Impact of a human gut microbe on Vibrio cholerae host colonization through biofilm enhancement

  1. Kelsey Barrassso
  2. Denise Chac
  3. Meti D Debela
  4. Catherine Geigel
  5. Anjali Steenhaut
  6. Abigail Rivera Seda
  7. Chelsea N Dunmire
  8. Jason B Harris
  9. Regina C Larocque
  10. Firas S Midani
  11. Firdausi Qadri
  12. Jing Yan
  13. Ana A Weil  Is a corresponding author
  14. Wai-Leung Ng  Is a corresponding author
  1. Tufts University School of Medicine, United States
  2. University of Washington, United States
  3. Massachusetts General Hospital, United States
  4. Yale University, United States
  5. Baylor College of Medicine, United States
  6. icddr,b, Bangladesh

Abstract

Recent studies indicate that the human intestinal microbiota could impact the outcome of infection by Vibrio cholerae, the etiological agent of the diarrheal disease cholera. A commensal bacterium, Paracoccus aminovorans, was previously identified in high abundance in stool collected from individuals infected with V. cholerae when compared to stool from uninfected persons. However, if and how P. aminovorans interacts with V. cholerae has not been experimentally determined; moreover, whether any association between this bacterium alters the behaviors of V. cholerae to affect the disease outcome is unclear. Here we show that P. aminovorans and V. cholerae together form dual-species biofilm structure at the air-liquid interface, with previously uncharacterized novel features. Importantly, the presence of P. aminovorans within the murine small intestine enhances V. cholerae colonization in the same niche that is dependent on the Vibrio exopolysaccharide (VPS) and other major components of mature V. cholerae biofilm. These studies illustrate that multi-species biofilm formation is a plausible mechanism used by a gut microbe to increase the virulence of the pathogen, and this interaction may alter outcomes in enteric infections.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figures 1-3, 5, 7.

The following previously published data sets were used

Article and author information

Author details

  1. Kelsey Barrassso

    Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Denise Chac

    Department of Medicine, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Meti D Debela

    Division of Infectious Diseases, Massachusetts General Hospital, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Catherine Geigel

    Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Anjali Steenhaut

    Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Abigail Rivera Seda

    Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Chelsea N Dunmire

    Department of Medicine, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Jason B Harris

    Department of Pediatrics, Massachusetts General Hospital, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Regina C Larocque

    Division of Infectious Diseases, Massachusetts General Hospital, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Firas S Midani

    Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2473-7758
  11. Firdausi Qadri

    icddr,b, Dhaka, Bangladesh
    Competing interests
    The authors declare that no competing interests exist.
  12. Jing Yan

    Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Ana A Weil

    Department of Medicine, University of Washington, Seattle, United States
    For correspondence
    anaweil@uw.edu
    Competing interests
    The authors declare that no competing interests exist.
  14. Wai-Leung Ng

    Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, United States
    For correspondence
    wai-leung.ng@tufts.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8966-6604

Funding

National Institutes of Health (AI121337)

  • Wai-Leung Ng

National Institutes of Health (AI123494)

  • Ana A Weil

National Institutes of Health (DP2GM146253)

  • Jing Yan

National Institutes of Health (R25 GM066567)

  • Abigail Rivera Seda

Burroughs Wellcome Fund (1015763.02)

  • Jing Yan

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Melanie Blokesch, Ecole Polytechnique Fédérale de Lausanne, Switzerland

Ethics

Animal experimentation: All animal experiments were performed at and in accordance with the rules of the Tufts Comparative Medicine Services (CMS), following the guidelines of the American Veterinary Medical Association (AVMA) as well as the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All procedures were performed with approval of the Tufts University CMS (Protocol# B 2018-99). Euthanasia was performed in accordance with guidelines provided by the AVMA and was approved by the Tufts CMS.

Human subjects: The previously published study from which Figure 1 is derived from ref (7) received approval from the Ethical Review Committee at the icddr,b and the institutional review boards of Massachusetts General Hospital and the University of Washington. Participants or their guardians provided written informed consent.

Version history

  1. Preprint posted: February 2, 2021 (view preprint)
  2. Received: August 12, 2021
  3. Accepted: March 25, 2022
  4. Accepted Manuscript published: March 28, 2022 (version 1)
  5. Accepted Manuscript updated: March 31, 2022 (version 2)
  6. Version of Record published: April 8, 2022 (version 3)

Copyright

© 2022, Barrassso et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Kelsey Barrassso
  2. Denise Chac
  3. Meti D Debela
  4. Catherine Geigel
  5. Anjali Steenhaut
  6. Abigail Rivera Seda
  7. Chelsea N Dunmire
  8. Jason B Harris
  9. Regina C Larocque
  10. Firas S Midani
  11. Firdausi Qadri
  12. Jing Yan
  13. Ana A Weil
  14. Wai-Leung Ng
(2022)
Impact of a human gut microbe on Vibrio cholerae host colonization through biofilm enhancement
eLife 11:e73010.
https://doi.org/10.7554/eLife.73010

Share this article

https://doi.org/10.7554/eLife.73010

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