Stable Hypermutators Revealed by the Genomic Landscape of Genes Involved in Genome Stability Among Yeast Species
Mutator phenotypes are short-lived due to the rapid accumulation of deleterious mutations. Yet, recent observations reveal that certain fungi can undergo prolonged accelerated evolution after losing genes involved in DNA repair. Here, we surveyed 1,154 yeast genomes representing nearly all known yeast species of the subphylum Saccharomycotina (phylum Ascomycota) to examine the relationship between reduced gene repertoires broadly associated with genome stability functions (eg DNA repair, cell cycle) and elevated evolutionary rates. We identified 3 distantly related lineages-encompassing 12% of species-that had both the most streamlined sets of genes involved in genome stability (specifically DNA repair) and the highest evolutionary rates in the entire subphylum. Two of these "faster-evolving lineages" (FELs)-a subclade within the order Pichiales and the Wickerhamiella/Starmerella (W/S) clade (order Dipodascales)-are described here for the first time, while the third corresponds to a previously documented Hanseniaspora FEL. Examination of genome stability gene repertoires revealed a set of genes predominantly absent in these 3 FELs, suggesting a potential role in the observed acceleration of evolutionary rates. In the W/S clade, genomic signatures are consistent with a substantial mutational burden, including pronounced A|T bias and endogenous DNA damage. Interestingly, we found that the W/S clade also contains DNA repair genes possibly acquired through horizontal gene transfer, including a photolyase of bacterial origin. These findings highlight how hypermutators can persist across macroevolutionary timescales, potentially linked to the loss of genes related to genome stability, with horizontal gene transfer as a possible avenue for partial functional compensation.
Authors
- Marizeth Groenewald (ORCID: https://orcid.org/0000-0003-0835-5925)
- Carla Gonçalves (ORCID: https://orcid.org/0000-0002-0420-4970)
- Dana A. Opulente (ORCID: https://orcid.org/0000-0003-3224-7510)
- John F. Wolters (ORCID: https://orcid.org/0000-0002-5477-4250)
- Marie‐Claire Harrison (ORCID: https://orcid.org/0000-0002-3013-9906)
- Antonis Rokas (ORCID: https://orcid.org/0000-0002-7248-6551)
- Chris Todd Hittinger (ORCID: https://orcid.org/0000-0001-5088-7461)
- Jacob L. Steenwyk (ORCID: https://orcid.org/0000-0002-8436-595X)
- Abigail L. LaBella (ORCID: https://orcid.org/0000-0003-0068-6703)
- Xing‐Xing Shen (ORCID: https://orcid.org/0000-0001-5765-1419)
- Xiaofan Zhou (ORCID: https://orcid.org/0000-0002-2879-6317)
- David C. Rinker (ORCID: https://orcid.org/0000-0001-5894-7633)
- Shay Covo
Institutions
- South China Agricultural University (CN)
- University of North Carolina at Charlotte (US)
- Howard Hughes Medical Institute (US)
- University of Wisconsin–Madison (US)
- Hebrew University of Jerusalem (IL)
- Vanderbilt University (US)
- Great Lakes Bioenergy Research Center (US)
- Westerdijk Fungal Biodiversity Institute (NL)
- Zhejiang University (CN)
- Villanova University (US)
- Universidade Nova de Lisboa (PT)
- University of California, Berkeley (US)
Publication Details
- Journal
- Molecular Biology and Evolution
- Published
- 2025-10-29
- DOI
- https://doi.org/10.1093/molbev/msaf285
- Citations
- 1
- Primary Topic
- Fungal and yeast genetics research
- Type
- article
- Field-Weighted Citation Impact
- 0.81
Funders
- National Science Foundation
- U.S. Department of Energy
- U.S. Department of Agriculture
- Vanderbilt University
- Life Sciences Research Foundation
- National Institutes of Health
- National Institute of Food and Agriculture
- Office of Science
- Great Lakes Bioenergy Research Center
- Fundação para a Ciência e a Tecnologia
- Fundamental Research Funds for the Central Universities
- National Science Fund for Distinguished Young Scholars
- National Institute of Allergy and Infectious Diseases
- Division of Graduate Education
- Science Fund for Distinguished Young Scholars of Zhejiang Province