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Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut

Bile acids (BAs) mediate the crosstalk between human and microbial cells and influence diseases including Clostridioides difficile infection (CDI). While bile salt hydrolases (BSHs) shape the BA pool by deconjugating conjugated BAs, the basis for their substrate selectivity and impact on C. difficil...

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Autores principales: Foley, Matthew H., Walker, Morgan E., Stewart, Allison K., O’Flaherty, Sarah, Gentry, Emily C., Patel, Shakshi, Beaty, Violet V., Allen, Garrison, Pan, Meichen, Simpson, Joshua B., Perkins, Caroline, Vanhoy, Molly E., Dougherty, Michael K., McGill, Sarah K., Gulati, Ajay S., Dorrestein, Pieter C., Baker, Erin S., Redinbo, Matthew R., Barrangou, Rodolphe, Theriot, Casey M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10066039/
https://www.ncbi.nlm.nih.gov/pubmed/36914755
http://dx.doi.org/10.1038/s41564-023-01337-7
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author Foley, Matthew H.
Walker, Morgan E.
Stewart, Allison K.
O’Flaherty, Sarah
Gentry, Emily C.
Patel, Shakshi
Beaty, Violet V.
Allen, Garrison
Pan, Meichen
Simpson, Joshua B.
Perkins, Caroline
Vanhoy, Molly E.
Dougherty, Michael K.
McGill, Sarah K.
Gulati, Ajay S.
Dorrestein, Pieter C.
Baker, Erin S.
Redinbo, Matthew R.
Barrangou, Rodolphe
Theriot, Casey M.
author_facet Foley, Matthew H.
Walker, Morgan E.
Stewart, Allison K.
O’Flaherty, Sarah
Gentry, Emily C.
Patel, Shakshi
Beaty, Violet V.
Allen, Garrison
Pan, Meichen
Simpson, Joshua B.
Perkins, Caroline
Vanhoy, Molly E.
Dougherty, Michael K.
McGill, Sarah K.
Gulati, Ajay S.
Dorrestein, Pieter C.
Baker, Erin S.
Redinbo, Matthew R.
Barrangou, Rodolphe
Theriot, Casey M.
author_sort Foley, Matthew H.
collection PubMed
description Bile acids (BAs) mediate the crosstalk between human and microbial cells and influence diseases including Clostridioides difficile infection (CDI). While bile salt hydrolases (BSHs) shape the BA pool by deconjugating conjugated BAs, the basis for their substrate selectivity and impact on C. difficile remain elusive. Here we survey the diversity of BSHs in the gut commensals Lactobacillaceae, which are commonly used as probiotics, and other members of the human gut microbiome. We structurally pinpoint a loop that predicts BSH preferences for either glycine or taurine substrates. BSHs with varying specificities were shown to restrict C. difficile spore germination and growth in vitro and colonization in pre-clinical in vivo models of CDI. Furthermore, BSHs reshape the pool of microbial conjugated bile acids (MCBAs) in the murine gut, and these MCBAs can further restrict C. difficile virulence in vitro. The recognition of conjugated BAs by BSHs defines the resulting BA pool, including the expansive MCBAs. This work provides insights into the structural basis of BSH mechanisms that shape the BA landscape and promote colonization resistance against C. difficile.
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spelling pubmed-100660392023-04-02 Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut Foley, Matthew H. Walker, Morgan E. Stewart, Allison K. O’Flaherty, Sarah Gentry, Emily C. Patel, Shakshi Beaty, Violet V. Allen, Garrison Pan, Meichen Simpson, Joshua B. Perkins, Caroline Vanhoy, Molly E. Dougherty, Michael K. McGill, Sarah K. Gulati, Ajay S. Dorrestein, Pieter C. Baker, Erin S. Redinbo, Matthew R. Barrangou, Rodolphe Theriot, Casey M. Nat Microbiol Article Bile acids (BAs) mediate the crosstalk between human and microbial cells and influence diseases including Clostridioides difficile infection (CDI). While bile salt hydrolases (BSHs) shape the BA pool by deconjugating conjugated BAs, the basis for their substrate selectivity and impact on C. difficile remain elusive. Here we survey the diversity of BSHs in the gut commensals Lactobacillaceae, which are commonly used as probiotics, and other members of the human gut microbiome. We structurally pinpoint a loop that predicts BSH preferences for either glycine or taurine substrates. BSHs with varying specificities were shown to restrict C. difficile spore germination and growth in vitro and colonization in pre-clinical in vivo models of CDI. Furthermore, BSHs reshape the pool of microbial conjugated bile acids (MCBAs) in the murine gut, and these MCBAs can further restrict C. difficile virulence in vitro. The recognition of conjugated BAs by BSHs defines the resulting BA pool, including the expansive MCBAs. This work provides insights into the structural basis of BSH mechanisms that shape the BA landscape and promote colonization resistance against C. difficile. Nature Publishing Group UK 2023-03-13 2023 /pmc/articles/PMC10066039/ /pubmed/36914755 http://dx.doi.org/10.1038/s41564-023-01337-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Foley, Matthew H.
Walker, Morgan E.
Stewart, Allison K.
O’Flaherty, Sarah
Gentry, Emily C.
Patel, Shakshi
Beaty, Violet V.
Allen, Garrison
Pan, Meichen
Simpson, Joshua B.
Perkins, Caroline
Vanhoy, Molly E.
Dougherty, Michael K.
McGill, Sarah K.
Gulati, Ajay S.
Dorrestein, Pieter C.
Baker, Erin S.
Redinbo, Matthew R.
Barrangou, Rodolphe
Theriot, Casey M.
Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut
title Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut
title_full Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut
title_fullStr Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut
title_full_unstemmed Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut
title_short Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut
title_sort bile salt hydrolases shape the bile acid landscape and restrict clostridioides difficile growth in the murine gut
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10066039/
https://www.ncbi.nlm.nih.gov/pubmed/36914755
http://dx.doi.org/10.1038/s41564-023-01337-7
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