Evolution of plasmid mobility: origin and fate of conjugative and nonconjugative plasmids

Conjugation drives the horizontal transfer of adaptive traits across prokaryotes. One-fourth of the plasmids encode the functions necessary to conjugate autonomously, the others being eventually mobilizable by conjugation. To understand the evolution of plasmid mobility, we studied plasmid size, gen...

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Detalles Bibliográficos
Autores: Coluzzi, Charles, Garcillán Barcia, María del Pilar, Cruz, Fernando de la|||0000-0003-4758-6857, Rocha, Eduardo P.C.
Tipo de recurso: artículo
Fecha de publicación:2022
País:España
Institución:Universidad de Cantabria (UC)
Repositorio:UCrea Repositorio Abierto de la Universidad de Cantabria
Idioma:inglés
OAI Identifier:oai:repositorio.unican.es:10902/25170
Acceso en línea:http://hdl.handle.net/10902/25170
Access Level:acceso abierto
Palabra clave:Plasmids
Conjugation
Horizontal gene transfer
Bacteria
Genomes
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spelling Evolution of plasmid mobility: origin and fate of conjugative and nonconjugative plasmidsColuzzi, CharlesGarcillán Barcia, María del PilarCruz, Fernando de la|||0000-0003-4758-6857Rocha, Eduardo P.C.PlasmidsConjugationHorizontal gene transferBacteriaGenomesConjugation drives the horizontal transfer of adaptive traits across prokaryotes. One-fourth of the plasmids encode the functions necessary to conjugate autonomously, the others being eventually mobilizable by conjugation. To understand the evolution of plasmid mobility, we studied plasmid size, gene repertoires, and conjugation-related genes. Plasmid gene repertoires were found to vary rapidly in relation to the evolutionary rate of relaxases, for example, most pairs of plasmids with 95% identical relaxases have fewer than 50% of homologs. Among 249 recent transitions of mobility type, we observed a clear excess of plasmids losing the capacity to conjugate. These transitions are associated with even greater changes in gene repertoires, possibly mediated by transposable elements, including pseudogenization of the conjugation locus, exchange of replicases reducing the problem of incompatibility, and extensive loss of other genes. At the microevolutionary scale of plasmid taxonomy, transitions of mobility type sometimes result in the creation of novel taxonomic units. Interestingly, most transitions from conjugative to mobilizable plasmids seem to be lost in the long term. This suggests a source-sink dynamic, where conjugative plasmids generate nonconjugative plasmids that tend to be poorly adapted and are frequently lost. Still, in some cases, these relaxases seem to have evolved to become efficient at plasmid mobilization in trans, possibly by hijacking multiple conjugative systems. This resulted in specialized relaxases of mobilizable plasmids. In conclusion, the evolution of plasmid mobility is frequent, shapes the patterns of gene flow in bacteria, the dynamics of gene repertoires, and the ecology of plasmids.Acknowledgements: Eugen Pfeifer for providing the wGRR data and Marie Touchon for providing the ISEScan analysis. Manuel Ares-Arroyo for comments and suggestions. Jorge Moura de Sousa, Matthieu Haudiquet, and Olaya Rendueles-Garcia for scientific discussions. INCEPTION project (PIA/ANR-16-CONV-0005), Equipe FRM (EQU201903007835), Laboratoire d’Excellence IBEID (ANR-10-LABX-62-IBEID) to E.P.C.R. and C.C. PID2020-117923GB-I00 project funded by Spanish Ministry of Science and Innovation to FdlC and MPG-B.Oxford University PressUniversidad de Cantabria20222022-01-01journal articlehttp://purl.org/coar/resource_type/c_6501NAhttp://purl.org/coar/version/c_be7fb7dd8ff6fe43info:eu-repo/semantics/articlehttp://hdl.handle.net/10902/25170Molecular Biology and Evolution, 2022, 39(6), msac115reponame:UCrea Repositorio Abierto de la Universidad de Cantabriainstname:Universidad de Cantabria (UC)Inglésengopen accesshttp://purl.org/coar/access_right/c_abf2Attribution-NonCommercial 4.0 Internationalhttp://creativecommons.org/licenses/by-nc/4.0/info:eu-repo/semantics/openAccessoai:repositorio.unican.es:10902/251702026-06-02T12:39:31Z
dc.title.none.fl_str_mv Evolution of plasmid mobility: origin and fate of conjugative and nonconjugative plasmids
title Evolution of plasmid mobility: origin and fate of conjugative and nonconjugative plasmids
spellingShingle Evolution of plasmid mobility: origin and fate of conjugative and nonconjugative plasmids
Coluzzi, Charles
Plasmids
Conjugation
Horizontal gene transfer
Bacteria
Genomes
title_short Evolution of plasmid mobility: origin and fate of conjugative and nonconjugative plasmids
title_full Evolution of plasmid mobility: origin and fate of conjugative and nonconjugative plasmids
title_fullStr Evolution of plasmid mobility: origin and fate of conjugative and nonconjugative plasmids
title_full_unstemmed Evolution of plasmid mobility: origin and fate of conjugative and nonconjugative plasmids
title_sort Evolution of plasmid mobility: origin and fate of conjugative and nonconjugative plasmids
dc.creator.none.fl_str_mv Coluzzi, Charles
Garcillán Barcia, María del Pilar
Cruz, Fernando de la|||0000-0003-4758-6857
Rocha, Eduardo P.C.
