Extensive sampling of Saccharomyces cerevisiae in Taiwan reveals ecology and evolution of predomesticated lineages
- Tracy Jiaye Lee1,2,3,
- Yu-Ching Liu1,
- Wei-An Liu1,
- Yu-Fei Lin1,
- Hsin-Han Lee1,4,5,
- Huei-Mien Ke1,
- Jen-Pan Huang1,
- Mei-Yeh Jade Lu1,
- Chia-Lun Hsieh1,
- Kuo-Fang Chung1,
- Gianni Liti6 and
- Isheng Jason Tsai1,2,3,4,5
- 1Biodiversity Research Center, Academia Sinica, 115 Taipei, Taiwan;
- 2Biodiversity Program, Taiwan International Graduate Program, Academia Sinica and National Taiwan Normal University, 115 Taipei, Taiwan;
- 3Department of Life Science, National Taiwan Normal University, 116 Taipei, Taiwan;
- 4Bioinformatics Program, Taiwan International Graduate Program, National Taiwan University, 106 Taipei, Taiwan;
- 5Bioinformatics Program, Institute of Information Science, Taiwan International Graduate Program, Academia Sinica, 115 Taipei, Taiwan;
- 6Université Côte d'Azur, CNRS, INSERM, IRCAN, 06107 Nice, France
Abstract
The ecology and genetic diversity of the model yeast Saccharomyces cerevisiae before 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 broadleaf 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 the 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 that 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.
Footnotes
-
[Supplemental material is available for this article.]
-
Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.276286.121.
-
Freely available online through the Genome Research Open Access option.
- Received October 13, 2021.
- Accepted March 25, 2022.
This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
