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Genome Dynamics of Escherichia coli during Antibiotic Treatment: Transfer, Loss, and Persistence of Genetic Elements In situ of the Infant Gut

Elucidating the adaptive strategies and plasticity of bacterial genomes in situ is crucial for understanding the epidemiology and evolution of pathogens threatening human health. While much is known about the evolution of Escherichia coli in controlled laboratory environments, less effort has been m...

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Autores principales: Porse, Andreas, Gumpert, Heidi, Kubicek-Sutherland, Jessica Z., Karami, Nahid, Adlerberth, Ingegerd, Wold, Agnes E., Andersson, Dan I., Sommer, Morten O. A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5388698/
https://www.ncbi.nlm.nih.gov/pubmed/28447026
http://dx.doi.org/10.3389/fcimb.2017.00126
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author Porse, Andreas
Gumpert, Heidi
Kubicek-Sutherland, Jessica Z.
Karami, Nahid
Adlerberth, Ingegerd
Wold, Agnes E.
Andersson, Dan I.
Sommer, Morten O. A.
author_facet Porse, Andreas
Gumpert, Heidi
Kubicek-Sutherland, Jessica Z.
Karami, Nahid
Adlerberth, Ingegerd
Wold, Agnes E.
Andersson, Dan I.
Sommer, Morten O. A.
author_sort Porse, Andreas
collection PubMed
description Elucidating the adaptive strategies and plasticity of bacterial genomes in situ is crucial for understanding the epidemiology and evolution of pathogens threatening human health. While much is known about the evolution of Escherichia coli in controlled laboratory environments, less effort has been made to elucidate the genome dynamics of E. coli in its native settings. Here, we follow the genome dynamics of co-existing E. coli lineages in situ of the infant gut during the first year of life. One E. coli lineage causes a urinary tract infection (UTI) and experiences several alterations of its genomic content during subsequent antibiotic treatment. Interestingly, all isolates of this uropathogenic E. coli strain carried a highly stable plasmid implicated in virulence of diverse pathogenic strains from all over the world. While virulence elements are certainly beneficial during infection scenarios, their role in gut colonization and pathogen persistence is poorly understood. We performed in vivo competitive fitness experiments to assess the role of this highly disseminated virulence plasmid in gut colonization, but found no evidence for a direct benefit of plasmid carriage. Through plasmid stability assays, we demonstrate that this plasmid is maintained in a parasitic manner, by strong first-line inheritance mechanisms, acting on the single-cell level, rather than providing a direct survival advantage in the gut. Investigating the ecology of endemic accessory genetic elements, in their pathogenic hosts and native environment, is of vital importance if we want to understand the evolution and persistence of highly virulent and drug resistant bacterial isolates.
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spelling pubmed-53886982017-04-26 Genome Dynamics of Escherichia coli during Antibiotic Treatment: Transfer, Loss, and Persistence of Genetic Elements In situ of the Infant Gut Porse, Andreas Gumpert, Heidi Kubicek-Sutherland, Jessica Z. Karami, Nahid Adlerberth, Ingegerd Wold, Agnes E. Andersson, Dan I. Sommer, Morten O. A. Front Cell Infect Microbiol Microbiology Elucidating the adaptive strategies and plasticity of bacterial genomes in situ is crucial for understanding the epidemiology and evolution of pathogens threatening human health. While much is known about the evolution of Escherichia coli in controlled laboratory environments, less effort has been made to elucidate the genome dynamics of E. coli in its native settings. Here, we follow the genome dynamics of co-existing E. coli lineages in situ of the infant gut during the first year of life. One E. coli lineage causes a urinary tract infection (UTI) and experiences several alterations of its genomic content during subsequent antibiotic treatment. Interestingly, all isolates of this uropathogenic E. coli strain carried a highly stable plasmid implicated in virulence of diverse pathogenic strains from all over the world. While virulence elements are certainly beneficial during infection scenarios, their role in gut colonization and pathogen persistence is poorly understood. We performed in vivo competitive fitness experiments to assess the role of this highly disseminated virulence plasmid in gut colonization, but found no evidence for a direct benefit of plasmid carriage. Through plasmid stability assays, we demonstrate that this plasmid is maintained in a parasitic manner, by strong first-line inheritance mechanisms, acting on the single-cell level, rather than providing a direct survival advantage in the gut. Investigating the ecology of endemic accessory genetic elements, in their pathogenic hosts and native environment, is of vital importance if we want to understand the evolution and persistence of highly virulent and drug resistant bacterial isolates. Frontiers Media S.A. 2017-04-12 /pmc/articles/PMC5388698/ /pubmed/28447026 http://dx.doi.org/10.3389/fcimb.2017.00126 Text en Copyright © 2017 Porse, Gumpert, Kubicek-Sutherland, Karami, Adlerberth, Wold, Andersson and Sommer. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Porse, Andreas
Gumpert, Heidi
Kubicek-Sutherland, Jessica Z.
Karami, Nahid
Adlerberth, Ingegerd
Wold, Agnes E.
Andersson, Dan I.
Sommer, Morten O. A.
Genome Dynamics of Escherichia coli during Antibiotic Treatment: Transfer, Loss, and Persistence of Genetic Elements In situ of the Infant Gut
title Genome Dynamics of Escherichia coli during Antibiotic Treatment: Transfer, Loss, and Persistence of Genetic Elements In situ of the Infant Gut
title_full Genome Dynamics of Escherichia coli during Antibiotic Treatment: Transfer, Loss, and Persistence of Genetic Elements In situ of the Infant Gut
title_fullStr Genome Dynamics of Escherichia coli during Antibiotic Treatment: Transfer, Loss, and Persistence of Genetic Elements In situ of the Infant Gut
title_full_unstemmed Genome Dynamics of Escherichia coli during Antibiotic Treatment: Transfer, Loss, and Persistence of Genetic Elements In situ of the Infant Gut
title_short Genome Dynamics of Escherichia coli during Antibiotic Treatment: Transfer, Loss, and Persistence of Genetic Elements In situ of the Infant Gut
title_sort genome dynamics of escherichia coli during antibiotic treatment: transfer, loss, and persistence of genetic elements in situ of the infant gut
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5388698/
https://www.ncbi.nlm.nih.gov/pubmed/28447026
http://dx.doi.org/10.3389/fcimb.2017.00126
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