Impact of a human gut microbe on Vibrio cholerae host colonization through biofilm enhancement
- Tufts University School of Medicine, United States
- University of Washington, United States
- Massachusetts General Hospital, United States
- Yale University, United States
- Baylor College of Medicine, United States
- 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.
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Human Gut Microbiota Predicts Susceptibility to Vibrio cholerae Infection.European Nucleotide Archive accession number PRJEB17860.
Article and author information
Author details
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.
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.
Reviewing Editor
- Melanie Blokesch, Ecole Polytechnique Fédérale de Lausanne, Switzerland
Version history
- Preprint posted: February 2, 2021 (view preprint)
- Received: August 12, 2021
- Accepted: March 25, 2022
- Accepted Manuscript published: March 28, 2022 (version 1)
- Accepted Manuscript updated: March 31, 2022 (version 2)
- 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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Impact of a human gut microbe on Vibrio cholerae host colonization through biofilm enhancement
eLife 11:e73010.
https://doi.org/10.7554/eLife.73010
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