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...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2022-03-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3001585 |
| _version_ | 1818239669984296960 |
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| author | Andrew A Bridges Jojo A Prentice Chenyi Fei Ned S Wingreen Bonnie L Bassler |
| author_facet | Andrew A Bridges Jojo A Prentice Chenyi Fei Ned S Wingreen Bonnie L Bassler |
| author_sort | Andrew A Bridges |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-12T13:01:14Z |
| format | Article |
| id | doaj.art-e37ea7b17a5b450993e0774cbfd2f5bd |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-12-12T13:01:14Z |
| publishDate | 2022-03-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-e37ea7b17a5b450993e0774cbfd2f5bd2022-12-22T00:23:47ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852022-03-01203e300158510.1371/journal.pbio.3001585Quantitative input-output dynamics of a c-di-GMP signal transduction cascade in Vibrio cholerae.Andrew A BridgesJojo A PrenticeChenyi FeiNed S WingreenBonnie L BasslerBacterial 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.https://doi.org/10.1371/journal.pbio.3001585 |
| spellingShingle | Andrew A Bridges Jojo A Prentice Chenyi Fei Ned S Wingreen Bonnie L Bassler Quantitative input-output dynamics of a c-di-GMP signal transduction cascade in Vibrio cholerae. PLoS Biology |
| 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 |
| url | https://doi.org/10.1371/journal.pbio.3001585 |
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