A genome-informed higher rank classification of the biotechnologically important fungal subphylum <i> Saccharomycotina</i>

Abstract

The subphylum <i>Saccharomycotina</i> is a lineage in the fungal phylum <i>Ascomycota</i> that exhibits levels of genomic diversity similar to those of plants and animals. The <i>Saccharomycotina</i> consist of more than 1 200 known species currently divided into 16 families, one order, and one class. Species in this subphylum are ecologically and metabolically diverse and include important opportunistic human pathogens, as well as species important in biotechnological applications. Many traits of biotechnological interest are found in closely related species and often restricted to single phylogenetic clades. However, the biotechnological potential of most yeast species remains unexplored. Although the subphylum <i>Saccharomycotina</i> has much higher rates of genome sequence evolution than its sister subphylum, <i>Pezizomycotina</i>, it contains only one class compared to the 16 classes in <i>Pezizomycotina</i>. The third subphylum of <i>Ascomycota</i>, the <i>Taphrinomycotina</i>, consists of six classes and has approximately 10 times fewer species than the <i>Saccharomycotina</i>. These data indicate that the current classification of all these yeasts into a single class and a single order is an underappreciation of their diversity. Our previous genome-scale phylogenetic analyses showed that the <i>Saccharomycotina</i> contains 12 major and robustly supported phylogenetic clades; seven of these are current families (<i>Lipomycetaceae, Trigonopsidaceae, Alloascoideaceae, Pichiaceae, Phaffomycetaceae, Saccharomycodaceae</i>, and <i>Saccharomycetaceae</i>), one comprises two current families (<i>Dipodascaceae</i> and <i>Trichomonascaceae</i>), one represents the genus <i>Sporopachydermia</i>, and three represent lineages that differ in their translation of the CUG codon (CUG-Ala, CUG-Ser1, and CUG-Ser2). Using these analyses in combination with relative evolutionary divergence and genome content analyses, we propose an updated classification for the <i>Saccharomycotina</i>, including seven classes and 12 orders that can be diagnosed by genome content. This updated classification is consistent with the high levels of genomic diversity within this subphylum and is necessary to make the higher rank classification of the <i>Saccharomycotina</i> more comparable to that of other fungi, as well as to communicate efficiently on lineages that are not yet formally named. <b>Taxonomic novelties: New classes:</b> <i>Alloascoideomycetes</i> M. Groenew., Hittinger, Opulente & A. Rokas, <i>Dipodascomycetes</i> M. Groenew., Hittinger, Opulente & A. Rokas, <i>Lipomycetes</i> M. Groenew., Hittinger, Opulente, A. Rokas, <i>Pichiomycetes</i> M. Groenew., Hittinger, Opulente & A. Rokas, <i>Sporopachydermiomycetes</i> M. Groenew., Hittinger, Opulente & A. Rokas, <i>Trigonopsidomycetes</i> M. Groenew., Hittinger, Opulente & A. Rokas. <b>New orders:</b> <i><b>Alloascoideomycetes:</b></i> <i>Alloascoideales</i> M. Groenew., Hittinger, Opulente & A. Rokas; <i><b>Dipodascomycetes:</b> Dipodascales</i> M. Groenew., Hittinger, Opulente & A. Rokas; <i><b>Lipomycetes:</b></i> <i>Lipomycetales</i> M. Groenew., Hittinger, Opulente & A. Rokas; <i><b>Pichiomycetes:</b> Alaninales</i> M. Groenew., Hittinger, Opulente & A. Rokas, <i>Pichiales</i> M. Groenew., Hittinger, Opulente & A. Rokas, <i>Serinales</i> M. Groenew., Hittinger, Opulente & A. Rokas; <i><b>Saccharomycetes:</b> Phaffomycetales</i> M. Groenew., Hittinger, Opulente & A. Rokas, <i>Saccharomycodales</i> M. Groenew., Hittinger, Opulente & A. Rokas; <i><b>Sporopachydermiomycetes:</b> Sporopachydermiales</i> M. Groenew., Hittinger, Opulente & A. Rokas; <i><b>Trigonopsidomycetes:</b> Trigonopsidales</i> M. Groenew., Hittinger, Opulente & A. Rokas. <b>New families:</b> <i><b>Alaninales:</b> Pachysolenaceae</i> M. Groenew., Hittinger, Opulente & A. Rokas; <i><b>Pichiales:</b> Pichiaceae</i> M. Groenew., Hittinger, Opulente & A. Rokas; <i><b>Sporopachydermiales:</b> Sporopachydermiaceae</i> M. Groenew., Hittinger, Opulente & A. Rokas. <b>Citation:</b> Groenewald M, Hittinger CT, Bensch K, Opulente DA, Shen X-X, Li Y, Liu C, LaBella AL, Zhou X, Limtong S, Jindamorakot S, Gonçalves P, Robert V, Wolfe KH, Rosa CA, Boekhout T, Čadež N, Péter G, Sampaio JP, Lachance M-A, Yurkov AM, Daniel H-M, Takashima M, Boundy-Mills K, Libkind D, Aoki K, Sugita T, Rokas A (2023). A genome-informed higher rank classification of the biotechnologically important fungal subphylum <i>Saccharomycotina</i>. <i>Studies in Mycology</i> <b>105</b>: 1-22. doi: 10.3114/sim.2023.105.01 This study is dedicated to the memory of Cletus P. Kurtzman (1938-2017), a pioneer of yeast taxonomy.