The Ecology and Evolution of the Baker's Yeast Saccharomyces cerevisiae

Abstract

The baker's yeast Saccharomyces cerevisiae has become a powerful model in ecology and evolutionary biology. A global effort on field survey and population genetics and genomics of S. cerevisiae in past decades has shown that the yeast distributes ubiquitously in nature with clearly structured populations. The global genetic diversity of S. cerevisiae is mainly contributed by strains from Far East Asia, and the ancient basal lineages of the species have been found only in China, supporting an 'out-of-China' origin hypothesis. The wild and domesticated populations are clearly separated in phylogeny and exhibit hallmark differences in sexuality, heterozygosity, gene copy number variation (CNV), horizontal gene transfer (HGT) and introgression events, and maltose utilization ability. The domesticated strains from different niches generally form distinct lineages and harbor lineage-specific CNVs, HGTs and introgressions, which contribute to their adaptations to specific fermentation environments. However, whether the domesticated lineages originated from a single, or multiple domestication events is still hotly debated and the mechanism causing the diversification of the wild lineages remains to be illuminated. Further worldwide investigations on both wild and domesticated S. cerevisiae, especially in Africa and West Asia, will be helpful for a better understanding of the natural and domestication histories and evolution of S. cerevisiae.

Keywords: Saccharomyces cerevisiae; ecology; evolution; phylogeography; population genomics; yeast domestication.

Figure 2

Success rates of S. cerevisiae isolation from different substrates in the wild. Data are from Wang et al. [20] except those marked with an asterisk which are from Barbosa et al. [59]. The substrates with more than ten samples subjected to S. cerevisiae isolation are selected. The types of the substrates (fruit, tree bark, soil and rotten wood) are distinguished using different colors and the specific substrates in each group are arranged according to the success rates of S. cerevisiae isolation.

Figure 1

The life cycle and mating behaviors of S. cerevisiae. Vegetative cells are usually diploid and reproduce asexually by budding (mitosis). A diploid cell undergoes meiosis and sporulation due to nitrogen starvation and results in the formation of a tetrad with four ascospores, which either undergo intratetrad mating to form a diploid cell, or germinate to form haploid cells. A haploid cell either reproduces by budding, or mates with a sibling or non-sibling haploid with an opposite mating type to form a diploid cell, or undergoes haplo-selfing or autodiploidization through a process known as mating-type (MAT) switch to restore the diploid phase.

Figure 3

Geographic (A) and ecological (B) origins of the S. cerevisiae strains with their genome sequences available to the public.

Figure 4

A schematic diagram showing the phylogenetic relationships of the recognized lineages of S. cerevisiae. The dendrogram is drawn according to the phylogenomic analysis performed by Han et al. [22] based on genome-wide SNPs from a set of S. cerevisiae strains representing the maximum global genetic diversity and almost all recognized lineages of S. cerevisiae, however, branch lengths do not exactly correspond to genetic distances between different lineages. The mosaic strains are not included. The wild and domesticated (liquid- and solid-state fermentation) groups are distinguished using branch lines with different colors. The pie charts represent the geographic origins of the strains in each lineage.

Figure 5

Sequence diversity within and divergence between different lineages (A), and sequence diversity of different groups (B), of S. cerevisiae. The data were calculated from the genome-wide SNPs from a set of 612 strains compared in Han et al. [22] representing the maximum global genetic diversity and almost all recognized lineages of S. cerevisiae. SSF, solid-state fermentation; LSF, liquid-state fermentation.

Figure 6

A schematic illustration of a modified Mortimer’s genome renewal model for explaining the diversification of wild S. cerevisiae strains. Theoretically, in the case of one neutral mutation in one locus (A), one new homozygous diploid cell line with a new genotype can be created; while in the case of two loci harboring one neutral mutation each (B), three new homozygous diploid cell lines with different genotypes can be created via meiotic recombination and haplo-selfing processes.