Gene gain and loss push prokaryotes beyond the homologous recombination barrier and accelerate genome sequence divergence

Bacterial and archaeal evolution involve extensive gene gain and loss. Thus, phylogenetic trees of prokaryotes can be constructed both by traditional sequence-based methods (gene trees) and by comparison of gene compositions (genome trees). Comparing the branch lengths in gene and genome trees with...

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Authors: Iranzo, Jaime, Wolf, Yuri I., Koonin, Eugene V., Sela, Itamar
Format: article
Status:Published version
Publication Date:2019
Country:España
Institution:Consejo Superior de Investigaciones Científicas (CSIC)
Repository:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/346217
Online Access:http://hdl.handle.net/10261/346217
Access Level:Open access
Keyword:Evolutionary genetics
Evolutionary theory
Genome evolution
Microbial genetics
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spelling Gene gain and loss push prokaryotes beyond the homologous recombination barrier and accelerate genome sequence divergenceIranzo, JaimeWolf, Yuri I.Koonin, Eugene V.Sela, ItamarEvolutionary geneticsEvolutionary theoryGenome evolutionMicrobial geneticsBacterial and archaeal evolution involve extensive gene gain and loss. Thus, phylogenetic trees of prokaryotes can be constructed both by traditional sequence-based methods (gene trees) and by comparison of gene compositions (genome trees). Comparing the branch lengths in gene and genome trees with identical topologies for 34 clusters of closely related bacterial and archaeal genomes, we show here that terminal branches of gene trees are systematically compressed compared to those of genome trees. Thus, sequence evolution is delayed compared to genome evolution by gene gain and loss. The extent of this delay differs widely among bacteria and archaea. Mathematical modeling shows that the divergence delay can result from sequence homogenization by homologous recombination. The model explains how homologous recombination maintains the cohesiveness of the core genome of a species while allowing extensive gene gain and loss within the accessory genome. Once evolving genomes become isolated by barriers impeding homologous recombination, gene and genome evolution processes settle into parallel trajectories, and genomes diverge, resulting in speciation.The authors’ research is supported by intramural research program funds of the National Institutes of Health (National Library of Medicine). J.I. is funded by the “Ramón y Cajal Program” from the Spanish Ministry of Science and Innovation and by the “Severo Ochoa Program for Centres of Excellence in R&D” from the Agencia Estatal de Investigación of Spain (grant SEV-2016-0672 (2017–2021) to the CBGP).Peer reviewedSpringer NatureNational Institutes of Health (US)Ministerio de Ciencia e Innovación (España)Agencia Estatal de Investigación (España)Ministerio de Economía y Competitividad (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242019info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/346217reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MINECO//SEV-2016-0672https://doi.org/10.1038/s41467-019-13429-2Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3462172026-05-22T06:33:51Z
dc.title.none.fl_str_mv Gene gain and loss push prokaryotes beyond the homologous recombination barrier and accelerate genome sequence divergence
title Gene gain and loss push prokaryotes beyond the homologous recombination barrier and accelerate genome sequence divergence
spellingShingle Gene gain and loss push prokaryotes beyond the homologous recombination barrier and accelerate genome sequence divergence
Iranzo, Jaime
Evolutionary genetics
Evolutionary theory
Genome evolution
Microbial genetics
title_short Gene gain and loss push prokaryotes beyond the homologous recombination barrier and accelerate genome sequence divergence
title_full Gene gain and loss push prokaryotes beyond the homologous recombination barrier and accelerate genome sequence divergence
title_fullStr Gene gain and loss push prokaryotes beyond the homologous recombination barrier and accelerate genome sequence divergence
title_full_unstemmed Gene gain and loss push prokaryotes beyond the homologous recombination barrier and accelerate genome sequence divergence
title_sort Gene gain and loss push prokaryotes beyond the homologous recombination barrier and accelerate genome sequence divergence
dc.creator.none.fl_str_mv Iranzo, Jaime
Wolf, Yuri I.
Koonin, Eugene V.
Sela, Itamar
author Iranzo, Jaime
author_facet Iranzo, Jaime
Wolf, Yuri I.
Koonin, Eugene V.
Sela, Itamar
author_role author
author2 Wolf, Yuri I.
Koonin, Eugene V.
Sela, Itamar
author2_role author
author
author
dc.contributor.none.fl_str_mv National Institutes of Health (US)
Ministerio de Ciencia e Innovación (España)
Agencia Estatal de Investigación (España)
Ministerio de Economía y Competitividad (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Evolutionary genetics
Evolutionary theory
Genome evolution
Microbial genetics
topic Evolutionary genetics
Evolutionary theory
Genome evolution
Microbial genetics
description Bacterial and archaeal evolution involve extensive gene gain and loss. Thus, phylogenetic trees of prokaryotes can be constructed both by traditional sequence-based methods (gene trees) and by comparison of gene compositions (genome trees). Comparing the branch lengths in gene and genome trees with identical topologies for 34 clusters of closely related bacterial and archaeal genomes, we show here that terminal branches of gene trees are systematically compressed compared to those of genome trees. Thus, sequence evolution is delayed compared to genome evolution by gene gain and loss. The extent of this delay differs widely among bacteria and archaea. Mathematical modeling shows that the divergence delay can result from sequence homogenization by homologous recombination. The model explains how homologous recombination maintains the cohesiveness of the core genome of a species while allowing extensive gene gain and loss within the accessory genome. Once evolving genomes become isolated by barriers impeding homologous recombination, gene and genome evolution processes settle into parallel trajectories, and genomes diverge, resulting in speciation.
publishDate 2019
dc.date.none.fl_str_mv 2019
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/346217
url http://hdl.handle.net/10261/346217
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/MINECO//SEV-2016-0672
https://doi.org/10.1038/s41467-019-13429-2
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Springer Nature
publisher.none.fl_str_mv Springer Nature
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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