Diverse signatures of convergent evolution in cacti-associated yeasts.

adaptive evolution cactophily convergent evolution machine learning pathogenicity thermotolerance yeast ecology

Journal

bioRxiv : the preprint server for biology
Titre abrégé: bioRxiv
Pays: United States
ID NLM: 101680187

Informations de publication

Date de publication:
17 Sep 2023
Historique:
pubmed: 25 9 2023
medline: 25 9 2023
entrez: 25 9 2023
Statut: epublish

Résumé

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 ~17 times. Using machine-learning, we further found that cactophily can be predicted with 76% accuracy from functional genomic and phenotypic data. The most informative feature for predicting cactophily was thermotolerance, which is likely associated with duplication and 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 through disparate molecular mechanisms. Remarkably, multiple cactophilic lineages and their close relatives are emerging human opportunistic pathogens, suggesting that the cactophilic lifestyle-and perhaps more generally lifestyles favoring thermotolerance-may 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.

Identifiants

pubmed: 37745407
doi: 10.1101/2023.09.14.557833
pmc: PMC10515907
pii:
doi:

Types de publication

Preprint

Langues

eng

Subventions

Organisme : NIAID NIH HHS
ID : R01 AI153356
Pays : United States
Organisme : NHGRI NIH HHS
ID : T32 HG002760
Pays : United States

Déclaration de conflit d'intérêts

Conflicts of interest JLS is a scientific advisor for WittGen Biotechnologies. JLS is an advisor for ForensisGroup Inc. AR is a scientific consultant for LifeMine Therapeutics, Inc.

Auteurs

Carla Gonçalves (C)

Vanderbilt University, Department of Biological Sciences, VU Station B #35-1634, Nashville, TN 37235, United States of America.
Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN 37235, USA.
Present address: Associate Laboratory i4HB-Institute for Health and Bioeconomy and UCIBIO-Applied Molecular Biosciences Unit, Department of Life Sciences, NOVA School of Science and Technology, Universidade NOVA de Lisboa, Caparica, Portugal.
Present address: UCIBIO-i4HB, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal.

Marie-Claire Harrison (MC)

Vanderbilt University, Department of Biological Sciences, VU Station B #35-1634, Nashville, TN 37235, United States of America.
Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN 37235, USA.

Jacob L Steenwyk (JL)

Vanderbilt University, Department of Biological Sciences, VU Station B #35-1634, Nashville, TN 37235, United States of America.
Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN 37235, USA.
Howards Hughes Medical Institute and the Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA, USA.

Dana A Opulente (DA)

Laboratory of Genetics, DOE Great Lakes Bioenergy Research Center, Center for Genomic Science Innovation, J. F. Crow Institute for the Study of Evolution, Wisconsin Energy Institu te, University of Wisconsin-Madison, Madison, WI 53726, USA.
Biology Department, Villanova University, Villanova, PA 19085, USA.

Abigail L LaBella (AL)

Vanderbilt University, Department of Biological Sciences, VU Station B #35-1634, Nashville, TN 37235, United States of America.
Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN 37235, USA.
Department of Bioinformatics and Genomics, University of North Carolina at Charlotte, Charlotte NC 28223.

John F Wolters (JF)

Laboratory of Genetics, DOE Great Lakes Bioenergy Research Center, Center for Genomic Science Innovation, J. F. Crow Institute for the Study of Evolution, Wisconsin Energy Institu te, University of Wisconsin-Madison, Madison, WI 53726, USA.

Xiaofan Zhou (X)

Vanderbilt University, Department of Biological Sciences, VU Station B #35-1634, Nashville, TN 37235, United States of America.
Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN 37235, USA.
Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou 510642, China.

Xing-Xing Shen (XX)

Vanderbilt University, Department of Biological Sciences, VU Station B #35-1634, Nashville, TN 37235, United States of America.
Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN 37235, USA.
College of Agriculture and Biotechnology and Centre for Evolutionary & Organismal Biology, Zhejiang University, Hangzhou 310058, China.

Marizeth Groenewald (M)

Westerdijk Fungal Biodiversity Institute, 3584 Utrecht, The Netherlands.

Chris Todd Hittinger (CT)

Laboratory of Genetics, DOE Great Lakes Bioenergy Research Center, Center for Genomic Science Innovation, J. F. Crow Institute for the Study of Evolution, Wisconsin Energy Institu te, University of Wisconsin-Madison, Madison, WI 53726, USA.

Antonis Rokas (A)

Vanderbilt University, Department of Biological Sciences, VU Station B #35-1634, Nashville, TN 37235, United States of America.
Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN 37235, USA.

Classifications MeSH