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Evolutionary and functional history of the Escherichia coli K1 capsule

Author

Listed:
  • Sergio Arredondo-Alonso

    (University of Oslo
    Wellcome Sanger Institute)

  • George Blundell-Hunter

    (University College London)

  • Zuyi Fu

    (Imperial College London)

  • Rebecca A. Gladstone

    (University of Oslo
    Wellcome Sanger Institute)

  • Alfred Fillol-Salom

    (Imperial College London)

  • Jessica Loraine

    (University College London)

  • Elaine Cloutman-Green

    (University College London)

  • Pål J. Johnsen

    (UiT The Arctic University of Norway)

  • Ørjan Samuelsen

    (UiT The Arctic University of Norway
    University Hospital of North Norway)

  • Anna K. Pöntinen

    (University of Oslo
    University Hospital of North Norway)

  • François Cléon

    (UiT The Arctic University of Norway)

  • Susana Chavez-Bueno

    (University of Missouri Kansas City
    UMKC School of Medicine)

  • Miguel A. Cruz

    (Centro Médico Nacional Siglo XXI Instituto Mexicano del Seguro Social
    Benemérita Universidad Autónoma de Puebla)

  • Miguel A. Ares

    (Centro Médico Nacional Siglo XXI Instituto Mexicano del Seguro Social)

  • Manivanh Vongsouvath

    (Mahosot Hospital)

  • Agnieszka Chmielarczyk

    (Jagiellonian University Medical College)

  • Carolyne Horner

    (British Society for Antimicrobial Chemotherapy)

  • Nigel Klein

    (University College London)

  • Alan McNally

    (University of Birmingham)

  • Joice N. Reis

    (Oswaldo Cruz Foundation
    Universidade Federal da Bahia)

  • José R. Penadés

    (Imperial College London)

  • Nicholas R. Thomson

    (Wellcome Sanger Institute
    London School of Hygiene and Tropical Medicine)

  • Jukka Corander

    (University of Oslo
    Wellcome Sanger Institute
    University of Helsinki)

  • Peter W. Taylor

    (University College London)

  • Alex J. McCarthy

    (Imperial College London)

Abstract

Escherichia coli is a leading cause of invasive bacterial infections in humans. Capsule polysaccharide has an important role in bacterial pathogenesis, and the K1 capsule has been firmly established as one of the most potent capsule types in E. coli through its association with severe infections. However, little is known about its distribution, evolution and functions across the E. coli phylogeny, which is fundamental to elucidating its role in the expansion of successful lineages. Using systematic surveys of invasive E. coli isolates, we show that the K1-cps locus is present in a quarter of bloodstream infection isolates and has emerged in at least four different extraintestinal pathogenic E. coli (ExPEC) phylogroups independently in the last 500 years. Phenotypic assessment demonstrates that K1 capsule synthesis enhances E. coli survival in human serum independent of genetic background, and that therapeutic targeting of the K1 capsule re-sensitizes E. coli from distinct genetic backgrounds to human serum. Our study highlights that assessing the evolutionary and functional properties of bacterial virulence factors at population levels is important to better monitor and predict the emergence of virulent clones, and to also inform therapies and preventive medicine to effectively control bacterial infections whilst significantly lowering antibiotic usage.

Suggested Citation

  • Sergio Arredondo-Alonso & George Blundell-Hunter & Zuyi Fu & Rebecca A. Gladstone & Alfred Fillol-Salom & Jessica Loraine & Elaine Cloutman-Green & Pål J. Johnsen & Ørjan Samuelsen & Anna K. Pöntinen , 2023. "Evolutionary and functional history of the Escherichia coli K1 capsule," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39052-w
    DOI: 10.1038/s41467-023-39052-w
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    References listed on IDEAS

    as
    1. Michael Biggel & Basil B. Xavier & James R. Johnson & Karen L. Nielsen & Niels Frimodt-Møller & Veerle Matheeussen & Herman Goossens & Pieter Moons & Sandra Van Puyvelde, 2020. "Horizontally acquired papGII-containing pathogenicity islands underlie the emergence of invasive uropathogenic Escherichia coli lineages," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    2. Amandine Nucci & Eduardo P. C. Rocha & Olaya Rendueles, 2022. "Adaptation to novel spatially-structured environments is driven by the capsule and alters virulence-associated traits," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
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    Cited by:

    1. Youssouf Sereme & Cécile Schrimp & Helène Faury & Maeva Agapoff & Esther Lefebvre-Wloszczowski & Yunhua Chang Marchand & Elisabeth Ageron-Ardila & Emilie Panafieu & Frank Blec & Mathieu Coureuil & Eri, 2024. "A live attenuated vaccine to prevent severe neonatal Escherichia coli K1 infections," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Nguyen Thi Khanh Nhu & M. Arifur Rahman & Kelvin G. K. Goh & Seung Jae Kim & Minh-Duy Phan & Kate M. Peters & Laura Alvarez-Fraga & Steven J. Hancock & Chitra Ravi & Timothy J. Kidd & Matthew J. Sulli, 2024. "A convergent evolutionary pathway attenuating cellulose production drives enhanced virulence of some bacteria," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. 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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