The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps

Detalhes bibliográficos
Autor(a) principal: João Barroso-Batista
Data de Publicação: 2014
Outros Autores: Ana Sousa, Marta Lourenço, Marie-Louise Bergman, Jocelyne Demengeot, Karina B. Xavier, Isabel Gordo
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10400.7/319
Resumo: The accumulation of adaptive mutations is essential for survival in novel environments. However, in clonal populations with a high mutational supply, the power of natural selection is expected to be limited. This is due to clonal interference - the competition of clones carrying different beneficial mutations - which leads to the loss of many small effect mutations and fixation of large effect ones. If interference is abundant, then mechanisms for horizontal transfer of genes, which allow the immediate combination of beneficial alleles in a single background, are expected to evolve. However, the relevance of interference in natural complex environments, such as the gut, is poorly known. To address this issue, we studied the invasion of beneficial mutations responsible for Escherichia coli's adaptation to the mouse gut and demonstrate the pervasiveness of clonal interference. The observed dynamics of change in frequency of beneficial mutations are consistent with soft sweeps, where a similar adaptive mutation arises repeatedly on different haplotypes without reaching fixation. The genetic basis of the adaptive mutations revealed a striking parallelism in independently evolving populations. This was mainly characterized by the insertion of transposable elements in both coding and regulatory regions of a few genes. Interestingly in most populations, we observed a complete phenotypic sweep without loss of genetic variation. The intense clonal interference during adaptation to the gut environment, here demonstrated, may be important for our understanding of the levels of strain diversity of E. coli inhabiting the human gut microbiota and of its recombination rate.
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spelling The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweepsQuantitative Biology - Populations and EvolutionCloningThe accumulation of adaptive mutations is essential for survival in novel environments. However, in clonal populations with a high mutational supply, the power of natural selection is expected to be limited. This is due to clonal interference - the competition of clones carrying different beneficial mutations - which leads to the loss of many small effect mutations and fixation of large effect ones. If interference is abundant, then mechanisms for horizontal transfer of genes, which allow the immediate combination of beneficial alleles in a single background, are expected to evolve. However, the relevance of interference in natural complex environments, such as the gut, is poorly known. To address this issue, we studied the invasion of beneficial mutations responsible for Escherichia coli's adaptation to the mouse gut and demonstrate the pervasiveness of clonal interference. The observed dynamics of change in frequency of beneficial mutations are consistent with soft sweeps, where a similar adaptive mutation arises repeatedly on different haplotypes without reaching fixation. The genetic basis of the adaptive mutations revealed a striking parallelism in independently evolving populations. This was mainly characterized by the insertion of transposable elements in both coding and regulatory regions of a few genes. Interestingly in most populations, we observed a complete phenotypic sweep without loss of genetic variation. The intense clonal interference during adaptation to the gut environment, here demonstrated, may be important for our understanding of the levels of strain diversity of E. coli inhabiting the human gut microbiota and of its recombination rate.Howard Hughes Medical Institute (HHMI-55007436), LAO/ITQB, FCT Grants: FRH/BD/80257/2011 and SFRH/BPD/14299/2003.PLOSARCAJoão Barroso-BatistaAna SousaMarta LourençoMarie-Louise BergmanJocelyne DemengeotKarina B. XavierIsabel Gordo2015-09-28T16:38:13Z2014-03-062014-03-06T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.7/319engBarroso-Batista J, Sousa A, Lourenço M, Bergman M-L, Sobral D, Demengeot J, et al. (2014) The First Steps of Adaptation of Escherichia coli to the Gut Are Dominated by Soft Sweeps. PLoS Genet 10(3): e1004182. doi:10.1371/journal.pgen.100418210.1371/journal.pgen.1004182info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2022-11-29T14:34:43Zoai:arca.igc.gulbenkian.pt:10400.7/319Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T16:11:38.273926Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps
title The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps
spellingShingle The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps
João Barroso-Batista
Quantitative Biology - Populations and Evolution
Cloning
title_short The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps
title_full The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps
title_fullStr The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps
title_full_unstemmed The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps
title_sort The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps
author João Barroso-Batista
author_facet João Barroso-Batista
Ana Sousa
Marta Lourenço
Marie-Louise Bergman
Jocelyne Demengeot
Karina B. Xavier
Isabel Gordo
author_role author
author2 Ana Sousa
Marta Lourenço
Marie-Louise Bergman
Jocelyne Demengeot
Karina B. Xavier
Isabel Gordo
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv ARCA
dc.contributor.author.fl_str_mv João Barroso-Batista
Ana Sousa
Marta Lourenço
Marie-Louise Bergman
Jocelyne Demengeot
Karina B. Xavier
Isabel Gordo
dc.subject.por.fl_str_mv Quantitative Biology - Populations and Evolution
Cloning
topic Quantitative Biology - Populations and Evolution
Cloning
description The accumulation of adaptive mutations is essential for survival in novel environments. However, in clonal populations with a high mutational supply, the power of natural selection is expected to be limited. This is due to clonal interference - the competition of clones carrying different beneficial mutations - which leads to the loss of many small effect mutations and fixation of large effect ones. If interference is abundant, then mechanisms for horizontal transfer of genes, which allow the immediate combination of beneficial alleles in a single background, are expected to evolve. However, the relevance of interference in natural complex environments, such as the gut, is poorly known. To address this issue, we studied the invasion of beneficial mutations responsible for Escherichia coli's adaptation to the mouse gut and demonstrate the pervasiveness of clonal interference. The observed dynamics of change in frequency of beneficial mutations are consistent with soft sweeps, where a similar adaptive mutation arises repeatedly on different haplotypes without reaching fixation. The genetic basis of the adaptive mutations revealed a striking parallelism in independently evolving populations. This was mainly characterized by the insertion of transposable elements in both coding and regulatory regions of a few genes. Interestingly in most populations, we observed a complete phenotypic sweep without loss of genetic variation. The intense clonal interference during adaptation to the gut environment, here demonstrated, may be important for our understanding of the levels of strain diversity of E. coli inhabiting the human gut microbiota and of its recombination rate.
publishDate 2014
dc.date.none.fl_str_mv 2014-03-06
2014-03-06T00:00:00Z
2015-09-28T16:38:13Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10400.7/319
url http://hdl.handle.net/10400.7/319
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Barroso-Batista J, Sousa A, Lourenço M, Bergman M-L, Sobral D, Demengeot J, et al. (2014) The First Steps of Adaptation of Escherichia coli to the Gut Are Dominated by Soft Sweeps. PLoS Genet 10(3): e1004182. doi:10.1371/journal.pgen.1004182
10.1371/journal.pgen.1004182
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
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dc.publisher.none.fl_str_mv PLOS
publisher.none.fl_str_mv PLOS
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
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reponame_str Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
collection Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository.name.fl_str_mv Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
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