Applying phylogenomics to understand the emergence of Shiga-toxin-producing Escherichia coli O157:H7 strains causing severe human disease in the UK

TJ Dallman, PM Ashton, L Byrne, NT Perry, L Petrovska, R Ellis, L Allison, M Hanson, A Holmes, GJ Gunn, ME Chase-Topping, MEJ Woolhouse, KA Grant, DL Gally, J Wain, C Jenkins

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Abstract

Shiga-toxin-producing Escherichia coli (STEC) O157:H7 is a recently emerged zoonotic pathogen with considerable morbidity. Since the emergence of this serotype in the 1980s, research has focussed on unravelling the evolutionary events from the E. coli O55:H7 ancestor to the contemporaneous globally dispersed strains observed today. In this study, the genomes of over 1000 isolates from both human clinical cases and cattle, spanning the history of STEC O157:H7 in the UK, were sequenced. Phylogenetic analysis revealed the ancestry, key acquisition events and global context of the strains. Dated phylogenies estimated the time to evolution of the most recent common ancestor of the current circulating global clone to be 175 years ago. This event was followed by rapid diversification. We show the acquisition of specific virulence determinates has occurred relatively recently and coincides with its recent detection in the human population. We used clinical outcome data from 493 cases of STEC O157:H7 to assess the relative risk of severe disease including haemolytic uraemic syndrome from each of the defined clades in the population and show the dramatic effect Shiga toxin repertoire has on virulence. We describe two strain replacement events that have occurred in the cattle population in the UK over the last 30 years, one resulting in a highly virulent strain that has accounted for the majority of clinical cases in the UK over the last decade. There is a need to understand the selection pressures maintaining Shiga-toxin-encoding bacteriophages in the ruminant reservoir and the study affirms the requirement for close surveillance of this pathogen in both ruminant and human populations.
Original languageEnglish
JournalMicrobial Genomics
DOIs
Publication statusFirst published - 2015

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Shiga-Toxigenic Escherichia coli
Escherichia coli O157
Shiga Toxin
Ruminants
Population
Virulence
Zoonoses
Bacteriophages
Clone Cells
History
Escherichia coli
Morbidity
Pressure
Research

Bibliographical note

2077648

Keywords

  • Emerging infections
  • Eschericia coli
  • Genomics
  • One Health
  • Public health microbiology
  • Shiga toxin

Cite this

Dallman, TJ ; Ashton, PM ; Byrne, L ; Perry, NT ; Petrovska, L ; Ellis, R ; Allison, L ; Hanson, M ; Holmes, A ; Gunn, GJ ; Chase-Topping, ME ; Woolhouse, MEJ ; Grant, KA ; Gally, DL ; Wain, J ; Jenkins, C. / Applying phylogenomics to understand the emergence of Shiga-toxin-producing Escherichia coli O157:H7 strains causing severe human disease in the UK. In: Microbial Genomics. 2015.
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abstract = "Shiga-toxin-producing Escherichia coli (STEC) O157:H7 is a recently emerged zoonotic pathogen with considerable morbidity. Since the emergence of this serotype in the 1980s, research has focussed on unravelling the evolutionary events from the E. coli O55:H7 ancestor to the contemporaneous globally dispersed strains observed today. In this study, the genomes of over 1000 isolates from both human clinical cases and cattle, spanning the history of STEC O157:H7 in the UK, were sequenced. Phylogenetic analysis revealed the ancestry, key acquisition events and global context of the strains. Dated phylogenies estimated the time to evolution of the most recent common ancestor of the current circulating global clone to be 175 years ago. This event was followed by rapid diversification. We show the acquisition of specific virulence determinates has occurred relatively recently and coincides with its recent detection in the human population. We used clinical outcome data from 493 cases of STEC O157:H7 to assess the relative risk of severe disease including haemolytic uraemic syndrome from each of the defined clades in the population and show the dramatic effect Shiga toxin repertoire has on virulence. We describe two strain replacement events that have occurred in the cattle population in the UK over the last 30 years, one resulting in a highly virulent strain that has accounted for the majority of clinical cases in the UK over the last decade. There is a need to understand the selection pressures maintaining Shiga-toxin-encoding bacteriophages in the ruminant reservoir and the study affirms the requirement for close surveillance of this pathogen in both ruminant and human populations.",
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Dallman, TJ, Ashton, PM, Byrne, L, Perry, NT, Petrovska, L, Ellis, R, Allison, L, Hanson, M, Holmes, A, Gunn, GJ, Chase-Topping, ME, Woolhouse, MEJ, Grant, KA, Gally, DL, Wain, J & Jenkins, C 2015, 'Applying phylogenomics to understand the emergence of Shiga-toxin-producing Escherichia coli O157:H7 strains causing severe human disease in the UK', Microbial Genomics. https://doi.org/10.1099/mgen.0.000029

