Diverse signatures of convergent evolution in cactus-associated yeasts

Gonçalves, Carla; Harrison, Marie-Claire; Steenwyk, Jacob L.; Opulente, Dana A.; LaBella, Abigail L.; Wolters, John F.; Zhou, Xiaofan; Shen, Xing-Xing; Groenewald, Marizeth; Hittinger, Chris Todd; Rokas, Antonis

doi:10.1371/journal.pbio.3002832

Diverse signatures of convergent evolution in cactus-associated yeasts

Journal Article · Mon Sep 23 00:00:00 EDT 2024 · PLoS Biology (Online)

DOI:https://doi.org/10.1371/journal.pbio.3002832· OSTI ID:2473023

Gonçalves, Carla ^[1]; Harrison, Marie-Claire ^[2]; Steenwyk, Jacob L. ^[3]; Opulente, Dana A. ^[4]; LaBella, Abigail L. ^[5]; Wolters, John F. ^[6]; Zhou, Xiaofan ^[7]; Shen, Xing-Xing ^[8]; Groenewald, Marizeth ^[9]; Hittinger, Chris Todd ^[6]; ^[2]

Vanderbilt University, Nashville, TN (United States); Universidade Nova de Lisboa, Caparica (Portugal); Vanderbilt University Department of Biological Sciences
Vanderbilt University, Nashville, TN (United States)
Vanderbilt University, Nashville, TN (United States); University of California, Berkeley, CA (United States)
University of Wisconsin-Madison, WI (United States); Villanova University, PA (United States)
Vanderbilt University, Nashville, TN (United States); University of North Carolina at Charlotte, NC (United States)
University of Wisconsin-Madison, WI (United States)
Vanderbilt University, Nashville, TN (United States); South China Agricultural University, Guangzhou (China)
Vanderbilt University, Nashville, TN (United States); Zhejiang University, Hangzhou (China)
Westerdijk Fungal Biodiversity Institute, Utrecht (The Netherlands)

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.

View Accepted Manuscript (DOE)

Research Organization:: Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); National Institutes of Health/National Institute of Allergy and Infectious Diseases; National Key R&D Program of China; National Science Foundation for Distinguished Young Scholars of Zhejiang Province; Fundamental Research Funds for the Central Universities; National Institutes of Health (NIH); Federation of European Microbiological Societies

Grant/Contract Number:: SC0018409

OSTI ID:: 2473023

Journal Information:: PLoS Biology (Online), Journal Name: PLoS Biology (Online) Journal Issue: 9 Vol. 22; ISSN 1545-7885

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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