycology, monophyly is becoming a stated requirement, although Verkley et al (2014), in a revision of some genera of Montagnulaceae, opted to retain a paraphyletic genus primarily because of uncertainties in the phylogeny.…”

Molecular identification of Pseudozyma aphidis (Henninger & Windisch) Boekhout: first record from a Brazilian mangrove swamp

“…Boekhout pro tempore comprises approximately 25 distinct anamorphic yeast species from the Ustilaginaceae, Basidiomycota (Index Fungorum 2016). Although a reliable connection with their teleomorph stages has not been established for many of these species (Boekhout 2011), recent studies have proposed to transfer anamorphic yeast species to their corresponding teleomorphic genera based on strongly supported phylogenetic affinities (Piatek et al 2015, Wang et al 2015. From these studies, many species of the genus Pseudozyma have been transferred to the genus Moesziomyces, as is the case of Pseudozyma aphidis (= Moesziomyces aphidis) and the use of the "pro tempore" was suggested by the authors to indicate that in Pseudozyma species names are temporarily remained.…”