Trade-Offs of Escherichia coli Adaptation to an Intracellular Lifestyle in Macrophages

Detalhes bibliográficos
Autor(a) principal: Azevedo, M
Data de Publicação: 2016
Outros Autores: Sousa, A, Moura de Sousa, J, Thompson, J A, Proença, J T, Gordo, I
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10400.7/547
Resumo: The bacterium Escherichia coli exhibits remarkable genomic and phenotypic variation, with some pathogenic strains having evolved to survive and even replicate in the harsh intra-macrophage environment. The rate and effects of mutations that can cause pathoadaptation are key determinants of the pace at which E. coli can colonize such niches and become pathogenic. We used experimental evolution to determine the speed and evolutionary paths undertaken by a commensal strain of E. coli when adapting to intracellular life. We estimated the acquisition of pathoadaptive mutations at a rate of 10-6 per genome per generation, resulting in the fixation of more virulent strains in less than a hundred generations. Whole genome sequencing of independently evolved clones showed that the main targets of intracellular adaptation involved loss of function mutations in genes implicated in the assembly of the lipopolysaccharide core, iron metabolism and di- and tri-peptide transport, namely rfaI, fhuA and tppB, respectively. We found a substantial amount of antagonistic pleiotropy in evolved populations, as well as metabolic trade-offs, commonly found in intracellular bacteria with reduced genome sizes. Overall, the low levels of clonal interference detected indicate that the first steps of the transition of a commensal E. coli into intracellular pathogens are dominated by a few pathoadaptive mutations with very strong effects.
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spelling Trade-Offs of Escherichia coli Adaptation to an Intracellular Lifestyle in MacrophagesCloningMacrophagesEvolutionary adaptationIntracellular pathogensBacterial evolutionBacterial pathogensInsertion mutationBacterial geneticsThe bacterium Escherichia coli exhibits remarkable genomic and phenotypic variation, with some pathogenic strains having evolved to survive and even replicate in the harsh intra-macrophage environment. The rate and effects of mutations that can cause pathoadaptation are key determinants of the pace at which E. coli can colonize such niches and become pathogenic. We used experimental evolution to determine the speed and evolutionary paths undertaken by a commensal strain of E. coli when adapting to intracellular life. We estimated the acquisition of pathoadaptive mutations at a rate of 10-6 per genome per generation, resulting in the fixation of more virulent strains in less than a hundred generations. Whole genome sequencing of independently evolved clones showed that the main targets of intracellular adaptation involved loss of function mutations in genes implicated in the assembly of the lipopolysaccharide core, iron metabolism and di- and tri-peptide transport, namely rfaI, fhuA and tppB, respectively. We found a substantial amount of antagonistic pleiotropy in evolved populations, as well as metabolic trade-offs, commonly found in intracellular bacteria with reduced genome sizes. Overall, the low levels of clonal interference detected indicate that the first steps of the transition of a commensal E. coli into intracellular pathogens are dominated by a few pathoadaptive mutations with very strong effects.LAO/ITQB, FCT.PLOSARCAAzevedo, MSousa, AMoura de Sousa, JThompson, J AProença, J TGordo, I2016-01-19T17:56:38Z2016-01-112016-01-11T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.7/547engAzevedo M, Sousa A, Moura de Sousa J, Thompson JA, Proença JT, Gordo I (2016) Trade- Offs of Escherichia coli Adaptation to an Intracellular Lifestyle in Macrophages. PLoS ONE 11(1): e0146123. doi:10.1371/journal.pone.01461210.1371/journal.pone.0146123info: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:RCAAP2022-11-29T14:34:54Zoai:arca.igc.gulbenkian.pt:10400.7/547Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T16:11:47.927470Repositório 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 Trade-Offs of Escherichia coli Adaptation to an Intracellular Lifestyle in Macrophages
title Trade-Offs of Escherichia coli Adaptation to an Intracellular Lifestyle in Macrophages
spellingShingle Trade-Offs of Escherichia coli Adaptation to an Intracellular Lifestyle in Macrophages
Azevedo, M
Cloning
Macrophages
Evolutionary adaptation
Intracellular pathogens
Bacterial evolution
Bacterial pathogens
Insertion mutation
Bacterial genetics
title_short Trade-Offs of Escherichia coli Adaptation to an Intracellular Lifestyle in Macrophages
title_full Trade-Offs of Escherichia coli Adaptation to an Intracellular Lifestyle in Macrophages
title_fullStr Trade-Offs of Escherichia coli Adaptation to an Intracellular Lifestyle in Macrophages
title_full_unstemmed Trade-Offs of Escherichia coli Adaptation to an Intracellular Lifestyle in Macrophages
title_sort Trade-Offs of Escherichia coli Adaptation to an Intracellular Lifestyle in Macrophages
author Azevedo, M
author_facet Azevedo, M
Sousa, A
Moura de Sousa, J
Thompson, J A
Proença, J T
Gordo, I
author_role author
author2 Sousa, A
Moura de Sousa, J
Thompson, J A
Proença, J T
Gordo, I
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv ARCA
dc.contributor.author.fl_str_mv Azevedo, M
Sousa, A
Moura de Sousa, J
Thompson, J A
Proença, J T
Gordo, I
dc.subject.por.fl_str_mv Cloning
Macrophages
Evolutionary adaptation
Intracellular pathogens
Bacterial evolution
Bacterial pathogens
Insertion mutation
Bacterial genetics
topic Cloning
Macrophages
Evolutionary adaptation
Intracellular pathogens
Bacterial evolution
Bacterial pathogens
Insertion mutation
Bacterial genetics
description The bacterium Escherichia coli exhibits remarkable genomic and phenotypic variation, with some pathogenic strains having evolved to survive and even replicate in the harsh intra-macrophage environment. The rate and effects of mutations that can cause pathoadaptation are key determinants of the pace at which E. coli can colonize such niches and become pathogenic. We used experimental evolution to determine the speed and evolutionary paths undertaken by a commensal strain of E. coli when adapting to intracellular life. We estimated the acquisition of pathoadaptive mutations at a rate of 10-6 per genome per generation, resulting in the fixation of more virulent strains in less than a hundred generations. Whole genome sequencing of independently evolved clones showed that the main targets of intracellular adaptation involved loss of function mutations in genes implicated in the assembly of the lipopolysaccharide core, iron metabolism and di- and tri-peptide transport, namely rfaI, fhuA and tppB, respectively. We found a substantial amount of antagonistic pleiotropy in evolved populations, as well as metabolic trade-offs, commonly found in intracellular bacteria with reduced genome sizes. Overall, the low levels of clonal interference detected indicate that the first steps of the transition of a commensal E. coli into intracellular pathogens are dominated by a few pathoadaptive mutations with very strong effects.
publishDate 2016
dc.date.none.fl_str_mv 2016-01-19T17:56:38Z
2016-01-11
2016-01-11T00:00:00Z
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/10400.7/547
url http://hdl.handle.net/10400.7/547
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Azevedo M, Sousa A, Moura de Sousa J, Thompson JA, Proença JT, Gordo I (2016) Trade- Offs of Escherichia coli Adaptation to an Intracellular Lifestyle in Macrophages. PLoS ONE 11(1): e0146123. doi:10.1371/journal.pone.014612
10.1371/journal.pone.0146123
dc.rights.driver.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 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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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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