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Quantitative input–output dynamics of a c-di-GMP signal transduction cascade in Vibrio cholerae

Bacterial biofilms are multicellular communities that collectively overcome environmental threats and clinical treatments. To regulate the biofilm lifecycle, bacteria commonly transduce sensory information via the second messenger molecule cyclic diguanylate (c-di-GMP). Using experimental and modeli...

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Autores principales: Bridges, Andrew A., Prentice, Jojo A., Fei, Chenyi, Wingreen, Ned S., Bassler, Bonnie L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8967002/
https://www.ncbi.nlm.nih.gov/pubmed/35302986
http://dx.doi.org/10.1371/journal.pbio.3001585
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author Bridges, Andrew A.
Prentice, Jojo A.
Fei, Chenyi
Wingreen, Ned S.
Bassler, Bonnie L.
author_facet Bridges, Andrew A.
Prentice, Jojo A.
Fei, Chenyi
Wingreen, Ned S.
Bassler, Bonnie L.
author_sort Bridges, Andrew A.
collection PubMed
description Bacterial biofilms are multicellular communities that collectively overcome environmental threats and clinical treatments. To regulate the biofilm lifecycle, bacteria commonly transduce sensory information via the second messenger molecule cyclic diguanylate (c-di-GMP). Using experimental and modeling approaches, we quantitatively capture c-di-GMP signal transmission via the bifunctional polyamine receptor NspS-MbaA, from ligand binding to output, in the pathogen Vibrio cholerae. Upon binding of norspermidine or spermidine, NspS-MbaA synthesizes or degrades c-di-GMP, respectively, which, in turn, drives alterations specifically to biofilm gene expression. A long-standing question is how output specificity is achieved via c-di-GMP, a diffusible molecule that regulates dozens of effectors. We show that NspS-MbaA signals locally to specific effectors, sensitizing V. cholerae to polyamines. However, local signaling is not required for specificity, as changes to global cytoplasmic c-di-GMP levels can selectively regulate biofilm genes. This work establishes the input–output dynamics underlying c-di-GMP signaling, which could be useful for developing bacterial manipulation strategies.
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spelling pubmed-89670022022-03-31 Quantitative input–output dynamics of a c-di-GMP signal transduction cascade in Vibrio cholerae Bridges, Andrew A. Prentice, Jojo A. Fei, Chenyi Wingreen, Ned S. Bassler, Bonnie L. PLoS Biol Research Article Bacterial biofilms are multicellular communities that collectively overcome environmental threats and clinical treatments. To regulate the biofilm lifecycle, bacteria commonly transduce sensory information via the second messenger molecule cyclic diguanylate (c-di-GMP). Using experimental and modeling approaches, we quantitatively capture c-di-GMP signal transmission via the bifunctional polyamine receptor NspS-MbaA, from ligand binding to output, in the pathogen Vibrio cholerae. Upon binding of norspermidine or spermidine, NspS-MbaA synthesizes or degrades c-di-GMP, respectively, which, in turn, drives alterations specifically to biofilm gene expression. A long-standing question is how output specificity is achieved via c-di-GMP, a diffusible molecule that regulates dozens of effectors. We show that NspS-MbaA signals locally to specific effectors, sensitizing V. cholerae to polyamines. However, local signaling is not required for specificity, as changes to global cytoplasmic c-di-GMP levels can selectively regulate biofilm genes. This work establishes the input–output dynamics underlying c-di-GMP signaling, which could be useful for developing bacterial manipulation strategies. Public Library of Science 2022-03-18 /pmc/articles/PMC8967002/ /pubmed/35302986 http://dx.doi.org/10.1371/journal.pbio.3001585 Text en © 2022 Bridges et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Bridges, Andrew A.
Prentice, Jojo A.
Fei, Chenyi
Wingreen, Ned S.
Bassler, Bonnie L.
Quantitative input–output dynamics of a c-di-GMP signal transduction cascade in Vibrio cholerae
title Quantitative input–output dynamics of a c-di-GMP signal transduction cascade in Vibrio cholerae
title_full Quantitative input–output dynamics of a c-di-GMP signal transduction cascade in Vibrio cholerae
title_fullStr Quantitative input–output dynamics of a c-di-GMP signal transduction cascade in Vibrio cholerae
title_full_unstemmed Quantitative input–output dynamics of a c-di-GMP signal transduction cascade in Vibrio cholerae
title_short Quantitative input–output dynamics of a c-di-GMP signal transduction cascade in Vibrio cholerae
title_sort quantitative input–output dynamics of a c-di-gmp signal transduction cascade in vibrio cholerae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8967002/
https://www.ncbi.nlm.nih.gov/pubmed/35302986
http://dx.doi.org/10.1371/journal.pbio.3001585
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