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Editor's Pick Research Article | Ecological and Evolutionary Science

Diversification of Colonization Factors in a Multidrug-Resistant Escherichia coli Lineage Evolving under Negative Frequency-Dependent Selection

Alan McNally, Teemu Kallonen, Christopher Connor, Khalil Abudahab, David M. Aanensen, Carolyne Horner, Sharon J. Peacock, Julian Parkhill, Nicholas J. Croucher, Jukka Corander
Julian E. Davies, Editor
Alan McNally
aInstitute of Microbiology and Infection, University of Birmingham, Birmingham, United Kingdom
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Teemu Kallonen
bInfection Genomics, Wellcome Sanger Institute, Cambridge, United Kingdom
cDepartment of Biostatistics, University of Oslo, Oslo, Norway
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Christopher Connor
aInstitute of Microbiology and Infection, University of Birmingham, Birmingham, United Kingdom
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Khalil Abudahab
bInfection Genomics, Wellcome Sanger Institute, Cambridge, United Kingdom
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David M. Aanensen
bInfection Genomics, Wellcome Sanger Institute, Cambridge, United Kingdom
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Carolyne Horner
dBritish Society of Antimicrobial Chemotherapy, Birmingham, United Kingdom
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Sharon J. Peacock
bInfection Genomics, Wellcome Sanger Institute, Cambridge, United Kingdom
eDepartment of Medicine, University of Cambridge, Cambridge, United Kingdom
fLondon School of Hygiene and Tropical Medicine, London, United Kingdom
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Julian Parkhill
bInfection Genomics, Wellcome Sanger Institute, Cambridge, United Kingdom
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Nicholas J. Croucher
gFaculty of Medicine, School of Public Health, Imperial College, London, United Kingdom
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Jukka Corander
bInfection Genomics, Wellcome Sanger Institute, Cambridge, United Kingdom
cDepartment of Biostatistics, University of Oslo, Oslo, Norway
hDepartment of Mathematics and Statistics, University of Helsinki, Helsinki, Finland
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Julian E. Davies
University of British Columbia
Roles: Editor
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Jesse Shapiro
University of Montreal
Roles: Solicited external reviewer
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Rene Niehus
University of Oxford
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DOI: 10.1128/mBio.00644-19
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ABSTRACT

Escherichia coli is a major cause of bloodstream and urinary tract infections globally. The wide dissemination of multidrug-resistant (MDR) strains of extraintestinal pathogenic E. coli (ExPEC) poses a rapidly increasing public health burden due to narrowed treatment options and increased risk of failure to clear an infection. Here, we present a detailed population genomic analysis of the ExPEC ST131 clone, in which we seek explanations for its success as an emerging pathogenic strain beyond the acquisition of antimicrobial resistance (AMR) genes. We show evidence for evolution toward separate ecological niches for the main clades of ST131 and differential evolution of anaerobic metabolism, key colonization, and virulence factors. We further demonstrate that negative frequency-dependent selection acting across accessory loci is a major mechanism that has shaped the population evolution of this pathogen.

IMPORTANCE Infections with multidrug-resistant (MDR) strains of Escherichia coli are a significant global public health concern. To combat these pathogens, we need a deeper understanding of how they evolved from their background populations. By understanding the processes that underpin their emergence, we can design new strategies to limit evolution of new clones and combat existing clones. By combining population genomics with modelling approaches, we show that dominant MDR clones of E. coli are under the influence of negative frequency-dependent selection, preventing them from rising to fixation in a population. Furthermore, we show that this selection acts on genes involved in anaerobic metabolism, suggesting that this key trait, and the ability to colonize human intestinal tracts, is a key step in the evolution of MDR clones of E. coli.

FOOTNOTES

    • Received 20 March 2019
    • Accepted 21 March 2019
    • Published 23 April 2019
  • Copyright © 2019 McNally et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Diversification of Colonization Factors in a Multidrug-Resistant Escherichia coli Lineage Evolving under Negative Frequency-Dependent Selection
Alan McNally, Teemu Kallonen, Christopher Connor, Khalil Abudahab, David M. Aanensen, Carolyne Horner, Sharon J. Peacock, Julian Parkhill, Nicholas J. Croucher, Jukka Corander
mBio Apr 2019, 10 (2) e00644-19; DOI: 10.1128/mBio.00644-19

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Diversification of Colonization Factors in a Multidrug-Resistant Escherichia coli Lineage Evolving under Negative Frequency-Dependent Selection
Alan McNally, Teemu Kallonen, Christopher Connor, Khalil Abudahab, David M. Aanensen, Carolyne Horner, Sharon J. Peacock, Julian Parkhill, Nicholas J. Croucher, Jukka Corander
mBio Apr 2019, 10 (2) e00644-19; DOI: 10.1128/mBio.00644-19
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KEYWORDS

AMR
Escherichia coli
evolutionary genomics
negative frequency-dependent selection

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