Regulation of Escherichia coli cell division genes ftsA and ftsZ by the two‐component system rcsC–rcsB

Carballès, Fabrice; Bertrand, Claire; Bouché, Jean‐Pierre; Cam, Kaymeuang

doi:10.1046/j.1365-2958.1999.01605.x

Cited by 109 publications

(122 citation statements)

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“…Bacteria were grown on LB medium or M9 minimal salts medium containing 0.4 % glycerol (Miller, 1972;Sambrook & Russell, 2001 et al, 2004). A position-specific weight matrix was generated using RcsB-binding sites described by Wehland & Bernhard (2000), as well as RcsB-binding sequences identified in the promoters of flhDC, rprA, osmC and ftsZ genes in E. coli (Carballes et al, 1999; DavalosGarcia et al, 2001;Francez-Charlot et al, 2003;Majdalani et al, 2002). The sensitivity threshold was set to 0.8-11.3, only RcsB-binding sites within 350 bp of the start of translation were considered, and the search was restricted to intergenic regions.…”

Section: Methodsmentioning

confidence: 99%

“…The Rcs phosphorelay has been implicated in the synthesis of virulence factors in Pcc and other plant-pathogenic bacteria and also in human pathogens (Hinchliffe et al, 2008;Mouslim et al, 2004;Wang et al, 2009Wang et al, , 2007. RcsB activates the biosynthesis of capsular exopolysaccharides, transcription of the cell division gene, ftsZ, transcription of a cell envelope protein, osmC, and transcription of RprA RNA to increase expression of the stationary-phase sigma factor, RpoS, in E. coli (Carballes et al, 1999;Davalos-Garcia et al, 2001;Gervais et al, 1992;Gottesman et al, 1985;Majdalani et al, 2002). Francez-Charlot et al (2003) demonstrated that the Rcs phosphorelay system represses motility through the direct binding of RcsB to the promoter of flhDC in E. coli.…”

Section: Introductionmentioning

confidence: 99%

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A role for the Rcs phosphorelay in regulating expression of plant cell wall degrading enzymes in Pectobacterium carotovorum subsp. carotovorum

et al. 2010

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The Rcs phosphorelay is a signal transduction system that influences the virulence phenotype of several pathogenic bacteria. In the plant pathogen Pectobacterium carotovorum subsp. carotovorum (Pcc) the response regulator of the Rcs phosphorelay, RcsB, represses expression of plant cell wall degrading enzymes (PCWDE) and motility. The focus of this study was to identify genes directly regulated by the binding of RcsB that also regulate expression of PCWDE genes in Pcc. RcsB-binding sites within the regulatory regions of the flhDC operon and the rprA and rsmB genes were identified using DNase I protection assays, while in vivo studies using flhDC : : gusA, rsmB : : gusA and rprA : : gusA gene fusions revealed gene regulation. These experiments demonstrated that the operon flhDC, a flagellar master regulator, was repressed by RcsB, and transcription of rprA was activated by RcsB. Regulation of the rsmB promoter by RcsB is more complicated. Our results show that RcsB represses rsmB expression mainly through modulating flhDC transcription. Neverthless, direct binding of RcsB on the rsmB promoter region is possible in certain conditions. Using an rprA-negative mutant, it was further demonstrated that RprA RNA is not essential for regulating expression of PCWDE under the conditions tested, whereas overexpression of rprA increased protease expression in wild-type cells. Stationary-phase sigma factor, RpoS, is the only known target gene for RprA RNA in Escherichia coli; however, in Pcc the effect of RprA RNA was found to be rpoS-independent. Overall, our results show that the Rcs phosphorelay negatively affects expression of PCWDE by inhibiting expression of flhDC and rsmB. INTRODUCTIONThe phytopathogenicity of Pectobacterium carotovorum subsp. carotovorum (Pcc) is largely due its capacity to synthesize and secrete plant cell wall degrading enzymes (PCWDE), including pectinases, cellulases and protease Marits et al., 1999; Mäe et al., 1995;Pirhonen et al., 1991). Survival of infecting Pcc largely depends on production of PCWDE for the transition from latent infection to disease state. A number of global and specific regulatory genes contribute to expression of PCWDE in Pcc (Burr et al., 2006;Chatterjee et al., 1995;Cui et al., 1995Cui et al., , 1999Cui et al., , 2001Cui et al., , 2005Eriksson et al., 1998;Flego et al., 2000;Harris et al., 1998; Hyytiäinen et al., 2003;Liu et al., 1998Liu et al., , 1999 Sjöblom et al., 2006). The posttranscriptional Rsm system plays a key role in regulating the expression of PCWDE Cui et al., 1995;Liu et al., 1998).The Rsm system consists of two regulators in Pcc: a small protein, RsmA, and RsmB RNA. RsmA is a post-transcriptional global regulator that is thought to bind mRNAs of PCWDE genes and affect their stability, whereas RsmB RNA binds multiple molecules of RsmA, thereby neutralizing its effect (Liu et al., 1998). Recently, the Rsm system was shown to be dependent on expression of a global regulator of flagellar genes, FlhDC. FlhDC activates the expression of PCWDE in Pcc strain 7...