Applying phylogenomics to understand the emergence of Shiga-toxin-producing Escherichia coli O157:H7 strains causing severe human disease in the UK. / Dallman, TJ; Ashton, PM; Byrne, L; Perry, NT; Petrovska, L; Ellis, R; Allison, L; Hanson, M; Holmes, A; Gunn, GJ; Chase-Topping, ME; Woolhouse, MEJ; Grant, KA; Gally, DL; Wain, J; Jenkins, C.

In: Microbial Genomics, 2015.

Research output: Contribution to journalArticle

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T1 - Applying phylogenomics to understand the emergence of Shiga-toxin-producing Escherichia coli O157:H7 strains causing severe human disease in the UK

AU - Dallman, TJ

AU - Ashton, PM

AU - Byrne, L

AU - Perry, NT

AU - Petrovska, L

AU - Ellis, R

AU - Allison, L

AU - Hanson, M

AU - Holmes, A

AU - Gunn, GJ

AU - Chase-Topping, ME

AU - Woolhouse, MEJ

AU - Grant, KA

AU - Gally, DL

AU - Wain, J

AU - Jenkins, C

N1 - 2077648

PY - 2015

Y1 - 2015

N2 - Shiga-toxin-producing Escherichia coli (STEC) O157:H7 is a recently emerged zoonotic pathogen with considerable morbidity. Since the emergence of this serotype in the 1980s, research has focussed on unravelling the evolutionary events from the E. coli O55:H7 ancestor to the contemporaneous globally dispersed strains observed today. In this study, the genomes of over 1000 isolates from both human clinical cases and cattle, spanning the history of STEC O157:H7 in the UK, were sequenced. Phylogenetic analysis revealed the ancestry, key acquisition events and global context of the strains. Dated phylogenies estimated the time to evolution of the most recent common ancestor of the current circulating global clone to be 175 years ago. This event was followed by rapid diversification. We show the acquisition of specific virulence determinates has occurred relatively recently and coincides with its recent detection in the human population. We used clinical outcome data from 493 cases of STEC O157:H7 to assess the relative risk of severe disease including haemolytic uraemic syndrome from each of the defined clades in the population and show the dramatic effect Shiga toxin repertoire has on virulence. We describe two strain replacement events that have occurred in the cattle population in the UK over the last 30 years, one resulting in a highly virulent strain that has accounted for the majority of clinical cases in the UK over the last decade. There is a need to understand the selection pressures maintaining Shiga-toxin-encoding bacteriophages in the ruminant reservoir and the study affirms the requirement for close surveillance of this pathogen in both ruminant and human populations.

AB - Shiga-toxin-producing Escherichia coli (STEC) O157:H7 is a recently emerged zoonotic pathogen with considerable morbidity. Since the emergence of this serotype in the 1980s, research has focussed on unravelling the evolutionary events from the E. coli O55:H7 ancestor to the contemporaneous globally dispersed strains observed today. In this study, the genomes of over 1000 isolates from both human clinical cases and cattle, spanning the history of STEC O157:H7 in the UK, were sequenced. Phylogenetic analysis revealed the ancestry, key acquisition events and global context of the strains. Dated phylogenies estimated the time to evolution of the most recent common ancestor of the current circulating global clone to be 175 years ago. This event was followed by rapid diversification. We show the acquisition of specific virulence determinates has occurred relatively recently and coincides with its recent detection in the human population. We used clinical outcome data from 493 cases of STEC O157:H7 to assess the relative risk of severe disease including haemolytic uraemic syndrome from each of the defined clades in the population and show the dramatic effect Shiga toxin repertoire has on virulence. We describe two strain replacement events that have occurred in the cattle population in the UK over the last 30 years, one resulting in a highly virulent strain that has accounted for the majority of clinical cases in the UK over the last decade. There is a need to understand the selection pressures maintaining Shiga-toxin-encoding bacteriophages in the ruminant reservoir and the study affirms the requirement for close surveillance of this pathogen in both ruminant and human populations.

KW - Emerging infections

KW - Eschericia coli

KW - Genomics

KW - One Health

KW - Public health microbiology

KW - Shiga toxin

U2 - 10.1099/mgen.0.000029

DO - 10.1099/mgen.0.000029

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SN - 2057-5858

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