Dissecting the cyclic di‐guanylate monophosphate signalling network regulating motility in <i>Salmonella enterica</i> serovar Typhimurium

Guyon, Soazig Le; Simm, Roger; Rehn, Mikael; Römling, Ute

doi:10.1111/1462-2920.13057

Cited by 23 publications

(16 citation statements)

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“…Of note, YhjH has been identified as the key PDE to regulate motility (Le Guyon et al., ; Pesavento et al., ; Simm et al., ). Although YhjH was conserved in all 61 strains (Povolotsky & Hengge, ), one or two aa substitutions are present in YhjH of the semi‐constitutive rdar strains except for Fec101.…”

Section: Discussionmentioning

confidence: 99%

“…C-di-GMP inhibits motility by binding to the molecular brake protein YcgR (Boehm et al, 2010;Paul, Nieto, Carlquist, Blair, & Harshey, 2010;Ryjenkov, Simm, Römling, & Gomelsky, 2006) and through production of cellulose (Le Guyon, Simm, Rehn, & Römling, 2015;Zorraquino et al, 2013)). Motility is promoted by the key PDE YhjH, which effectively removes motility-dedicated c-di-GMP (Le Guyon et al, 2015;Pesavento et al, 2008;Simm et al, 2007) and consequently the motility/sessility switch is observed upon deletion of YhjH (Simm et al, 2007) or, more pronounced, upon overexpression of DGCs and PDEs (Simm et al, 2004). Although csgD represses swimming motility in E. coli K-12 (Dudin et al, 2014;Ogasawara, Yamamoto, & Ishihama, 2011), a correlation between csgD expression and motility was not observed.…”

Section: Rdar Morphotype Formation Is Unrelated To the Liquid Biofimentioning

confidence: 99%

“…Of note, YhjH has been identified as the key PDE to regulate motility (Le Guyon et al, 2015;Pesavento et al, 2008;Simm et al, 2007).…”

Section: Variability In C-di-gmp Turnover Proteins Indicates Adaptamentioning

confidence: 99%

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Alterations of c‐di‐GMP turnover proteins modulate semi‐constitutive rdar biofilm formation in commensal and uropathogenic Escherichia coli

Cimdins

Simm

et al. 2017

MicrobiologyOpen

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Agar plate‐based biofilm of enterobacteria like Escherichia coli is characterized by expression of the extracellular matrix components amyloid curli and cellulose exopolysaccharide, which can be visually enhanced upon addition of the dye Congo Red, resulting in a red, dry, and rough (rdar) colony morphology. Expression of the rdar morphotype depends on the transcriptional regulator CsgD and occurs predominantly at ambient temperature in model strains. In contrast, commensal and pathogenic isolates frequently express the csgD‐dependent rdar morphotype semi‐constitutively, also at human host body temperature. To unravel the molecular basis of temperature‐independent rdar morphotype expression, biofilm components and c‐di‐GMP turnover proteins of seven commensal and uropathogenic E. coli isolates were analyzed. A diversity within the c‐di‐GMP signaling network was uncovered which suggests alteration of activity of the trigger phosphodiesterase YciR to contribute to (up)regulation of csgD expression and consequently semi‐constitutive rdar morphotype development.

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Section: Discussionmentioning

confidence: 99%

Section: Rdar Morphotype Formation Is Unrelated To the Liquid Biofimentioning

confidence: 99%

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Alterations of c‐di‐GMP turnover proteins modulate semi‐constitutive rdar biofilm formation in commensal and uropathogenic Escherichia coli

Cimdins

Simm

et al. 2017

MicrobiologyOpen

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“…C‐di‐GMP binds two PilZ domain protein receptors to independently regulate flagella and cellulose. YcgR binds c‐di‐GMP and inhibits flagellar rotation . BcsA binds c‐di‐GMP leading to an allosteric shift that no longer occludes the active site of BscB, the cellulose synthase, thereby allowing UDP‐glucose to be polymerized into cellulose .…”