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A role for the Rcs phosphorelay in regulating expression of plant cell wall degrading enzymes in Pectobacterium carotovorum subsp. carotovorum

et al. 2010

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“…In addition to the wza-wca gene cluster, targets regulated by the Rcs system with its cofactor RcsA include the motility master operon fhlDC (Francez-Charlot et al, 2003), rcsA and, in Salmonella, the gene ugd, which is required for the incorporation of 4-aminoarabinose into the lipopolysaccharide (Mouslim & Groisman, 2003). The cell division fts genes (Carballes et al, 1999), the osmoregulated osmC gene (Davalos-Garcia et al, 2001) and rprA, encoding a small RNA which stimulates the translation of the general stressresponse sigma factor RpoS (Majdalani et al, 2002), are also controlled by RcsB, but independently of RcsA. Although RcsB acts preferentially as an activator, it negatively controls flhDC expression (Francez-Charlot et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

Escherichia coli tol and rcs genes participate in the complex network affecting curli synthesis

et al. 2005

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Curli are necessary for the adherence of Escherichia coli to surfaces, and to each other, during biofilm formation, and the csgBA and csgDEFG operons are both required for their synthesis. A recent survey of gene expression in Pseudomonas aeruginosa biofilms has identified tolA as a gene activated in biofilms. The tol genes play a fundamental role in maintaining the outer-membrane integrity of Gram-negative bacteria. RcsC, the sensor of the RcsBCD phosphorelay, is involved, together with RcsA, in colanic acid capsule synthesis, and also modulates the expression of tolQRA and csgDEFG. In addition, the RcsBCD phosphorelay is activated in tol mutants or when Tol proteins are overexpressed. These results led the authors to investigate the role of the tol genes in biofilm formation in laboratory and clinical isolates of E. coli. It was shown that the adherence of cells was lowered in the tol mutants. This could be the result of a drastic decrease in the expression of the csgBA operon, even though the expression of csgDEFG was slightly increased under such conditions. It was also shown that the Rcs system negatively controls the expression of the two csg operons in an RcsA-dependent manner. In the tol mutants, activation of csgDEFG occurred via OmpR and was dominant upon repression by RcsB and RcsA, while these two regulatory proteins repressed csgBA through a dominant effect on the activator protein CsgD, thus affecting curli synthesis. The results demonstrate that the Rcs system, previously known to control the synthesis of the capsule and the flagella, is an additional component involved in the regulation of curli. Furthermore, it is shown that the defect in cell motility observed in the tol mutants depends on RcsB and RcsA. INTRODUCTIONThe ability of bacteria to recognize and adhere to a specific surface is a fundamental aspect of microbial ecology and pathogenesis. Bacterial adhesins and fimbriae confer specific recognition and adhesion to diverse target molecules, such as mammalian host tissue components or inorganic materials. Curli are highly adhesive proteinaceous fibres involved in this process that are produced by Escherichia coli (Vidal et al., 1998) and Salmonella (Collinson et al., 1991). The genes necessary for curli formation are clustered in the csgBA and csgDEFG operons. CsgA encodes the curlin subunit, CsgB is thought to nucleate CsgA curlin fibres (Bian & Normark, 1997), CsgD is a transcriptional activator of the csgBA operon, and CsgE, CsgF and CsgG are three putative curli assembly factors. The lipoprotein CsgG localizes to the inner leaflet of the outer membrane and may serve as a curli assembly platform (Loferer et al., 1997); CsgE and CsgF are thought to be chaperone-like proteins (Chapman et al., 2002). The csg genes appear to be expressed in environmental strains, clinical isolates and some laboratory strains of E. coli.Regulation of curli synthesis is carried out through a complex network of interactions between the transcription factors and the csg regulatory region. Nine regulators have ...

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“…The plasmid pHR758 was constructed by replacing the ampicillin resistance gene of pFZY1 (Koop et al, 1987) with the kanamycin resistance gene of pKC7 (Rao and Rogers, 1979). The 0.5 kb HincII fragment containing the promoter for the cps operon (P cps ) (Stout, 1996;Wehland and Bernhard, 2000) and the 1 kb BamHI-Bgl II fragment containing the promoter for ftsA and ftsZ (P ftsAZ ) (Carballès et al, 1999) were cloned into pHR758 to construct pHR770 and pHR771, respectively.…”

Section: Methodsmentioning

confidence: 99%

“…They are the last two genes but one in the 16-gene cluster of cell division/cell envelope biosynthesis genes, which has a complex transcriptional organization with multiple promoters (Joseleau-Petit et al, 1999). Among them, a promoter located just upstream of ftsA, P ftsAZ , has been shown to be positively regulated by RcsB, independently of RcsA (Carballès et al, 1999;Gervais and Drapeau, 1992). We initially suspected that ftsAZ hyperexpression due to the Rcs activation might be responsible for the growth defect of the pgsA null strain at 42°C.…”

Section: The Thermosensitive Defect Of the Pgsa Null Mutant At 42°c Dmentioning

confidence: 99%

RcsA-dependent and -independent growth defects caused by the activated Rcs phosphorelay system in the Escherichia coli pgsA null mutant

Nagahama

Sakamoto

Matsumoto

et al. 2006

J. Gen. Appl. Microbiol.

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Regulation of Escherichia coli cell division genes ftsA and ftsZ by the two‐component system rcsC–rcsB

Cited by 109 publications

References 36 publications

A role for the Rcs phosphorelay in regulating expression of plant cell wall degrading enzymes in Pectobacterium carotovorum subsp. carotovorum

A role for the Rcs phosphorelay in regulating expression of plant cell wall degrading enzymes in Pectobacterium carotovorum subsp. carotovorum

Escherichia coli tol and rcs genes participate in the complex network affecting curli synthesis

RcsA-dependent and -independent growth defects caused by the activated Rcs phosphorelay system in the Escherichia coli pgsA null mutant

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