Cyclic‐diGMP signal transduction systems in <i>Vibrio cholerae</i>: modulation of rugosity and biofilm formation

Lim, Bentley; Beyhan, Sinem; Meir, James Y.; Yildiz, Fitnat H.

doi:10.1111/j.1365-2958.2006.05106.x

Cited by 184 publications

(251 citation statements)

References 65 publications

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“…We typically observe the concentration of c-di-GMP in the WT strain grown in Luria-Bertani (LB) media to a density of OD 600 1.0, the optical density of the cultures examined in this study, to be 0.5-2 μM. Mutation of the master high-cell-density quorum-sensing regulator of V. cholerae, hapR, locks the cells into the low-cell-density state, increasing both cdi-GMP and biofilm formation (20,33). We have found that the concentration of c-di-GMP in a ΔhapR mutant is ∼8-10 μM.…”

Section: Discussionmentioning

confidence: 99%

Quantification of high-specificity cyclic diguanylate signaling

Massie¹,

Reynolds²,

Koestler³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

145

143

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Cyclic di-GMP (c-di-GMP) is a second messenger molecule that regulates the transition between sessile and motile lifestyles in bacteria. Bacteria often encode multiple diguanylate cyclase (DGC) and phosphodiesterase (PDE) enzymes that produce and degrade c-di-GMP, respectively. Because of multiple inputs into the c-di-GMP-signaling network, it is unclear whether this system functions via high or low specificity. High-specificity signaling is characterized by individual DGCs or PDEs that are specifically associated with downstream c-di-GMP-mediated responses. In contrast, low-specificity signaling is characterized by DGCs or PDEs that modulate a general signal pool, which, in turn, controls a global c-di-GMPmediated response. To determine whether c-di-GMP functions via high or low specificity in Vibrio cholerae, we correlated the in vivo c-di-GMP concentration generated by seven DGCs, each expressed at eight different levels, to the c-di-GMP-mediated induction of biofilm formation and transcription. There was no correlation between total intracellular c-di-GMP levels and biofilm formation or gene expression when considering all states. However, individual DGCs showed a significant correlation between c-di-GMP production and c-di-GMP-mediated responses. Moreover, the rate of phenotypic change versus c-di-GMP concentration was significantly different between DGCs, suggesting that bacteria can optimize phenotypic output to c-di-GMP levels via expression or activation of specific DGCs. Our results conclusively demonstrate that c-di-GMP does not function via a simple, low-specificity signaling pathway in V. cholerae.signaling specificity | systems biology

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Section: Discussionmentioning

confidence: 99%

Quantification of high-specificity cyclic diguanylate signaling

Massie¹,

Reynolds²,

Koestler³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

145

143

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“…In S. typhimurium, the c-di-GMP phosphodiesterase CdgR is involved in resistance to phagocyte oxidase and in the cytotoxic effect in macrophages (48). In V. cholerae, the c-di-GMP phosphodiesterase VieA regulates expression of the cholera toxin genes ctxAB (49), whereas the CdgC protein carrying the EAL and GGDEF domains is involved in the control of extracellular protein secretion and flagellar biosynthesis (50). In Pseudomonas aeruginosa, the biofilm and cytotoxicity phenotypes are mediated by different GGDEF and EAL domain proteins involved in c-di-GMP metabolism (51).…”

Section: Discussionmentioning

confidence: 99%

The Flagellar Sigma Factor FliA Regulates Adhesion and Invasion of Crohn Disease-associated Escherichia coli via a Cyclic Dimeric GMP-dependent Pathway

