Impact of Homologous Recombination on the Evolution of Prokaryotic Core Genomes

ABSTRACT Homologous recombination (HR) enables the exchange of genetic material between and within species. Recent studies suggest that this process plays a major role in the microevolution of microbial genomes, contributing to core genome homogenization and to the maintenance of cohesive population...

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Autores principales:	Pedro González-Torres, Francisco Rodríguez-Mateos, Josefa Antón, Toni Gabaldón
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	comparative genomics core genomes genome evolution intraspecific diversity homologous recombination Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e2295809a8684e6e9534a1ccfa3cb200
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spelling	oai:doaj.org-article:e2295809a8684e6e9534a1ccfa3cb2002021-11-15T15:55:14ZImpact of Homologous Recombination on the Evolution of Prokaryotic Core Genomes10.1128/mBio.02494-182150-7511https://doaj.org/article/e2295809a8684e6e9534a1ccfa3cb2002019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02494-18https://doaj.org/toc/2150-7511ABSTRACT Homologous recombination (HR) enables the exchange of genetic material between and within species. Recent studies suggest that this process plays a major role in the microevolution of microbial genomes, contributing to core genome homogenization and to the maintenance of cohesive population structures. However, we still have a very poor understanding of the possible adaptive roles of intraspecific HR and of the factors that determine its differential impact across clades and lifestyles. Here we used a unified methodological framework to assess HR in 338 complete genomes from 54 phylogenetically diverse and representative prokaryotic species, encompassing different lifestyles and a broad phylogenetic distribution. Our results indicate that lifestyle and presence of restriction-modification (RM) machineries are among the main factors shaping HR patterns, with symbionts and intracellular pathogens having the lowest HR levels. Similarly, the size of exchanged genomic fragments correlated with the presence of RM and competence machineries. Finally, genes exchanged by HR showed functional enrichments which could be related to adaptations to different environments and ecological strategies. Taken together, our results clarify the factors underlying HR impact and suggest important adaptive roles of genes exchanged through this mechanism. Our results also revealed that the extent of genetic exchange correlated with lifestyle and some genomic features. Moreover, the genes in exchanged regions were enriched for functions that reflected specific adaptations, supporting identification of HR as one of the main evolutionary mechanisms shaping prokaryotic core genomes. IMPORTANCE Microbial populations exchange genetic material through a process called homologous recombination. Although this process has been studied in particular organisms, we lack an understanding of its differential impact over the genome and across microbes with different life-styles. We used a common analytical framework to assess this process in a representative set of microorganisms. Our results uncovered important trends. First, microbes with different lifestyles are differentially impacted, with endosymbionts and obligate pathogens being those less prone to undergo this process. Second, certain genetic elements such as restriction-modification systems seem to be associated with higher rates of recombination. Most importantly, recombined genomes show the footprints of natural selection in which recombined regions preferentially contain genes that can be related to specific ecological adaptations. Taken together, our results clarify the relative contributions of factors modulating homologous recombination and show evidence for a clear a role of this process in shaping microbial genomes and driving ecological adaptations.Pedro González-TorresFrancisco Rodríguez-MateosJosefa AntónToni GabaldónAmerican Society for Microbiologyarticlecomparative genomicscore genomesgenome evolutionintraspecific diversityhomologous recombinationMicrobiologyQR1-502ENmBio, Vol 10, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	comparative genomics core genomes genome evolution intraspecific diversity homologous recombination Microbiology QR1-502
spellingShingle	comparative genomics core genomes genome evolution intraspecific diversity homologous recombination Microbiology QR1-502 Pedro González-Torres Francisco Rodríguez-Mateos Josefa Antón Toni Gabaldón Impact of Homologous Recombination on the Evolution of Prokaryotic Core Genomes
description	ABSTRACT Homologous recombination (HR) enables the exchange of genetic material between and within species. Recent studies suggest that this process plays a major role in the microevolution of microbial genomes, contributing to core genome homogenization and to the maintenance of cohesive population structures. However, we still have a very poor understanding of the possible adaptive roles of intraspecific HR and of the factors that determine its differential impact across clades and lifestyles. Here we used a unified methodological framework to assess HR in 338 complete genomes from 54 phylogenetically diverse and representative prokaryotic species, encompassing different lifestyles and a broad phylogenetic distribution. Our results indicate that lifestyle and presence of restriction-modification (RM) machineries are among the main factors shaping HR patterns, with symbionts and intracellular pathogens having the lowest HR levels. Similarly, the size of exchanged genomic fragments correlated with the presence of RM and competence machineries. Finally, genes exchanged by HR showed functional enrichments which could be related to adaptations to different environments and ecological strategies. Taken together, our results clarify the factors underlying HR impact and suggest important adaptive roles of genes exchanged through this mechanism. Our results also revealed that the extent of genetic exchange correlated with lifestyle and some genomic features. Moreover, the genes in exchanged regions were enriched for functions that reflected specific adaptations, supporting identification of HR as one of the main evolutionary mechanisms shaping prokaryotic core genomes. IMPORTANCE Microbial populations exchange genetic material through a process called homologous recombination. Although this process has been studied in particular organisms, we lack an understanding of its differential impact over the genome and across microbes with different life-styles. We used a common analytical framework to assess this process in a representative set of microorganisms. Our results uncovered important trends. First, microbes with different lifestyles are differentially impacted, with endosymbionts and obligate pathogens being those less prone to undergo this process. Second, certain genetic elements such as restriction-modification systems seem to be associated with higher rates of recombination. Most importantly, recombined genomes show the footprints of natural selection in which recombined regions preferentially contain genes that can be related to specific ecological adaptations. Taken together, our results clarify the relative contributions of factors modulating homologous recombination and show evidence for a clear a role of this process in shaping microbial genomes and driving ecological adaptations.
format	article
author	Pedro González-Torres Francisco Rodríguez-Mateos Josefa Antón Toni Gabaldón
author_facet	Pedro González-Torres Francisco Rodríguez-Mateos Josefa Antón Toni Gabaldón
author_sort	Pedro González-Torres
title	Impact of Homologous Recombination on the Evolution of Prokaryotic Core Genomes
title_short	Impact of Homologous Recombination on the Evolution of Prokaryotic Core Genomes
title_full	Impact of Homologous Recombination on the Evolution of Prokaryotic Core Genomes
title_fullStr	Impact of Homologous Recombination on the Evolution of Prokaryotic Core Genomes
title_full_unstemmed	Impact of Homologous Recombination on the Evolution of Prokaryotic Core Genomes
title_sort	impact of homologous recombination on the evolution of prokaryotic core genomes
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/e2295809a8684e6e9534a1ccfa3cb200
work_keys_str_mv	AT pedrogonzaleztorres impactofhomologousrecombinationontheevolutionofprokaryoticcoregenomes AT franciscorodriguezmateos impactofhomologousrecombinationontheevolutionofprokaryoticcoregenomes AT josefaanton impactofhomologousrecombinationontheevolutionofprokaryoticcoregenomes AT tonigabaldon impactofhomologousrecombinationontheevolutionofprokaryoticcoregenomes
_version_	1718427248537632768

Impact of Homologous Recombination on the Evolution of Prokaryotic Core Genomes

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