Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum

Abstract

Summary Budding yeasts (subphylum Saccharomycotina) are found in every biome and are as genetically diverse as plants or animals. To understand budding yeast evolution, we analyzed the genomes of 332 yeast species, including 220 newly sequenced ones, which represent nearly a third of all known budding yeast diversity. Here we establish a robust genus-level phylogeny comprised of 12 major clades, infer the timescale of diversification from the Devonian Period to the present, quantify horizontal gene transfer (HGT), and reconstruct the evolution of 45 metabolic traits and the metabolic toolkit of the Budding Yeast Common Ancestor (BYCA). We infer that BYCA was metabolically complex and chronicle the tempo and mode of genomic and phenotypic evolution across the subphylum, which is characterized by very low HGT levels and widespread losses of traits and the genes that control them. More generally, our results argue that reductive evolution is a major mode of evolutionary diversification.

The Wickerhamiella/Starmerella clade—A treasure trove for the study of the evolution of yeast metabolism

“…Ffz1 homologues are widespread but patchily distributed in the Ascomycota (present in the Pezizomycotina and the Saccharomycotina) and in the Basidiomycota (all three sub-phyla) but not in earlier derived fungal lineages (Gonçalves et al, 2016). Interestingly, the Ffz1 transporter from Ustilago maydis (Basidiomycota) expressed in Saccharomyces cerevisiae did not accept fructose as a substrate but transported instead mannose, glucose, and galactose These data correspond to a subset of the orthologue groups estimated by Shen et al, 2018, including all W/S taxa for which genomic data is available and selected outgroups. Due to the conditions imposed for their selection, the orthologue groups are very likely to contain only vertically inherited genes.…”

“…Presently, molecular phylogenies, especially those based on whole‐genome data, provide robust evidence for a phylogenetic proximity between these two genera, which, together, form a monophylum that branches in the phylogeny of the Saccharomycotina close to Yarrowia lipolytica (Shen et al, ). Many species that populate the clade formed by Wickerhamiella and Starmerella , henceforth named the W/S clade, were described before molecular phylogenies were the standard criterion for species delimitation.…”

“…(Panel a) Maximum‐likelihood inference estimated with 398 concatenated amino acid orthologue groups present in a single copy in all included species. These data correspond to a subset of the orthologue groups estimated by Shen et al, , including all W/S taxa for which genomic data is available and selected outgroups. Due to the conditions imposed for their selection, the orthologue groups are very likely to contain only vertically inherited genes.…”

“…Only bootstrap values below 100 are shown. Phylogeny was rooted using Tortispora caseinolytica as the outgroup based on the phylogenetic analyses of Shen et al, . (Panel b) Evolutionary events involving alcoholic fermentation (a), siderophore biosynthesis (s), and thiamine salvage (t) pathways in the W/S clade are shown.…”

“…The postulated loss of alcoholic fermentation in the W/S clade may have been part of a major loss of metabolic capabilities, mentioned above, which apparently took place after the separation of the lineage leading to the W/S clade from its neighbour lineage encompassing Sugiyamaella , Spencermartinsiella , Blastobotrys , and others (Shen et al, ). This is the most abrupt loss of metabolic traits in yeast evolution, as predicted by the analyses of Shen et al (). After or around the time of the loss of alcoholic fermentation and in most cases possibly unrelated to this event, multiple surges of horizontal gene transfer events occurred in the W/S clade over a relatively long period of time (Figure ).…”