Genomics and the making of yeast biodiversity

Abstract

Yeasts are unicellular fungi that do not form fruiting bodies. Although the yeast lifestyle has evolved multiple times, most known species belong to the subphylum Saccharomycotina (syn. Hemiascomycota, hereafter yeasts). This diverse group includes the premier eukaryotic model system, Saccharomyces cerevisiae; the common human commensal and opportunistic pathogen, Candida albicans; and over 1000 other known species (with more continuing to be discovered). Yeasts are found in every biome and continent and are more genetically diverse than angiosperms or chordates. Ease of culture, simple life cycles, and small genomes (∼10-20Mbp) have made yeasts exceptional models for molecular genetics, biotechnology, and evolutionary genomics. Here we discuss recent developments in understanding the genomic underpinnings of the making of yeast biodiversity, comparing and contrasting natural and human-associated evolutionary processes. Only a tiny fraction of yeast biodiversity and metabolic capabilities has been tapped by industry and science. Expanding the taxonomic breadth of deep genomic investigations will further illuminate how genome function evolves to encode their diverse metabolisms and ecologies.

Figure 1. Key traits and phylogenetic relationships of the 86 yeasts of the subphylum Saccharomycotina whose genomes have been sequenced

The topology of the cladogram has been estimated conservatively from previous analyses using genome [12,23] or multi-locus sequence data [27,36]. Major clades [36] are color-coded (clade names are shown in Figure 2). Only one reference genome per species is included with preference given to the highest quality and/or most widely used reference genome. Only publicly available genome assemblies are included. Interspecies hybrids are discussed in the text but are not shown here. WGD, whole genome duplication; recent work has shown that the WGD was caused by an allopolyploidization event that occurred between an early member of the Zygosaccharomyces/Torulaspora clade and an early member of the Kluyveromyces/Lachancea/Eremothecium clade, thus making this part of the phylogeny a network, rather than a tree [73]. CTG clade, yeasts using an alternate codon table where CTG encodes serine, instead of leucine. JGI, genomes publicly available on MycoCosm at http://genome.jgi-psf.org/programs/fungi/index.jsf, which are subject to the usage terms of the DOE Joint Genome Institute until formal publication. GB1, GenBank Accession CCBQ000000000; GB2, Genbank Accession JPPO00000000; GB3, GenBank Accession AEOI00000000; GB4, GenBank Accession LCTY00000000.

Figure 2. Most yeast clades remain underrepresented by genome sequence data

Estimated species counts for each major yeast clade [36] (light colors) are compared with the number of publicly available genomes from each clade (dark sliver within larger triangles). In addition to the 807 species shown, approximately 400 anamorphic species (e.g. Candida spp.) currently lack a clear phylogenetic placement. As the phylogeny is resolved, these species will be reassigned to genera and higher taxonomic ranks consistent with their phylogeny (Box 1). Color codes are the same as in Figure 1.