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

Andreas Porse, Heidi Gumpert, Jessica Z. Kubicek-Sutherland, Nahid Karami, Ingegerd Adlerberth, Agnes E. Wold, Dan I. Andersson, Morten Otto Alexander Sommer

Research output: Contribution to journalJournal articleResearchpeer-review

160 Downloads (Pure)

Abstract

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.
Original languageEnglish
Article number126
JournalFrontiers in Cellular and Infection Microbiology
Volume7
Number of pages12
ISSN2235-2988
DOIs
Publication statusPublished - 2017

Bibliographical note

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.

Keywords

  • Escherichia coli
  • Genome evolution
  • Virulence plasmid dynamics
  • Plasmid persistence
  • Horizontal gene transfer
  • Antibiotic treatment
  • Urinary tract infections
  • Infant gut

Cite this

Porse, Andreas ; Gumpert, Heidi ; Kubicek-Sutherland, Jessica Z. ; Karami, Nahid ; Adlerberth, Ingegerd ; Wold, Agnes E. ; Andersson, Dan I. ; Sommer, Morten Otto Alexander. / Genome Dynamics of Escherichia coli during Antibiotic Treatment: Transfer, Loss, and Persistence of Genetic Elements In situ of the Infant Gut. In: Frontiers in Cellular and Infection Microbiology. 2017 ; Vol. 7.
@article{8d9913234d6e4601ab25a74dafb73e9d,
title = "Genome Dynamics of Escherichia coli during Antibiotic Treatment: Transfer, Loss, and Persistence of Genetic Elements In situ of the Infant Gut",
abstract = "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.",
keywords = "Escherichia coli, Genome evolution, Virulence plasmid dynamics, Plasmid persistence, Horizontal gene transfer, Antibiotic treatment, Urinary tract infections, Infant gut",
author = "Andreas Porse and Heidi Gumpert and Kubicek-Sutherland, {Jessica Z.} and Nahid Karami and Ingegerd Adlerberth and Wold, {Agnes E.} and Andersson, {Dan I.} and Sommer, {Morten Otto Alexander}",
note = "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.",
year = "2017",
doi = "10.3389/fcimb.2017.00126",
language = "English",
volume = "7",
journal = "Frontiers in Cellular and Infection Microbiology",
issn = "2235-2988",
publisher = "Frontiers Media S.A.",

}

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 Otto Alexander.

In: Frontiers in Cellular and Infection Microbiology, Vol. 7, 126, 2017.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Genome Dynamics of Escherichia coli during Antibiotic Treatment: Transfer, Loss, and Persistence of Genetic Elements In situ of the Infant Gut

AU - Porse, Andreas

AU - Gumpert, Heidi

AU - Kubicek-Sutherland, Jessica Z.

AU - Karami, Nahid

AU - Adlerberth, Ingegerd

AU - Wold, Agnes E.

AU - Andersson, Dan I.

AU - Sommer, Morten Otto Alexander

N1 - 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.

PY - 2017

Y1 - 2017

N2 - 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.

AB - 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.

KW - Escherichia coli

KW - Genome evolution

KW - Virulence plasmid dynamics

KW - Plasmid persistence

KW - Horizontal gene transfer

KW - Antibiotic treatment

KW - Urinary tract infections

KW - Infant gut

U2 - 10.3389/fcimb.2017.00126

DO - 10.3389/fcimb.2017.00126

M3 - Journal article

VL - 7

JO - Frontiers in Cellular and Infection Microbiology

JF - Frontiers in Cellular and Infection Microbiology

SN - 2235-2988

M1 - 126

ER -