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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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-04-01
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| Series: | Frontiers in Cellular and Infection Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fcimb.2022.861677/full |
| _version_ | 1818275527445708800 |
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| author | Jennifer Y. Cho Jennifer Y. Cho Rui Liu Rui Liu Ansel Hsiao |
| author_facet | Jennifer Y. Cho Jennifer Y. Cho Rui Liu Rui Liu Ansel Hsiao |
| author_sort | Jennifer Y. Cho |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-12T22:31:10Z |
| format | Article |
| id | doaj.art-f2456efbd9b542bfb8a166706285ca7d |
| institution | Directory Open Access Journal |
| issn | 2235-2988 |
| language | English |
| last_indexed | 2024-12-12T22:31:10Z |
| publishDate | 2022-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj.art-f2456efbd9b542bfb8a166706285ca7d2022-12-22T00:09:36ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882022-04-011210.3389/fcimb.2022.861677861677Microbiota-Associated Biofilm Regulation Leads to Vibrio cholerae Resistance Against Intestinal Environmental StressJennifer Y. Cho0Jennifer Y. Cho1Rui Liu2Rui Liu3Ansel Hsiao4Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA, United StatesDepartment of Biochemistry, University of California, Riverside, Riverside, CA, United StatesDepartment of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA, United StatesGraduate Program in Genetics, Genomics, and Bioinformatics, University of California, Riverside, Riverside, CA, United StatesDepartment of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA, United StatesThe 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.https://www.frontiersin.org/articles/10.3389/fcimb.2022.861677/fullbiofilmVibrio choleraepathogenesismicrobiotabile acidsreactive oxygen species |
| spellingShingle | Jennifer Y. Cho Jennifer Y. Cho Rui Liu Rui Liu Ansel Hsiao Microbiota-Associated Biofilm Regulation Leads to Vibrio cholerae Resistance Against Intestinal Environmental Stress Frontiers in Cellular and Infection Microbiology biofilm Vibrio cholerae pathogenesis microbiota bile acids reactive oxygen species |
| 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 | biofilm Vibrio cholerae pathogenesis microbiota bile acids reactive oxygen species |
| url | https://www.frontiersin.org/articles/10.3389/fcimb.2022.861677/full |
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