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

Kelsey Barrasso, Denise Chac, Meti D. Debela, Jason B. Harris, Regina C. LaRocque, Firas S. Midani, Firdausi Qadri, Jing Yan, Ana A. Weil, Wai-Leung Ng
doi: https://doi.org/10.1101/2021.02.01.429194
Kelsey Barrasso
1Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, MA
2Program of Molecular Microbiology, Graduate School of Biomedical Sciences, Tufts University School of Medicine, Boston, MA
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Denise Chac
3Department of Medicine, University of Washington, Seattle, WA
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Meti D. Debela
4Division of Infectious Diseases, Massachusetts General Hospital, Boston, MA
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Jason B. Harris
4Division of Infectious Diseases, Massachusetts General Hospital, Boston, MA
5Department of Pediatrics, Harvard Medical School, Boston, MA
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Regina C. LaRocque
4Division of Infectious Diseases, Massachusetts General Hospital, Boston, MA
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Firas S. Midani
6Department of Molecular Virology and Microbiology at Baylor College of Medicine, Houston, TX
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Firdausi Qadri
7International Center for Diarrheal Disease Research, Bangladesh, Dhaka, Bangladesh
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Jing Yan
8Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT
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Ana A. Weil
3Department of Medicine, University of Washington, Seattle, WA
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  • For correspondence: anaweil@uw.edu wai-leung.ng@tufts.edu
Wai-Leung Ng
1Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, MA
2Program of Molecular Microbiology, Graduate School of Biomedical Sciences, Tufts University School of Medicine, Boston, MA
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  • For correspondence: anaweil@uw.edu wai-leung.ng@tufts.edu
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Abstract

The human intestinal microbiota plays a crucial role in protection against the infection of Vibrio cholerae, the etiological agent of the diarrheal disease cholera. A rare commensal bacterium, Paracoccus aminovorans, was previously identified to bloom in the intestines during V. cholerae infection in a cohort of patients exposed to the pathogen. However, 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 also unclear. Here we show that P. aminovorans and V. cholerae together form dual-species biofilm structures with previously uncharacterized novel features. Using an infant mouse colonization model, we demonstrate that the presence of P. aminovorans within the murine small intestine enhances V. cholerae colonization in the same niche that is dependent on the production of the Vibrio exopolysaccharide (VPS), a major component of mature V. cholerae biofilm. Our study has identified a novel mechanism by which a microbiota species increases V. cholerae virulence, and we establish a plausible explanation for the increased abundance of specific microbiota species in individuals during V. cholerae infection.

Significance Statement While ample evidence suggests that the outcome of various enteric infections can be affected by the intestinal microbiota, how specific gut microbes change the behaviors of a pathogen is unclear. Here we characterize the interaction between Vibrio cholerae and a rare gut microbe, Paracoccus aminovorans, that is known to bloom in the intestines during active V. cholerae infection. These two bacteria form a dual-species biofilm structure and increases the host colonization efficiency of V. cholerae. To our knowledge, no prior study has demonstrated that an individual microbe increases V. cholerae virulence. Importantly, our study illustrates a novel mechanism of gut microbe-pathogen interaction that has the potential to alter the disease outcome.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Competing Interest Statement: No competing interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted February 02, 2021.
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Impact of a human gut microbe on Vibrio cholerae host colonization through biofilm enhancement
Kelsey Barrasso, Denise Chac, Meti D. Debela, Jason B. Harris, Regina C. LaRocque, Firas S. Midani, Firdausi Qadri, Jing Yan, Ana A. Weil, Wai-Leung Ng
bioRxiv 2021.02.01.429194; doi: https://doi.org/10.1101/2021.02.01.429194
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Impact of a human gut microbe on Vibrio cholerae host colonization through biofilm enhancement
Kelsey Barrasso, Denise Chac, Meti D. Debela, Jason B. Harris, Regina C. LaRocque, Firas S. Midani, Firdausi Qadri, Jing Yan, Ana A. Weil, Wai-Leung Ng
bioRxiv 2021.02.01.429194; doi: https://doi.org/10.1101/2021.02.01.429194

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