TY - JOUR
T1 - Diverse signatures of convergent evolution in cactus-associated yeasts
AU - Gonçalves, Carla
AU - Harrison, Marie Claire
AU - Steenwyk, Jacob L.
AU - Opulente, Dana A.
AU - LaBella, Abigail L.
AU - Wolters, John F.
AU - Zhou, Xiaofan
AU - Shen, Xing Xing
AU - Groenewald, Marizeth
AU - Hittinger, Chris Todd
AU - Rokas, Antonis
N1 - Publisher Copyright:
Copyright: © 2024 Gonçalves et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
PY - 2024/9
Y1 - 2024/9
N2 - AU Many: Pleaseconfirmthatallheadinglevelsarerepresentedcorrectly 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 approximatelyAU 17 times.: PleasenotethatasperPLOSstyle Using a machine learning–based ; donotusethesymbol approach, we inprosetomeanabo 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.
AB - AU Many: Pleaseconfirmthatallheadinglevelsarerepresentedcorrectly 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 approximatelyAU 17 times.: PleasenotethatasperPLOSstyle Using a machine learning–based ; donotusethesymbol approach, we inprosetomeanabo 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.
UR - http://www.scopus.com/inward/record.url?scp=85204673470&partnerID=8YFLogxK
U2 - 10.1371/journal.pbio.3002832
DO - 10.1371/journal.pbio.3002832
M3 - Article
C2 - 39312572
AN - SCOPUS:85204673470
SN - 1544-9173
VL - 22
JO - PLoS Biology
JF - PLoS Biology
IS - 9
M1 - e3002832
ER -