Section: Gastrointestinal Pathogensmentioning

confidence: 99%

Cyclic‐di‐GMP regulation of virulence in bacterial pathogens

Hall

Lee

2017

WIREs RNA

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Signaling pathways allow bacteria to adapt to changing environments. For pathogenic bacteria, signaling pathways allow for timely expression of virulence factors and the repression of antivirulence factors within the mammalian host. As the bacteria exit the mammalian host, signaling pathways enable the expression of factors promoting survival in the environment and/or nonmammalian hosts. One such signaling pathway uses the dinucleotide cyclic-di-GMP (c-di-GMP), and many bacterial genomes encode numerous proteins that are responsible for synthesizing and degrading c-di-GMP. Once made, c-di-GMP binds to individual protein and RNA receptors to allosterically alter the macromolecule function to drive phenotypic changes. Each bacterial genome encodes unique sets of genes for c-di-GMP signaling and virulence factors so the regulation by c-di-GMP is organism specific. Recent works have pointed to evidence that c-di-GMP regulates virulence in different bacterial pathogens of mammalian hosts. In this review, we discuss the criteria for determining the contribution of signaling nucleotides to pathogenesis using a well-characterized signaling nucleotide, cyclic AMP (cAMP), in Pseudomonas aeruginosa. Using these criteria, we review the roles of c-di-GMP in mediating virulence and highlight common themes that exist among eight diverse pathogens that cause different diseases through different routes of infection and transmission. © 2017 Wiley Periodicals, Inc. How to cite this article:WIREs RNA 2018, 9:e1454. doi: 10.1002/wrna.1454 INTRODUCTIONB is-(3 0 -5 0 )-cyclic dimeric guanosine monophosphate (c-di-GMP) is a widely utilized signaling pathway that regulates bacterial adaptation to different environments. 1 C-di-GMP is synthesized from two GTP by diguanylate cyclases (DGCs) that contain a GGDEF domain and degraded into pGpG by phosphodiesterases (PDE-As) that contain EAL or HD-GYP domain. Signaling by c-di-GMP is completed when pGpG is degraded further to GMP by oligoribonuclease and related RNA degradation enzymes. [2][3][4] Thus, c-di-GMP represents one of the shortest signaling ribonucleotides. In addition, a number of genes can encode proteins with both GGDEF and EAL domains (GGDEF-EAL), indicating that levels of c-di-GMP in the cell are regulated by a complicated number of synthetic and degradative enzymes. Once made, c-di-GMP binds a diverse set of protein receptors and RNA riboswitches. 1 C-di-GMP binding to molecular receptors allosterically alters their function and downstream cellular phenotypes. 5 Genes encoding c-di-GMP signaling components are found in a large number of bacterial pathogens. This review seeks to cover the contribution of c-di-GMP signaling to bacterial pathogenesis for a number of different pathogens to identify common themes. For this review, virulence and pathogenesis is considered as the ability of the bacteria to replicate and cause disease symptoms in the mammalian host. Owing to space limitation, for each pathogen, we have referenced reviews that cover their virulence factors and their c...

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“…genome: the flagellar brake YcgR that inhibits motility (7) and the cellulose synthase BcsA that generates the extracellular polysaccharide cellulose (8,9). The S. Typhimurium c-di-GMP pathway has been well studied in regard to established in vitro c-di-GMP-regulated phenotypes such as motility and biofilm formation (10)(11)(12). However, relatively little is known about the role of c-di-GMP in the context of eukaryotic cell infection-and even less is known about the specific CMEs and signals that regulate [c-di-GMP] in these conditions-making this an area requiring further study.…”

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confidence: 99%

Cyclic-di-GMP regulation promotes survival of a slow-replicating subpopulation of intracellular Salmonella Typhimurium

Petersen

Mills

Miller

2019

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

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SalmonellaTyphimurium can invade and survive within macrophages where the bacterium encounters a range of host environmental conditions. Like many bacteria,S.Typhimurium rapidly responds to changing environments by the use of second messengers such as cyclic di-GMP (c-di-GMP). Here, we generate a fluorescent biosensor to measure c-di-GMP concentrations in thousands of individual bacteria during macrophage infection and to define the sensor enzymes important to c-di-GMP regulation. Three sensor phosphodiesterases were identified as critical to maintaining low c-di-GMP concentrations generated after initial phagocytosis by macrophages. Maintenance of low c-di-GMP concentrations by these phosphodiesterases was required to promote survival within macrophages and virulence for mice. Attenuation ofS. Typhimurium virulence was due to overproduction of c-di-GMP−regulated cellulose, as deletion of the cellulose synthase machinery restored virulence to a strain lacking enzymatic activity of the three phosphodiesterases. We further identified that the cellulose-mediated reduction in survival was constrained to a slow-replicating persister population ofS.Typhimurium induced within the macrophage intracellular environment. As utilization of glucose has been shown to be required forS.Typhimurium macrophage survival, one possible hypothesis is that this persister population requires the glucose redirected to the synthesis of cellulose to maintain a slow-replicating, metabolically active state.

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Dissecting the cyclic di‐guanylate monophosphate signalling network regulating motility in Salmonella enterica serovar Typhimurium

Cited by 23 publications

References 28 publications

Alterations of c‐di‐GMP turnover proteins modulate semi‐constitutive rdar biofilm formation in commensal and uropathogenic Escherichia coli

Alterations of c‐di‐GMP turnover proteins modulate semi‐constitutive rdar biofilm formation in commensal and uropathogenic Escherichia coli

Cyclic‐di‐GMP regulation of virulence in bacterial pathogens

Cyclic-di-GMP regulation promotes survival of a slow-replicating subpopulation of intracellular Salmonella Typhimurium

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