Functional Specialization in <italic toggle="yes">Vibrio cholerae</italic> Diguanylate Cyclases: Distinct Modes of Motility Suppression and c-di-GMP Production

ABSTRACT Vibrio cholerae biofilm formation and associated motility suppression are correlated with increased concentrations of cyclic diguanylate monophosphate (c-di-GMP), which are in turn driven by increased levels and/or activity of diguanylate cyclases (DGCs). To further our understanding of how...

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Autores principales:	David Zamorano-Sánchez, Wujing Xian, Calvin K. Lee, Mauro Salinas, Wiriya Thongsomboon, Lynette Cegelski, Gerard C. L. Wong, Fitnat H. Yildiz
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	biofilm motility Vibrio cholerae c-di-GMP Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1799c15680334db5b2cd9be4e80e0196
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spelling	oai:doaj.org-article:1799c15680334db5b2cd9be4e80e01962021-11-15T15:55:25ZFunctional Specialization in <italic toggle="yes">Vibrio cholerae</italic> Diguanylate Cyclases: Distinct Modes of Motility Suppression and c-di-GMP Production10.1128/mBio.00670-192150-7511https://doaj.org/article/1799c15680334db5b2cd9be4e80e01962019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00670-19https://doaj.org/toc/2150-7511ABSTRACT Vibrio cholerae biofilm formation and associated motility suppression are correlated with increased concentrations of cyclic diguanylate monophosphate (c-di-GMP), which are in turn driven by increased levels and/or activity of diguanylate cyclases (DGCs). To further our understanding of how c-di-GMP modulators in V. cholerae individually and collectively influence motility with cellular resolution, we determined how DGCs CdgD and CdgH impact intracellular c-di-GMP levels, motility, and biofilm formation. Our results indicated that CdgH strongly influences swim speed distributions; cells in which cdgH was deleted had higher average swim speeds than wild-type cells. Furthermore, our results suggest that CdgD, rather than CdgH, is the dominant DGC responsible for postattachment c-di-GMP production in biofilms. Lipopolysaccharide (LPS) biosynthesis genes were found to be extragenic bypass suppressors of the motility phenotypes of strains ΔcdgD and ΔcdgH. We compared the motility regulation mechanism of the DGCs with that of Gmd, an LPS O-antigen biosynthesis protein, and discovered that comodulation of c-di-GMP levels by these motility effectors can be positively or negatively cooperative rather than simply additive. Taken together, these results suggest that different environmental and metabolic inputs orchestrate DGC responses of V. cholerae via c-di-GMP production and motility modulation. IMPORTANCE Cyclic diguanylate monophosphate (c-di-GMP) is a broadly conserved bacterial signaling molecule that affects motility, biofilm formation, and virulence. Although it has been known that high intracellular concentrations of c-di-GMP correlate with motility suppression and biofilm formation, how the 53 predicted c-di-GMP modulators in Vibrio cholerae collectively influence motility is not understood in detail. Here we used a combination of plate assays and single-cell tracking methods to correlate motility and biofilm formation outcomes with specific enzymes involved in c-di-GMP synthesis in Vibrio cholerae, the causative agent of the disease cholera.David Zamorano-SánchezWujing XianCalvin K. LeeMauro SalinasWiriya ThongsomboonLynette CegelskiGerard C. L. WongFitnat H. YildizAmerican Society for MicrobiologyarticlebiofilmmotilityVibrio choleraec-di-GMPMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	biofilm motility Vibrio cholerae c-di-GMP Microbiology QR1-502
spellingShingle	biofilm motility Vibrio cholerae c-di-GMP Microbiology QR1-502 David Zamorano-Sánchez Wujing Xian Calvin K. Lee Mauro Salinas Wiriya Thongsomboon Lynette Cegelski Gerard C. L. Wong Fitnat H. Yildiz Functional Specialization in <italic toggle="yes">Vibrio cholerae</italic> Diguanylate Cyclases: Distinct Modes of Motility Suppression and c-di-GMP Production
description	ABSTRACT Vibrio cholerae biofilm formation and associated motility suppression are correlated with increased concentrations of cyclic diguanylate monophosphate (c-di-GMP), which are in turn driven by increased levels and/or activity of diguanylate cyclases (DGCs). To further our understanding of how c-di-GMP modulators in V. cholerae individually and collectively influence motility with cellular resolution, we determined how DGCs CdgD and CdgH impact intracellular c-di-GMP levels, motility, and biofilm formation. Our results indicated that CdgH strongly influences swim speed distributions; cells in which cdgH was deleted had higher average swim speeds than wild-type cells. Furthermore, our results suggest that CdgD, rather than CdgH, is the dominant DGC responsible for postattachment c-di-GMP production in biofilms. Lipopolysaccharide (LPS) biosynthesis genes were found to be extragenic bypass suppressors of the motility phenotypes of strains ΔcdgD and ΔcdgH. We compared the motility regulation mechanism of the DGCs with that of Gmd, an LPS O-antigen biosynthesis protein, and discovered that comodulation of c-di-GMP levels by these motility effectors can be positively or negatively cooperative rather than simply additive. Taken together, these results suggest that different environmental and metabolic inputs orchestrate DGC responses of V. cholerae via c-di-GMP production and motility modulation. IMPORTANCE Cyclic diguanylate monophosphate (c-di-GMP) is a broadly conserved bacterial signaling molecule that affects motility, biofilm formation, and virulence. Although it has been known that high intracellular concentrations of c-di-GMP correlate with motility suppression and biofilm formation, how the 53 predicted c-di-GMP modulators in Vibrio cholerae collectively influence motility is not understood in detail. Here we used a combination of plate assays and single-cell tracking methods to correlate motility and biofilm formation outcomes with specific enzymes involved in c-di-GMP synthesis in Vibrio cholerae, the causative agent of the disease cholera.
format	article
author	David Zamorano-Sánchez Wujing Xian Calvin K. Lee Mauro Salinas Wiriya Thongsomboon Lynette Cegelski Gerard C. L. Wong Fitnat H. Yildiz
author_facet	David Zamorano-Sánchez Wujing Xian Calvin K. Lee Mauro Salinas Wiriya Thongsomboon Lynette Cegelski Gerard C. L. Wong Fitnat H. Yildiz
author_sort	David Zamorano-Sánchez
title	Functional Specialization in <italic toggle="yes">Vibrio cholerae</italic> Diguanylate Cyclases: Distinct Modes of Motility Suppression and c-di-GMP Production
title_short	Functional Specialization in <italic toggle="yes">Vibrio cholerae</italic> Diguanylate Cyclases: Distinct Modes of Motility Suppression and c-di-GMP Production
title_full	Functional Specialization in <italic toggle="yes">Vibrio cholerae</italic> Diguanylate Cyclases: Distinct Modes of Motility Suppression and c-di-GMP Production
title_fullStr	Functional Specialization in <italic toggle="yes">Vibrio cholerae</italic> Diguanylate Cyclases: Distinct Modes of Motility Suppression and c-di-GMP Production
title_full_unstemmed	Functional Specialization in <italic toggle="yes">Vibrio cholerae</italic> Diguanylate Cyclases: Distinct Modes of Motility Suppression and c-di-GMP Production
title_sort	functional specialization in <italic toggle="yes">vibrio cholerae</italic> diguanylate cyclases: distinct modes of motility suppression and c-di-gmp production
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/1799c15680334db5b2cd9be4e80e0196
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Functional Specialization in <italic toggle="yes">Vibrio cholerae</italic> Diguanylate Cyclases: Distinct Modes of Motility Suppression and c-di-GMP Production

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