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

2017-11Journal article Open access
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dc.contributor.authorSousa, Ana
dc.contributor.authorRamiro, Ricardo S.
dc.contributor.authorBarroso-Batista, João
dc.contributor.authorGüleresi, Daniela
dc.contributor.authorLourenço, Marta
dc.contributor.authorGordo, Isabel
dc.date.accessioned2018-05-18T15:13:34Z
dc.date.available2018-11-01T01:30:09Z
dc.date.issued2017-11
dc.descriptionThe deposited article is a post-print version and has been submitted to peer review.pt_PT
dc.descriptionThis deposit is composed by the main article plus the supplementary materials of the publication.pt_PT
dc.description.abstractThe 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.pt_PT
dc.description.sponsorshipThis research received funding from the European Research Council (ERC): ERC-StG-ECOADAPT; University of Cologne-Instituto Gulbenkian de Ciência, under SFB of DFG.pt_PT
dc.description.versioninfo:eu-repo/semantics/publishedVersionpt_PT
dc.identifier.citationAna 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/msx221pt_PT
dc.identifier.doi10.1093/molbev/msx221pt_PT
dc.identifier.urihttp://hdl.handle.net/10400.7/873
dc.language.isoengpt_PT
dc.peerreviewedyespt_PT
dc.publisherOxford University Presspt_PT
dc.relationMicrobial adaptation within ecosystems
dc.relation.publisherversionhttps://academic.oup.com/mbe/article/34/11/2879/4086164pt_PT
dc.rights.urihttp://creativecommons.org/licenses/by-nc/4.0/pt_PT
dc.subjectexperimental evolutionpt_PT
dc.subjectmicrobiotapt_PT
dc.subjectreverse evolutionpt_PT
dc.subjectintrastrain polymorphismpt_PT
dc.subjectnutritional optimizationpt_PT
dc.subjectprecision medicinept_PT
dc.titleRecurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteriapt_PT
dc.typejournal article
dspace.entity.typePublication
oaire.awardTitleMicrobial adaptation within ecosystems
oaire.awardURIinfo:eu-repo/grantAgreement/EC/FP7/260421/EU
oaire.citation.endPage2892pt_PT
oaire.citation.issue11pt_PT
oaire.citation.startPage2879pt_PT
oaire.citation.titleMolecular Biology and Evolutionpt_PT
oaire.citation.volume34pt_PT
oaire.fundingStreamFP7
project.funder.identifierhttp://doi.org/10.13039/501100008530
project.funder.nameEuropean Commission
rcaap.embargofctThe deposited article has 12 months of embargo period in terms of access, because of the journal's policies and the publisher's copyright policy, which require a period of 12 months of embargo after the released date of the publication.pt_PT
rcaap.rightsembargoedAccesspt_PT
rcaap.typearticlept_PT
relation.isProjectOfPublication1f01df05-f8af-4e76-8dec-0fc6237b41fd
relation.isProjectOfPublication.latestForDiscovery1f01df05-f8af-4e76-8dec-0fc6237b41fd

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