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Epistatic interactions between the high pathogenicity island and other iron uptake systems shape Escherichia coli extra-intestinal virulence

Author

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  • Guilhem Royer

    (Université Paris Cité, IAME, INSERM
    Diagnostic et Traitement des Infections, Hôpital Henri Mondor
    Université Paris-Saclay
    EERA Unit “Ecology and Evolution of Antibiotics Resistance,” Institut Pasteur-Assistance Publique/Hôpitaux de Paris-Université Paris-Saclay)

  • Olivier Clermont

    (Université Paris Cité, IAME, INSERM)

  • Julie Marin

    (Université Paris Cité, IAME, INSERM
    Université Sorbonne Paris Nord, IAME, INSERM)

  • Bénédicte Condamine

    (Université Paris Cité, IAME, INSERM)

  • Sara Dion

    (Université Paris Cité, IAME, INSERM)

  • François Blanquart

    (PSL Research University)

  • Marco Galardini

    (a joint venture between the Hannover Medical School (MHH) and the Helmholtz Centre for Infection Research (HZI)
    Hannover Medical School (MHH))

  • Erick Denamur

    (Université Paris Cité, IAME, INSERM
    Laboratoire de Génétique Moléculaire)

Abstract

The intrinsic virulence of extra-intestinal pathogenic Escherichia coli is associated with numerous chromosomal and/or plasmid-borne genes, encoding diverse functions such as adhesins, toxins, and iron capture systems. However, the respective contribution to virulence of those genes seems to depend on the genetic background and is poorly understood. Here, we analyze genomes of 232 strains of sequence type complex STc58 and show that virulence (quantified in a mouse model of sepsis) emerged in a sub-group of STc58 due to the presence of the siderophore-encoding high-pathogenicity island (HPI). When extending our genome-wide association study to 370 Escherichia strains, we show that full virulence is associated with the presence of the aer or sit operons, in addition to the HPI. The prevalence of these operons, their co-occurrence and their genomic location depend on strain phylogeny. Thus, selection of lineage-dependent specific associations of virulence-associated genes argues for strong epistatic interactions shaping the emergence of virulence in E. coli.

Suggested Citation

  • Guilhem Royer & Olivier Clermont & Julie Marin & Bénédicte Condamine & Sara Dion & François Blanquart & Marco Galardini & Erick Denamur, 2023. "Epistatic interactions between the high pathogenicity island and other iron uptake systems shape Escherichia coli extra-intestinal virulence," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39428-y
    DOI: 10.1038/s41467-023-39428-y
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    References listed on IDEAS

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    1. Cameron J. Reid & Max L. Cummins & Stefan Börjesson & Michael S. M. Brouwer & Henrik Hasman & Anette M. Hammerum & Louise Roer & Stefanie Hess & Thomas Berendonk & Kristina Nešporová & Marisa Haenni &, 2022. "A role for ColV plasmids in the evolution of pathogenic Escherichia coli ST58," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Guillaume Gautreau & Adelme Bazin & Mathieu Gachet & Rémi Planel & Laura Burlot & Mathieu Dubois & Amandine Perrin & Claudine Médigue & Alexandra Calteau & Stéphane Cruveiller & Catherine Matias & Chr, 2020. "PPanGGOLiN: Depicting microbial diversity via a partitioned pangenome graph," PLOS Computational Biology, Public Library of Science, vol. 16(3), pages 1-27, March.
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    1. Tamim Khawaja & Tommi Mäklin & Teemu Kallonen & Rebecca A. Gladstone & Anna K. Pöntinen & Sointu Mero & Harry A. Thorpe & Ørjan Samuelsen & Julian Parkhill & Mateen Izhar & M. Waheed Akhtar & Jukka Co, 2024. "Deep sequencing of Escherichia coli exposes colonisation diversity and impact of antibiotics in Punjab, Pakistan," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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