author Coluzzi, Charles
author_facet Coluzzi, Charles
Garcillán Barcia, María del Pilar
Cruz, Fernando de la|||0000-0003-4758-6857
Rocha, Eduardo P.C.
author_role author
author2 Garcillán Barcia, María del Pilar
Cruz, Fernando de la|||0000-0003-4758-6857
Rocha, Eduardo P.C.
author2_role author
author
author
dc.contributor.none.fl_str_mv Universidad de Cantabria
dc.subject.none.fl_str_mv Plasmids
Conjugation
Horizontal gene transfer
Bacteria
Genomes
topic Plasmids
Conjugation
Horizontal gene transfer
Bacteria
Genomes
description Conjugation drives the horizontal transfer of adaptive traits across prokaryotes. One-fourth of the plasmids encode the functions necessary to conjugate autonomously, the others being eventually mobilizable by conjugation. To understand the evolution of plasmid mobility, we studied plasmid size, gene repertoires, and conjugation-related genes. Plasmid gene repertoires were found to vary rapidly in relation to the evolutionary rate of relaxases, for example, most pairs of plasmids with 95% identical relaxases have fewer than 50% of homologs. Among 249 recent transitions of mobility type, we observed a clear excess of plasmids losing the capacity to conjugate. These transitions are associated with even greater changes in gene repertoires, possibly mediated by transposable elements, including pseudogenization of the conjugation locus, exchange of replicases reducing the problem of incompatibility, and extensive loss of other genes. At the microevolutionary scale of plasmid taxonomy, transitions of mobility type sometimes result in the creation of novel taxonomic units. Interestingly, most transitions from conjugative to mobilizable plasmids seem to be lost in the long term. This suggests a source-sink dynamic, where conjugative plasmids generate nonconjugative plasmids that tend to be poorly adapted and are frequently lost. Still, in some cases, these relaxases seem to have evolved to become efficient at plasmid mobilization in trans, possibly by hijacking multiple conjugative systems. This resulted in specialized relaxases of mobilizable plasmids. In conclusion, the evolution of plasmid mobility is frequent, shapes the patterns of gene flow in bacteria, the dynamics of gene repertoires, and the ecology of plasmids.
publishDate 2022
dc.date.none.fl_str_mv 2022
2022-01-01
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
NA
http://purl.org/coar/version/c_be7fb7dd8ff6fe43
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/10902/25170
url http://hdl.handle.net/10902/25170
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
Attribution-NonCommercial 4.0 International
http://creativecommons.org/licenses/by-nc/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
Attribution-NonCommercial 4.0 International
http://creativecommons.org/licenses/by-nc/4.0/
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv Molecular Biology and Evolution, 2022, 39(6), msac115
reponame:UCrea Repositorio Abierto de la Universidad de Cantabria
instname:Universidad de Cantabria (UC)
instname_str Universidad de Cantabria (UC)
reponame_str UCrea Repositorio Abierto de la Universidad de Cantabria
collection UCrea Repositorio Abierto de la Universidad de Cantabria
repository.name.fl_str_mv
repository.mail.fl_str_mv
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