Phage predation shapes the population structure of Shiga-toxigenic Escherichia coli O157:H7 in the UK: An evolutionary perspective

Lauren A. Cowley; Timothy J. Dallman; Claire Jenkins; Samuel K. Sheppard

doi:10.3389/fgene.2019.00763

Phage predation shapes the population structure of Shiga-toxigenic Escherichia coli O157:H7 in the UK: An evolutionary perspective

Lauren A. Cowley^*, Timothy J. Dallman, Claire Jenkins, Samuel K. Sheppard

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

3 Citations (Scopus)

Abstract

Bacterial–host interactions are non-linear and actually threefold, involving significant selection through predatory lytic bacteriophages in the host environment. In studies of human and animal gut microbiome bacteria, it is important to consider phage in all host–pathogen interactions. We use an important zoonotic pathogen, Shiga toxigenic Escherichia coli (STEC) O157:H7, to investigate this. Our study provides evidence that phage resistance profiles are well maintained at the sub-lineage level with variation in profiles within sub-lineages uncommon. This indicates that phage resistance heterogeneity happened early on in the STEC O157:H7 natural history and that occasional “wobbles” do not often outcompete the stable lineage unless combined with a competitive advantage. We discuss an example of this in the acquisition of stx2a that, while an important virulence factor, also conveys increased phage cross-resistance. We also discuss the role of phage resistance in co-occurrence of the three stable lineages worldwide and whether differing phage resistance is maintaining diversity.

Original language	English
Article number	763
Journal	Frontiers in Genetics
Volume	10
Issue number	JUL
DOIs	https://doi.org/10.3389/fgene.2019.00763
Publication status	Published - 2019

Bibliographical note

Funding Information:
LC is supported under the University of Bath prize fellowship scheme. SS is a principal investigator for the MRC CLIMB consortium (MR/L015080/1). TD and CJ are funded through PHE.

Publisher Copyright:
Copyright © 2019 Cowley, Dallman, Jenkins and Sheppard. 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) and the copyright owner(s) 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 O157:H7
Evolution
Host
Phage
Population structure

Access to Document

10.3389/fgene.2019.00763

Cite this

@article{3139e360dfd340aa8fe4e2bbfb45e25c,

title = "Phage predation shapes the population structure of Shiga-toxigenic Escherichia coli O157:H7 in the UK: An evolutionary perspective",

abstract = "Bacterial–host interactions are non-linear and actually threefold, involving significant selection through predatory lytic bacteriophages in the host environment. In studies of human and animal gut microbiome bacteria, it is important to consider phage in all host–pathogen interactions. We use an important zoonotic pathogen, Shiga toxigenic Escherichia coli (STEC) O157:H7, to investigate this. Our study provides evidence that phage resistance profiles are well maintained at the sub-lineage level with variation in profiles within sub-lineages uncommon. This indicates that phage resistance heterogeneity happened early on in the STEC O157:H7 natural history and that occasional “wobbles” do not often outcompete the stable lineage unless combined with a competitive advantage. We discuss an example of this in the acquisition of stx2a that, while an important virulence factor, also conveys increased phage cross-resistance. We also discuss the role of phage resistance in co-occurrence of the three stable lineages worldwide and whether differing phage resistance is maintaining diversity.",

keywords = "Escherichia coli O157:H7, Evolution, Host, Phage, Population structure",

author = "Cowley, {Lauren A.} and Dallman, {Timothy J.} and Claire Jenkins and Sheppard, {Samuel K.}",

note = "Funding Information: LC is supported under the University of Bath prize fellowship scheme. SS is a principal investigator for the MRC CLIMB consortium (MR/L015080/1). TD and CJ are funded through PHE. Publisher Copyright: Copyright {\textcopyright} 2019 Cowley, Dallman, Jenkins and Sheppard. 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) and the copyright owner(s) 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 = "2019",

doi = "10.3389/fgene.2019.00763",

language = "English",

volume = "10",

journal = "Frontiers in Genetics",

issn = "1664-8021",

publisher = "Frontiers Media",

number = "JUL",

}

TY - JOUR

T1 - Phage predation shapes the population structure of Shiga-toxigenic Escherichia coli O157:H7 in the UK

T2 - An evolutionary perspective

AU - Cowley, Lauren A.

AU - Dallman, Timothy J.

AU - Jenkins, Claire

AU - Sheppard, Samuel K.

N1 - Funding Information: LC is supported under the University of Bath prize fellowship scheme. SS is a principal investigator for the MRC CLIMB consortium (MR/L015080/1). TD and CJ are funded through PHE. Publisher Copyright: Copyright © 2019 Cowley, Dallman, Jenkins and Sheppard. 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) and the copyright owner(s) 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 - 2019

Y1 - 2019

N2 - Bacterial–host interactions are non-linear and actually threefold, involving significant selection through predatory lytic bacteriophages in the host environment. In studies of human and animal gut microbiome bacteria, it is important to consider phage in all host–pathogen interactions. We use an important zoonotic pathogen, Shiga toxigenic Escherichia coli (STEC) O157:H7, to investigate this. Our study provides evidence that phage resistance profiles are well maintained at the sub-lineage level with variation in profiles within sub-lineages uncommon. This indicates that phage resistance heterogeneity happened early on in the STEC O157:H7 natural history and that occasional “wobbles” do not often outcompete the stable lineage unless combined with a competitive advantage. We discuss an example of this in the acquisition of stx2a that, while an important virulence factor, also conveys increased phage cross-resistance. We also discuss the role of phage resistance in co-occurrence of the three stable lineages worldwide and whether differing phage resistance is maintaining diversity.

AB - Bacterial–host interactions are non-linear and actually threefold, involving significant selection through predatory lytic bacteriophages in the host environment. In studies of human and animal gut microbiome bacteria, it is important to consider phage in all host–pathogen interactions. We use an important zoonotic pathogen, Shiga toxigenic Escherichia coli (STEC) O157:H7, to investigate this. Our study provides evidence that phage resistance profiles are well maintained at the sub-lineage level with variation in profiles within sub-lineages uncommon. This indicates that phage resistance heterogeneity happened early on in the STEC O157:H7 natural history and that occasional “wobbles” do not often outcompete the stable lineage unless combined with a competitive advantage. We discuss an example of this in the acquisition of stx2a that, while an important virulence factor, also conveys increased phage cross-resistance. We also discuss the role of phage resistance in co-occurrence of the three stable lineages worldwide and whether differing phage resistance is maintaining diversity.

KW - Escherichia coli O157:H7

KW - Evolution

KW - Host

KW - Phage

KW - Population structure

UR - http://www.scopus.com/inward/record.url?scp=85071446006&partnerID=8YFLogxK

U2 - 10.3389/fgene.2019.00763

DO - 10.3389/fgene.2019.00763

M3 - Article

AN - SCOPUS:85071446006

SN - 1664-8021

VL - 10

JO - Frontiers in Genetics

JF - Frontiers in Genetics

IS - JUL

M1 - 763

ER -

Phage predation shapes the population structure of Shiga-toxigenic Escherichia coli O157:H7 in the UK: An evolutionary perspective

Abstract

Bibliographical note

Keywords

Access to Document

Other files and links

Fingerprint

Cite this