Deep sampling of ancestral genetic diversity reveals Saccharomyces cerevisiae pre-domestication life histories

Abstract

The ecology and genetic diversity of model yeast Saccharomyces cerevisiae prior to human domestication remain poorly understood. Taiwan is regarded as part of this yeast's geographic birthplace where the most divergent natural lineage was discovered. Here, we deep sampled the broad-leaf forests across this continental island to probe the ancestral species diversity. We found that S. cerevisiae is ubiquitously distributed at low abundance in the forests. Whole-genome sequencing of 121 isolates revealed nine distinct lineages, the highest known in any region. Three lineages are endemic to Taiwan and six lineages are widespread in Asia. Molecular dating placed the divergence of the Taiwanese and Asian lineages during the Pleistocene, when a continental shelf land bridge exposed connecting Taiwan to other major landmasses. Extensive historical and recent admixture events were detected between natural lineages. In particular, the genetic component from a lineage associated with fruits that spanned the widest geographical range was present in most admixed isolates. Collectively, Taiwanese isolates harbor genetic diversity comparable to that of the whole Asia continent, and different lineages have coexisted at a fine spatial scale even on the same tree. Patterns of variations within each lineage revealed that S. cerevisiae is highly clonal and predominantly reproduces asexually in nature. We detected prevalent purifying selection genome-wide across all natural lineages with signals of positive or directional selection independent between lineages. This study establishes that S. cerevisiae has rich natural diversity without human influences, making it a powerful model system in microbial ecology.

Yeasts from temperate forests

“…Large variations exist in the frequency of sex in yeast (for a review, see Nieuwenhuis & James, 2016). Population genomic methods can be used to estimate the relative frequency of asexual and sexual reproduction by comparing differences in mutation and recombination rates (Friedrich et al, 2015; Lee et al, 2021; Tsai et al, 2008) and have shown population‐level differences (Drott et al, 2020; Koufopanou et al, 2020; Liti et al, 2009; Tsai et al, 2008).…”

“…Similar surveys also identified other northern hemisphere Saccharomyces species (Sampaio & Gonçalves, 2008). For instance, recent studies suggest that eastern Asia harbors several Saccharomyces species characterized by high genetic diversity (Bendixsen et al, 2021; Bing et al, 2014; Duan et al, 2018; Han et al, 2021; Lee et al, 2021; Peter et al, 2018; Wang et al, 2012), including temperate forest S. cerevisiae populations that are strongly diverged from domesticated populations (Duan et al, 2018; Wang et al, 2012). Some examples of successful sampling efforts that uncovered multiple species include a study in which S. kudriavzevii , S. uvarum , and S. cerevisiae were isolated from oak bark in Portugal (Sampaio & Gonçalves, 2008, 2017), and another in which S. arboricola , S. kudriavzevii , and S. cerevisiae were isolated from mushrooms, litter and leaves in Taiwan (Naumov, Lee, & Naumova, 2013).…”