Claret

Miquel

Vieille

et al. 2007

Journal of Biological Chemistry

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The invasion of intestinal epithelial cells by the Crohn disease-associated adherent-invasive Escherichia coli (AIEC) strain LF82 depends on surface appendages, such as type 1 pili and flagella. The absence of flagella in the AIEC strain LF82 results in a concomitant loss of type 1 pili. Here, we show that flagellar regulators, transcriptional activator FlhD 2 C 2 , and sigma factor FliA are involved in the coordination of flagellar and type 1 pili synthesis. In the deletion mutants lacking these regulators, type 1 pili synthesis, adhesion, and invasion were severely decreased. FliA expressed alone in trans was sufficient to restore these defects in both the LF82-⌬flhD and LF82-⌬fliA mutants. We related the loss of type 1 pili to the decreased expression of the FliA-dependent yhjH gene in the LF82-⌬fliA mutant. YhjH is an EAL domain phosphodiesterase involved in degradation of the bacterial second messenger cyclic dimeric GMP (c-di-GMP). Increased expression of either yhjH or an alternative c-di-GMP phosphodiesterase, yahA, partially restored type 1 pili synthesis, adhesion, and invasion in the LF82-⌬fliA mutant. Deletion of the GGDEF domain diguanylate cyclase gene, yaiC, involved in c-di-GMP synthesis in the LF82-⌬fliA mutant also partially restored these defects, whereas overexpression of the c-di-GMP receptor YcgR had the opposite effect. These findings show that in the AIEC strain LF82, FliA is a key regulatory component linking flagellar and type 1 pili synthesis and that its effect on type 1 pili is mediated, at least in part, via a c-di-GMP-dependent pathway.Many virulent bacteria, including Aeromonas caviae (1), Campylobacter jejuni (2), Clostridium difficile (3), Helicobacter pylori (4), Legionella pneumophila (5), Salmonella enterica serovar Typhimurium (6), and Vibrio cholerae (7), use flagellar motility to avoid unfavorable environments and to establish replication niches at different stages of infection. In Enterobacteriaceae, flagellar type III secretion and assembly are strictly dependent on the organization of a hierarchy that controls the sequential expression of structural and regulatory genes. In Escherichia coli and Salmonella typhimurium, the heterotetrameric transcription factor FlhD 2 C 2 (8) is positioned at the top of the flagellar expression hierarchy, where the decision to produce flagella is made (9, 10). The flhDC operon encoding FlhD 2 C 2 is transcribed from a class 1 flagellar promoter. FlhD 2 C 2 , in turn, activates 70 -dependent transcription from the class 2 flagellar promoters that drive expression of the structural subunits required for the hook-basal body structure and expression of regulatory subunits (10, 11). One of these regulatory subunits, 28 or FliA, is encoded by the fliAZ operon. FliA can associate with the core RNA polymerase to drive transcription of the class 3 flagellar genes (12). The activity of FliA depends on its interaction with the cytoplasmic anti-sigma factor FlgM, which inhibits the FliA-RNA polymerase association until completion of the hook-basal bo...

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“…It is thought that the adeptness of Vibrio cells at changing back and forth from either phenotypic variant would favor the variant derivative that is more fit for survival under the prevailing environment conditions, such as those encountered in a human host or on an environmental surface. Regulation of rugosity seems to be multifactorial and highly complex (5,17,26,36,37). Although there are some similarities, great differences are observed among organisms capable of expressing rugosity (3,36,37).…”

Section: Discussionmentioning

confidence: 99%

Rugosity in Grimontia hollisae

Curtis

Kothary

Blodgett

et al. 2007

Appl Environ Microbiol

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Grimontia hollisae, formerly Vibrio hollisae, produces both smooth and rugose colonial variants. The rugose colony phenotype is characterized by wrinkled colonies producing copious amounts of exopolysaccharide. Cells from a rugose colony grown at 30°C form rugose colonies, while the same cells grown at 37°C form smooth colonies, which are characterized by a nonwrinkled, uncrannied appearance. Stress response studies revealed that after exposure to bleach for 30 min, rugose survivors outnumbered smooth survivors.

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Cyclic‐diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation

Cited by 184 publications

References 65 publications

Quantification of high-specificity cyclic diguanylate signaling

Quantification of high-specificity cyclic diguanylate signaling

The Flagellar Sigma Factor FliA Regulates Adhesion and Invasion of Crohn Disease-associated Escherichia coli via a Cyclic Dimeric GMP-dependent Pathway

Rugosity in Grimontia hollisae

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