Extensive sampling of Saccharomyces cerevisiae in Taiwan reveals ecology and evolution of predomesticated lineages

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 extensively sampled the broad-leaf forests across this continental island to probe the ancestral species diversity. We found that S. cerevisiae is distributed ubiquitously at low abundance in the forests. Whole-genome sequencing of 121 isolates revealed nine distinct lineages that diverged from Asian lineages during the Pleistocene, when a transient continental shelf land bridge connected Taiwan to other major landmasses. Three lineages are endemic to Taiwan and six are widespread in Asia, making this region a focal biodiversity hotspot. Both ancient and recent admixture events were detected between natural lineages and a genetic ancestry component associated with isolates from fruits was detected 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 identified different selection patterns shaping the coding sequences of natural lineages and found fewer gene family expansion and contractions which contrast with domesticated lineages. This study establishes that S. cerevisiae has rich natural diversity sheltered from human influences, making it a powerful model system in microbial ecology.

142 telomere-to-telomere assemblies reveal the genome structural landscape inSaccharomyces cerevisiae

“…1D). The root of the ortholog-based tree groups together the two most diverged Taiwanese I and the Chinese IX wild populations, which is consistent with the East Asian geographical origin of the species (Duan et al ., 2018; Lee et al ., 2022; Peter et al ., 2018; Wang et al ., 2012).…”

“…As expected, classical model organisms and species of anthropocentric and economic importance such as Escherichia coli (Wang et al, 2021), Drosophila melanogaster (Rech et al, 2022;Kim et al, 2021), Solanum lycopersicum (tomato) (Alonge et al, 2020), Glycine max (soybean) (Liu et al, 2020), Oryza sativa (rice) (Qin et al, 2021;Zhang et al, 2022), Bombyx mori (silkworm) (Tong et al, 2022) and humans (Audano et al, 2019;Beyter et al, 2021;Wong et al, 2018) already have several contiguous genomes within each species. As has often been the case in genetics and genomics, the baker's yeast, Saccharomyces cerevisiae, is at the forefront of the field currently totaling 68 long-read genome assemblies of non-reference strains (Abou Saada et al, 2021;Bendixsen et al, 2021;Berlin et al, 2015;Czaja et al, 2020;Istace et al, 2017;Jenjaroenpun et al, 2018;Lee et al, 2022;Shao et al, 2018;Yue et al, 2017;Zhang and Emerson, 2019;Heasley and Argueso, 2022).…”

“…As expected, classical model organisms and species of anthropocentric and economic importance such as Escherichia coli (Wang et al ., 2021), Drosophila melanogaster (Rech et al ., 2022; Kim et al ., 2021), Solanum lycopersicum (tomato) (Alonge et al ., 2020), Glycine max (soybean) (Liu et al ., 2020), Oryza sativa (rice) (Qin et al ., 2021; Zhang et al ., 2022), Bombyx mori (silkworm) (Tong et al ., 2022) and humans (Audano et al ., 2019; Beyter et al ., 2021; Wong et al ., 2018) already have several contiguous genomes within each species. As has often been the case in genetics and genomics, the baker’s yeast, Saccharomyces cerevisiae , is at the forefront of the field currently totaling 68 long-read genome assemblies of non-reference strains (Abou Saada et al ., 2021; Bendixsen et al ., 2021; Berlin et al ., 2015; Czaja et al ., 2020; Istace et al ., 2017; Jenjaroenpun et al ., 2018; Lee et al ., 2022; Shao et al ., 2018; Yue et al ., 2017; Zhang and Emerson, 2019; Heasley and Argueso, 2022). This data has been used to quantify contiguity improvements of long-read sequencing over short-read data (Istace et al ., 2017), create genome-wide maps of transposable elements (Bendixsen et al ., 2021; Czaja et al ., 2020; Istace et al ., 2017), characterize subtelomeric regions (Yue et al ., 2017), phase haplotypes and detect large SVs (Bendixsen et al ., 2021; Istace et al ., 2017; Jenjaroenpun et al ., 2018; Yue et al ., 2017; Heasley and Argueso, 2022).…”

Long-read genomes reveal pangenomic variation underlying yeast phenotypic diversity

“…Beyond the reference genome, S. cerevisiae presents substantial genetic and phenotypic diversity, making yeast a premier model for understanding the genetic basis of trait differences between diverse individuals. S. cerevisiae has been isolated from around the world and from diverse environments (Peter et al 2018), including domestic fermentative environments, patient samples, and wild forests, especially trees in the beech family, Fagaceae (Lee et al 2022). Whole-genome sequencing of diverse yeast isolates has revealed that many strains’ genomes contain genes not seen in the reference genome sequence.…”

“…The resulting inferred genome sequences are often fragmented and incomplete, with particular assembly challenges arising from repetitive sequences and structural variants such as translocations, copy number variants, and pangenomic insertions and deletions. In contrast, the advent of long-read sequencing, which generates reads of 10 kb or longer (Koren and Phillippy 2015), allows for assembly of highly complete yeast genomes, as repetitive or diverged DNA sequences are generally short enough that a 10-kb long read can span them completely (Yue et al 2017; Bendixsen et al 2021; Saada et al 2022; Donnell et al 2022; Istace et al 2017; Lee et al 2022). Genome sequences assembled from long reads have the potential to significantly aid the resolution of QTLs to their true underlying causal genetic factors, especially those caused by pangenomic, repetitive, or structural variation.…”