Recurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteria

Detalhes bibliográficos
Autor(a) principal: Sousa, Ana
Data de Publicação: 2017
Outros Autores: Ramiro, Ricardo S., Barroso-Batista, João, Güleresi, Daniela, Lourenço, Marta, Gordo, Isabel
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10400.7/873
Resumo: The deposited article is a post-print version and has been submitted to peer review.
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spelling Recurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteriaexperimental evolutionmicrobiotareverse evolutionintrastrain polymorphismnutritional optimizationprecision medicineThe deposited article is a post-print version and has been submitted to peer review.This deposit is composed by the main article plus the supplementary materials of the publication.The evolution of new strains within the gut ecosystem is poorly understood. We used a natural but controlled system to follow the emergence of intraspecies diversity of commensal Escherichia coli, during three rounds of adaptation to the mouse gut (∼1,300 generations). We previously showed that, in the first round, a strongly beneficial phenotype (loss-of-function for galactitol consumption; gat-negative) spread to >90% frequency in all colonized mice. Here, we show that this loss-of-function is repeatedly reversed when a gat-negative clone colonizes new mice. The regain of function occurs via compensatory mutation and reversion, the latter leaving no trace of past adaptation. We further show that loss-of-function adaptive mutants reevolve, after colonization with an evolved gat-positive clone. Thus, even under strong bottlenecks a regime of strong-mutation-strong-selection dominates adaptation. Coupling experiments and modeling, we establish that reverse evolution recurrently generates two coexisting phenotypes within the microbiota that can or not consume galactitol (gat-positive and gat-negative, respectively). Although the abundance of the dominant strain, the gat-negative, depends on the microbiota composition, gat-positive abundance is independent of the microbiota composition and can be precisely manipulated by supplementing the diet with galactitol. These results show that a specific diet is able to change the abundance of specific strains. Importantly, we find polymorphism for these phenotypes in indigenous Enterobacteria of mice and man. Our results demonstrate that natural selection can greatly overwhelm genetic drift at structuring the strain diversity of gut commensals and that competition for limiting resources may be a key mechanism for maintaining polymorphism in the gut.This research received funding from the European Research Council (ERC): ERC-StG-ECOADAPT; University of Cologne-Instituto Gulbenkian de Ciência, under SFB of DFG.Oxford University PressARCASousa, AnaRamiro, Ricardo S.Barroso-Batista, JoãoGüleresi, DanielaLourenço, MartaGordo, Isabel2018-11-01T01:30:09Z2017-112017-11-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfapplication/pdfhttp://hdl.handle.net/10400.7/873engAna Sousa, Ricardo S. Ramiro, João Barroso-Batista, Daniela Güleresi, Marta Lourenço, Isabel Gordo; Recurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteria, Molecular Biology and Evolution, Volume 34, Issue 11, 1 November 2017, Pages 2879–2892, https://doi.org/10.1093/molbev/msx22110.1093/molbev/msx221info:eu-repo/semantics/embargoedAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2022-11-29T14:35:17Zoai:arca.igc.gulbenkian.pt:10400.7/873Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T16:12:05.142143Repositório 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 Recurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteria
title Recurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteria
spellingShingle Recurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteria
Sousa, Ana
experimental evolution
microbiota
reverse evolution
intrastrain polymorphism
nutritional optimization
precision medicine
title_short Recurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteria
title_full Recurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteria
title_fullStr Recurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteria
title_full_unstemmed Recurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteria
title_sort Recurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteria
author Sousa, Ana
author_facet Sousa, Ana
Ramiro, Ricardo S.
Barroso-Batista, João
Güleresi, Daniela
Lourenço, Marta
Gordo, Isabel
author_role author
author2 Ramiro, Ricardo S.
Barroso-Batista, João
Güleresi, Daniela
Lourenço, Marta
Gordo, Isabel
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv ARCA
dc.contributor.author.fl_str_mv Sousa, Ana
Ramiro, Ricardo S.
Barroso-Batista, João
Güleresi, Daniela
Lourenço, Marta
Gordo, Isabel
dc.subject.por.fl_str_mv experimental evolution
microbiota
reverse evolution
intrastrain polymorphism
nutritional optimization
precision medicine
topic experimental evolution
microbiota
reverse evolution
intrastrain polymorphism
nutritional optimization
precision medicine
description The deposited article is a post-print version and has been submitted to peer review.
publishDate 2017
dc.date.none.fl_str_mv 2017-11
2017-11-01T00:00:00Z
2018-11-01T01:30:09Z
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/10400.7/873
url http://hdl.handle.net/10400.7/873
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Ana Sousa, Ricardo S. Ramiro, João Barroso-Batista, Daniela Güleresi, Marta Lourenço, Isabel Gordo; Recurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteria, Molecular Biology and Evolution, Volume 34, Issue 11, 1 November 2017, Pages 2879–2892, https://doi.org/10.1093/molbev/msx221
10.1093/molbev/msx221
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application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
instacron:RCAAP
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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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