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A convergent evolutionary pathway attenuating cellulose production drives enhanced virulence of some bacteria

Author

Listed:
  • Nguyen Thi Khanh Nhu

    (The University of Queensland
    The University of Queensland
    The University of Queensland)

  • M. Arifur Rahman

    (The University of Queensland
    The University of Queensland, Translational Research Institute
    QIMR Berghofer Medical Research Institute)

  • Kelvin G. K. Goh

    (Griffith University
    Griffith University)

  • Seung Jae Kim

    (The University of Queensland
    The University of Queensland)

  • Minh-Duy Phan

    (The University of Queensland
    The University of Queensland
    The University of Queensland)

  • Kate M. Peters

    (The University of Queensland
    The University of Queensland
    The University of Queensland)

  • Laura Alvarez-Fraga

    (The University of Queensland
    The University of Queensland
    INRAE, Univ Montpellier, LBE)

  • Steven J. Hancock

    (The University of Queensland
    The University of Queensland
    Queen’s University Belfast)

  • Chitra Ravi

    (The University of Queensland
    The University of Queensland
    The University of Queensland)

  • Timothy J. Kidd

    (The University of Queensland
    The University of Queensland
    Royal Brisbane and Women’s Hospital)

  • Matthew J. Sullivan

    (Griffith University
    Griffith University
    University of East Anglia)

  • Katharine M. Irvine

    (The University of Queensland
    The University of Queensland, Translational Research Institute)

  • Scott A. Beatson

    (The University of Queensland
    The University of Queensland)

  • Matthew J. Sweet

    (The University of Queensland
    The University of Queensland)

  • Adam D. Irwin

    (The University of Queensland
    University of Queensland Centre for Clinical Research
    Queensland Children’s Hospital)

  • Jana Vukovic

    (The University of Queensland
    The University of Queensland)

  • Glen C. Ulett

    (Griffith University
    Griffith University)

  • Sumaira Z. Hasnain

    (The University of Queensland
    The University of Queensland, Translational Research Institute)

  • Mark A. Schembri

    (The University of Queensland
    The University of Queensland
    The University of Queensland)

Abstract

Bacteria adapt to selective pressure in their immediate environment in multiple ways. One mechanism involves the acquisition of independent mutations that disable or modify a key pathway, providing a signature of adaptation via convergent evolution. Extra-intestinal pathogenic Escherichia coli (ExPEC) belonging to sequence type 95 (ST95) represent a global clone frequently associated with severe human infections including acute pyelonephritis, sepsis, and neonatal meningitis. Here, we analysed a publicly available dataset of 613 ST95 genomes and identified a series of loss-of-function mutations that disrupt cellulose production or its modification in 55.3% of strains. We show the inability to produce cellulose significantly enhances ST95 invasive infection in a rat model of neonatal meningitis, leading to the disruption of intestinal barrier integrity in newborn pups and enhanced dissemination to the liver, spleen and brain. Consistent with these observations, disruption of cellulose production in ST95 augmented innate immune signalling and tissue neutrophil infiltration in a mouse model of urinary tract infection. Mutations that disrupt cellulose production were also identified in other virulent ExPEC STs, Shigella and Salmonella, suggesting a correlative association with many Enterobacteriaceae that cause severe human infection. Together, our findings provide an explanation for the emergence of hypervirulent Enterobacteriaceae clones.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45176-4
    DOI: 10.1038/s41467-024-45176-4
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    References listed on IDEAS

    as
    1. 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.
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