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Microbiota-Associated Biofilm Regulation Leads to Vibrio cholerae Resistance Against Intestinal Environmental Stress

The commensal microbes of the gut microbiota make important contributions to host defense against gastrointestinal pathogens, including Vibrio cholerae, the etiologic agent of cholera. As interindividual microbiota variation drives individual differences in infection susceptibility, we examined both...

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Autores principales: Cho, Jennifer Y., Liu, Rui, Hsiao, Ansel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9095495/
https://www.ncbi.nlm.nih.gov/pubmed/35573801
http://dx.doi.org/10.3389/fcimb.2022.861677
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author Cho, Jennifer Y.
Liu, Rui
Hsiao, Ansel
author_facet Cho, Jennifer Y.
Liu, Rui
Hsiao, Ansel
author_sort Cho, Jennifer Y.
collection PubMed
description The commensal microbes of the gut microbiota make important contributions to host defense against gastrointestinal pathogens, including Vibrio cholerae, the etiologic agent of cholera. As interindividual microbiota variation drives individual differences in infection susceptibility, we examined both host and V. cholerae gene expression during infection of suckling mice transplanted with different model human commensal communities, including an infection-susceptible configuration representing communities damaged by recurrent diarrhea and malnutrition in cholera endemic areas and a representative infection-resistant microbiota characteristic of healthy individuals. In comparison to colonization of animals with resistant microbiota, animals bearing susceptible microbiota challenged with V. cholerae downregulate genes associated with generation of reactive oxygen/nitrogen stress, while V. cholerae in these animals upregulates biofilm-associated genes. We show that V. cholerae in susceptible microbe infection contexts are more resistant to oxidative stress and inhibitory bile metabolites generated by the action of commensal microbes and that both phenotypes are dependent on biofilm-associated genes, including vpsL. We also show that susceptible and infection-resistant microbes drive different bile acid compositions in vivo by the action of bile salt hydrolase enzymes. Taken together, these findings provide a better understanding of how the microbiota uses multiple mechanisms to modulate the infection-associated host environment encountered by V. cholerae, leading to commensal-dependent differences in infection susceptibility.
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spelling pubmed-90954952022-05-13 Microbiota-Associated Biofilm Regulation Leads to Vibrio cholerae Resistance Against Intestinal Environmental Stress Cho, Jennifer Y. Liu, Rui Hsiao, Ansel Front Cell Infect Microbiol Cellular and Infection Microbiology The commensal microbes of the gut microbiota make important contributions to host defense against gastrointestinal pathogens, including Vibrio cholerae, the etiologic agent of cholera. As interindividual microbiota variation drives individual differences in infection susceptibility, we examined both host and V. cholerae gene expression during infection of suckling mice transplanted with different model human commensal communities, including an infection-susceptible configuration representing communities damaged by recurrent diarrhea and malnutrition in cholera endemic areas and a representative infection-resistant microbiota characteristic of healthy individuals. In comparison to colonization of animals with resistant microbiota, animals bearing susceptible microbiota challenged with V. cholerae downregulate genes associated with generation of reactive oxygen/nitrogen stress, while V. cholerae in these animals upregulates biofilm-associated genes. We show that V. cholerae in susceptible microbe infection contexts are more resistant to oxidative stress and inhibitory bile metabolites generated by the action of commensal microbes and that both phenotypes are dependent on biofilm-associated genes, including vpsL. We also show that susceptible and infection-resistant microbes drive different bile acid compositions in vivo by the action of bile salt hydrolase enzymes. Taken together, these findings provide a better understanding of how the microbiota uses multiple mechanisms to modulate the infection-associated host environment encountered by V. cholerae, leading to commensal-dependent differences in infection susceptibility. Frontiers Media S.A. 2022-04-27 /pmc/articles/PMC9095495/ /pubmed/35573801 http://dx.doi.org/10.3389/fcimb.2022.861677 Text en Copyright © 2022 Cho, Liu and Hsiao https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cellular and Infection Microbiology
Cho, Jennifer Y.
Liu, Rui
Hsiao, Ansel
Microbiota-Associated Biofilm Regulation Leads to Vibrio cholerae Resistance Against Intestinal Environmental Stress
title Microbiota-Associated Biofilm Regulation Leads to Vibrio cholerae Resistance Against Intestinal Environmental Stress
title_full Microbiota-Associated Biofilm Regulation Leads to Vibrio cholerae Resistance Against Intestinal Environmental Stress
title_fullStr Microbiota-Associated Biofilm Regulation Leads to Vibrio cholerae Resistance Against Intestinal Environmental Stress
title_full_unstemmed Microbiota-Associated Biofilm Regulation Leads to Vibrio cholerae Resistance Against Intestinal Environmental Stress
title_short Microbiota-Associated Biofilm Regulation Leads to Vibrio cholerae Resistance Against Intestinal Environmental Stress
title_sort microbiota-associated biofilm regulation leads to vibrio cholerae resistance against intestinal environmental stress
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9095495/
https://www.ncbi.nlm.nih.gov/pubmed/35573801
http://dx.doi.org/10.3389/fcimb.2022.861677
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