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High Levels of Cyclic Diguanylate Interfere with Beneficial Bacterial Colonization

During colonization of the Hawaiian bobtail squid (Euprymna scolopes), Vibrio fischeri bacteria undergo a lifestyle transition from a planktonic motile state in the environment to a biofilm state in host mucus. Cyclic diguanylate (c-di-GMP) is a cytoplasmic signaling molecule that is important for r...

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Autores principales: Isenberg, Ruth Y., Christensen, David G., Visick, Karen L., Mandel, Mark J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9426504/
https://www.ncbi.nlm.nih.gov/pubmed/35916402
http://dx.doi.org/10.1128/mbio.01671-22
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author Isenberg, Ruth Y.
Christensen, David G.
Visick, Karen L.
Mandel, Mark J.
author_facet Isenberg, Ruth Y.
Christensen, David G.
Visick, Karen L.
Mandel, Mark J.
author_sort Isenberg, Ruth Y.
collection PubMed
description During colonization of the Hawaiian bobtail squid (Euprymna scolopes), Vibrio fischeri bacteria undergo a lifestyle transition from a planktonic motile state in the environment to a biofilm state in host mucus. Cyclic diguanylate (c-di-GMP) is a cytoplasmic signaling molecule that is important for regulating motility-biofilm transitions in many bacterial species. V. fischeri encodes 50 proteins predicted to synthesize and/or degrade c-di-GMP, but a role for c-di-GMP regulation during host colonization has not been investigated. We examined strains exhibiting either low or high levels of c-di-GMP during squid colonization and found that while a low-c-di-GMP strain had no colonization defect, a high c-di-GMP strain was severely impaired. Expression of a heterologous c-di-GMP phosphodiesterase restored colonization, demonstrating that the effect is due to high c-di-GMP levels. In the constitutive high-c-di-GMP state, colonizing V. fischeri exhibited reduced motility, altered biofilm aggregate morphology, and a regulatory interaction where transcription of one polysaccharide locus is inhibited by the presence of the other polysaccharide. Our results highlight the importance of proper c-di-GMP regulation during beneficial animal colonization, illustrate multiple pathways regulated by c-di-GMP in the host, and uncover an interplay of multiple exopolysaccharide systems in host-associated aggregates.
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spelling pubmed-94265042022-08-31 High Levels of Cyclic Diguanylate Interfere with Beneficial Bacterial Colonization Isenberg, Ruth Y. Christensen, David G. Visick, Karen L. Mandel, Mark J. mBio Research Article During colonization of the Hawaiian bobtail squid (Euprymna scolopes), Vibrio fischeri bacteria undergo a lifestyle transition from a planktonic motile state in the environment to a biofilm state in host mucus. Cyclic diguanylate (c-di-GMP) is a cytoplasmic signaling molecule that is important for regulating motility-biofilm transitions in many bacterial species. V. fischeri encodes 50 proteins predicted to synthesize and/or degrade c-di-GMP, but a role for c-di-GMP regulation during host colonization has not been investigated. We examined strains exhibiting either low or high levels of c-di-GMP during squid colonization and found that while a low-c-di-GMP strain had no colonization defect, a high c-di-GMP strain was severely impaired. Expression of a heterologous c-di-GMP phosphodiesterase restored colonization, demonstrating that the effect is due to high c-di-GMP levels. In the constitutive high-c-di-GMP state, colonizing V. fischeri exhibited reduced motility, altered biofilm aggregate morphology, and a regulatory interaction where transcription of one polysaccharide locus is inhibited by the presence of the other polysaccharide. Our results highlight the importance of proper c-di-GMP regulation during beneficial animal colonization, illustrate multiple pathways regulated by c-di-GMP in the host, and uncover an interplay of multiple exopolysaccharide systems in host-associated aggregates. American Society for Microbiology 2022-08-02 /pmc/articles/PMC9426504/ /pubmed/35916402 http://dx.doi.org/10.1128/mbio.01671-22 Text en Copyright © 2022 Isenberg et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Isenberg, Ruth Y.
Christensen, David G.
Visick, Karen L.
Mandel, Mark J.
High Levels of Cyclic Diguanylate Interfere with Beneficial Bacterial Colonization
title High Levels of Cyclic Diguanylate Interfere with Beneficial Bacterial Colonization
title_full High Levels of Cyclic Diguanylate Interfere with Beneficial Bacterial Colonization
title_fullStr High Levels of Cyclic Diguanylate Interfere with Beneficial Bacterial Colonization
title_full_unstemmed High Levels of Cyclic Diguanylate Interfere with Beneficial Bacterial Colonization
title_short High Levels of Cyclic Diguanylate Interfere with Beneficial Bacterial Colonization
title_sort high levels of cyclic diguanylate interfere with beneficial bacterial colonization
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9426504/
https://www.ncbi.nlm.nih.gov/pubmed/35916402
http://dx.doi.org/10.1128/mbio.01671-22
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