Reconstructing the Backbone of the Saccharomycotina Yeast Phylogeny Using Genome-Scale Data

Abstract

Understanding the phylogenetic relationships among the yeasts of the subphylum Saccharomycotina is a prerequisite for understanding the evolution of their metabolisms and ecological lifestyles. In the last two decades, the use of rDNA and multilocus data sets has greatly advanced our understanding of the yeast phylogeny, but many deep relationships remain unsupported. In contrast, phylogenomic analyses have involved relatively few taxa and lineages that were often selected with limited considerations for covering the breadth of yeast biodiversity. Here we used genome sequence data from 86 publicly available yeast genomes representing nine of the 11 known major lineages and 10 nonyeast fungal outgroups to generate a 1233-gene, 96-taxon data matrix. Species phylogenies reconstructed using two different methods (concatenation and coalescence) and two data matrices (amino acids or the first two codon positions) yielded identical and highly supported relationships between the nine major lineages. Aside from the lineage comprised by the family Pichiaceae, all other lineages were monophyletic. Most interrelationships among yeast species were robust across the two methods and data matrices. However, eight of the 93 internodes conflicted between analyses or data sets, including the placements of: the clade defined by species that have reassigned the CUG codon to encode serine, instead of leucine; the clade defined by a whole genome duplication; and the species Ascoidea rubescens. These phylogenomic analyses provide a robust roadmap for future comparative work across the yeast subphylum in the disciplines of taxonomy, molecular genetics, evolutionary biology, ecology, and biotechnology. To further this end, we have also provided a BLAST server to query the 86 Saccharomycotina genomes, which can be found at http://y1000plus.org/blast.

Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum

“…Surprisingly, one of the resolved internodes concerned the placement of the CUG-Ser2 clade, which was equivocal in previous phylogenomic studies (Riley et al, 2016; Shen et al, 2016a, 2017). For example, the most recent phylogenomic analysis, in which the CUG-Ser2 clade was represented by a single taxon, showed that the clade’s placement was unduly influenced by inclusion of the DPMI (in S. cerevisieae) gene (Shen et al, 2017).…”

“…The new phylogeny divides the subphylum into 12 major clades (Figure 2), at least two and up to eight more than previously recognized (Dujon and Louis, 2017; Hittinger et al, 2015; Kurtzman and Boekhout, 2017; Kurtzman et al, 2011; Shen et al, 2016a). Several families are now well circumscribed (e.g., Pichiaceae), while other families are not reciprocally monophyletic (e.g., Dipodascaceae/Trichomonascaceae), leading us to consider them as major clades comprised of multiple known families.…”

“…The qualities of the genome assemblies of the 196 newly sequenced (Y1000+ Project genomes) and 136 publicly available (RIKEN plus previously published genomes) budding yeast species were assessed by quantifying their completeness based on the expected gene content of the Benchmarking Universal Single-Copy Orthologs (BUSCO), version 2.0.1 (Waterhouse et al, 2018), as described previously (Shen et al, 2016a). We used a set of 1,759 BUSCO genes inferred to be saccharomyceta-specific (“saccharomyceta” is an informal taxonomic rank used by many databases, including NCBI: https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?mode=Info&id=716545) and single-copy in at least 90% of 60 genomes in the OrthoDB Version 9 database (Zdobnov et al, 2017) to evaluate the completeness of the 332 genome assemblies.…”

An Evolutionary Perspective on Yeast Mating-Type Switching

“…It is likely that the two-locus system corresponds to a simpler ancestral mechanism of switching (Hanson et al 2014), and this conclusion is supported by the existence of switching by inversion in both A. rubescens and the methylotrophs, regardless of which of the proposed phylogenetic positions of A. rubescens is correct (Riley et al 2016; Shen et al 2016). …”

“…Based on Riley et al (2016), with placement of A. rubescens as in Shen et al (2016). Mating-type switching does not occur in species with only one MAT -like locus or in Aspergillus nidulans , which is a primary homothallic species.…”