Escherichia coli killing by epidemiologically successful sublineages of Shigella sonnei is mediated by colicins.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Nov 2023
Historique:
received: 11 04 2023
revised: 20 09 2023
accepted: 21 09 2023
medline: 13 11 2023
pubmed: 9 10 2023
entrez: 8 10 2023
Statut: ppublish

Résumé

Shigella sp. are enteric pathogens which causes >125 million cases of shigellosis annually. S. sonnei accounts for about a quarter of those cases and is increasingly prevalent in industrialising nations. Being an enteric pathogen, S. sonnei benefits from outcompeting gut commensals such as Escherichia coli to establish itself and cause disease. There are numerous mechanisms that bacterial pathogens use to outcompete its rivals including molecules called colicins. A Type 6 Secretion System (T6SS) was recently described as contributing to E. coli killing in S. sonnei. We used Bulk Phenotyping of Epidemiological Replicates (BPER) which combined bacterial Genome Wide Association Studies (bGWAS) and high throughput phenotyping on a collection of S. sonnei surveillance isolates to identify the genetic features associated with E. coli killing and explore their relationship with epidemiological behaviour. We further explored the presence of colicins and T6SS components in the isolates using genomics, laboratory experimentation, and proteomics. Our bGWAS analysis returned known and novel colicin and colicin related genes as significantly associated with E. coli killing. In silico analyses identified key colicin clusters responsible for the killing phenotype associated with epidemiologically successful sub-lineages. The killing phenotype was not associated with the presence of a T6SS. Laboratory analyses confirmed the presence of the key colicin clusters and that killing was contact-independent. Colicins are responsible for E. coli killing by S. sonnei, not a T6SS. This phenotype contributes to shaping the observed epidemiology of S. sonnei and may contribute to its increasing prevalence globally. BPER is an epidemiologically relevant approach to phenotypic testing that enables the rapid identification of genetic drivers of phenotypic changes, and assessment of their relevance to epidemiology in natural settings. Biotechnology and Biological Sciences Research Council, Biotechnology and Biological Sciences Research Council Doctoral Training Partnership studentship, Wellcome Trust, Medical Research Council (UK), French National Research Agency.

Sections du résumé

BACKGROUND BACKGROUND
Shigella sp. are enteric pathogens which causes >125 million cases of shigellosis annually. S. sonnei accounts for about a quarter of those cases and is increasingly prevalent in industrialising nations. Being an enteric pathogen, S. sonnei benefits from outcompeting gut commensals such as Escherichia coli to establish itself and cause disease. There are numerous mechanisms that bacterial pathogens use to outcompete its rivals including molecules called colicins. A Type 6 Secretion System (T6SS) was recently described as contributing to E. coli killing in S. sonnei.
METHODS METHODS
We used Bulk Phenotyping of Epidemiological Replicates (BPER) which combined bacterial Genome Wide Association Studies (bGWAS) and high throughput phenotyping on a collection of S. sonnei surveillance isolates to identify the genetic features associated with E. coli killing and explore their relationship with epidemiological behaviour. We further explored the presence of colicins and T6SS components in the isolates using genomics, laboratory experimentation, and proteomics.
FINDINGS RESULTS
Our bGWAS analysis returned known and novel colicin and colicin related genes as significantly associated with E. coli killing. In silico analyses identified key colicin clusters responsible for the killing phenotype associated with epidemiologically successful sub-lineages. The killing phenotype was not associated with the presence of a T6SS. Laboratory analyses confirmed the presence of the key colicin clusters and that killing was contact-independent.
INTERPRETATION CONCLUSIONS
Colicins are responsible for E. coli killing by S. sonnei, not a T6SS. This phenotype contributes to shaping the observed epidemiology of S. sonnei and may contribute to its increasing prevalence globally. BPER is an epidemiologically relevant approach to phenotypic testing that enables the rapid identification of genetic drivers of phenotypic changes, and assessment of their relevance to epidemiology in natural settings.
FUNDING BACKGROUND
Biotechnology and Biological Sciences Research Council, Biotechnology and Biological Sciences Research Council Doctoral Training Partnership studentship, Wellcome Trust, Medical Research Council (UK), French National Research Agency.

Identifiants

pubmed: 37806286
pii: S2352-3964(23)00388-2
doi: 10.1016/j.ebiom.2023.104822
pmc: PMC10579285
pii:
doi:

Substances chimiques

Colicins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104822

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests Authors declare no competing interests.

Auteurs

P Malaka De Silva (PM)

Department of Clinical Infection, Microbiology, and Immunology, Institute for Infection, Veterinary, and Ecological Sciences (IVES), University of Liverpool, Liverpool, United Kingdom.

Rebecca J Bennett (RJ)

Department of Clinical Infection, Microbiology, and Immunology, Institute for Infection, Veterinary, and Ecological Sciences (IVES), University of Liverpool, Liverpool, United Kingdom.

Lauriane Kuhn (L)

Plateforme protéomique Strasbourg Esplanade FR1589 du CNRS, Université de Strasbourg, Strasbourg, France.

Patryk Ngondo (P)

Université de Strasbourg, CNRS, Architecture et Réactivité de l'ARN, UPR9002, F-67000, Strasbourg, France.

Lorine Debande (L)

Université de Strasbourg, CNRS, Architecture et Réactivité de l'ARN, UPR9002, F-67000, Strasbourg, France.

Elisabeth Njamkepo (E)

Institut Pasteur, Université Paris Cité, Unité des Bactéries pathogènes entériques, Centre National de Référence des Escherichia coli, Shigella et Salmonella, Paris, F-75015, France.

Brian Ho (B)

Institute of Structural and Molecular Biology, University College London and Birkbeck, London, UK.

François-Xavier Weill (FX)

Institut Pasteur, Université Paris Cité, Unité des Bactéries pathogènes entériques, Centre National de Référence des Escherichia coli, Shigella et Salmonella, Paris, F-75015, France.

Benoît S Marteyn (BS)

Université de Strasbourg, CNRS, Architecture et Réactivité de l'ARN, UPR9002, F-67000, Strasbourg, France.

Claire Jenkins (C)

Gastro and Food Safety (One Health) Division, UK Health Security Agency, Colindale, London, UK.

Kate S Baker (KS)

Department of Clinical Infection, Microbiology, and Immunology, Institute for Infection, Veterinary, and Ecological Sciences (IVES), University of Liverpool, Liverpool, United Kingdom; Department of Genetics, University of Cambridge, Downing Place, Cambridge, UK. Electronic address: kb827@cam.ac.uk.

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