Diverse signatures of convergent evolution in cactus-associated yeasts
Many distantly related organisms have convergently evolved traits and lifestyles that enable them to live in similar ecological environments. However, the extent of phenotypic convergence evolving through the same or distinct genetic trajectories remains an open question. Here, we leverage a comprehensive dataset of genomic and phenotypic data from 1,049 yeast species in the subphylum Saccharomycotina (Kingdom Fungi, Phylum Ascomycota) to explore signatures of convergent evolution in cactophilic yeasts, ecological specialists associated with cacti. We inferred that the ecological association of yeasts with cacti arose independently approximately 17 times. Using a machine learning-based approach, we further found that cactophily can be predicted with 76% accuracy from both functional genomic and phenotypic data. The most informative feature for predicting cactophily was thermotolerance, which we found to be likely associated with altered evolutionary rates of genes impacting the cell envelope in several cactophilic lineages. We also identified horizontal gene transfer and duplication events of plant cell wall-degrading enzymes in distantly related cactophilic clades, suggesting that putatively adaptive traits evolved independently through disparate molecular mechanisms. Notably, we found that multiple cactophilic species and their close relatives have been reported as emerging human opportunistic pathogens, suggesting that the cactophilic lifestyle-and perhaps more generally lifestyles favoring thermotolerance-might preadapt yeasts to cause human disease. This work underscores the potential of a multifaceted approach involving high-throughput genomic and phenotypic data to shed light onto ecological adaptation and highlights how convergent evolution to wild environments could facilitate the transition to human pathogenicity.
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)
- Xiaofan Zhou
- 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)
Institutions
- South China Agricultural University (CN)
- University of North Carolina at Charlotte (US)
- Howard Hughes Medical Institute (US)
- 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
- PLoS Biology
- Published
- 2024-09-23
- DOI
- https://doi.org/10.1371/journal.pbio.3002832
- Citations
- 13
- Primary Topic
- Yeasts and Rust Fungi Studies
- Type
- article
- Field-Weighted Citation Impact
- 3.04
Funders
- National Science Foundation
- U.S. Department of Energy
- U.S. Department of Agriculture
- Burroughs Wellcome Fund
- Wisconsin Alumni Research Foundation
- Vanderbilt University
- Life Sciences Research Foundation
- Federation of European Microbiological Societies
- Applied Molecular Biosciences Unit
- 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 Institute of Allergy and Infectious Diseases
- Division of Graduate Education
- Division of Microbiology and Infectious Diseases, National Institute of Allergy and Infectious Diseases
- Science Fund for Distinguished Young Scholars of Zhejiang Province