Inverse regulatory coordination of motility and curli-mediated adhesion in <i>Escherichia coli</i>

Pesavento, Christina; Becker, Gisela; Sommerfeldt, Nicole; Possling, Alexandra; Tschowri, Natalia; Mehlis, Anika; Hengge, Regine

doi:10.1101/gad.475808

Cited by 322 publications

(491 citation statements)

References 54 publications

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“…c-di-GMP intracellular concentrations did not strictly correlate with DGC overproduction levels, as judged by SDS-PAGE analysis of cell extracts (data not shown). The expression of each DGC led to a reduction in bacterial mobility (Supplementary Table S2), in agreement with earlier observations (Méndez-Ortiz et al, 2006;Jonas et al, 2008;Pesavento et al, 2008).…”

Section: Overexpression Of Dgcssupporting

confidence: 81%

“…In Enterobacteria, biosynthesis of the c-di-GMP signal molecule by DGCs stimulates the transition from planktonic to biofilm cells, repressing flagellar synthesis and cell motility, while promoting production of adhesion factors (Méndez-Ortiz et al, 2006;Pesavento et al, 2008). In this report, we have shown that overexpression of YddV, a DGC protein, promotes production of the EPS PNAG (Figs 2 and 3) by activating the expression of pgaABCD, the PNAG biosynthetic operon (Fig.…”

Section: Discussionmentioning

confidence: 58%

“…Primers used for gene inactivation and for confirmation of target gene disruption by PCR are listed in Supplementary Table S1. Bacterial cell motility was evaluated as described by Pesavento et al (2008). Determination of intracellular c-di-GMP concentration was performed as previously described .…”

Section: Methodsmentioning

confidence: 99%

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The diguanylate cyclase YddV controls production of the exopolysaccharide poly-N-acetylglucosamine (PNAG) through regulation of the PNAG biosynthetic pgaABCD operon

et al. 2010

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In Gram-negative bacteria, production of adhesion factors and extracellular polysaccharides (EPS) is promoted by the activity of diguanylate cyclases (DGCs), a class of enzymes able to catalyse the synthesis of the signal molecule bis-(39,59)-cyclic di-guanylic acid (c-di-GMP). In this report we show that in Escherichia coli, overexpression of the YddV protein, but not of other DGCs such as AdrA and YcdT, induces the production of the EPS poly-N-acetylglucosamine (PNAG) by stimulating expression of pgaABCD, the PNAG-biosynthetic operon. Stimulation of PNAG production and activation of pgaABCD expression by the YddV protein are abolished by inactivation of its GGDEF motif, responsible for DGC activity. Consistent with the effects of YddV overexpression, inactivation of the yddV gene negatively affects pgaABCD transcription and PNAG-mediated biofilm formation. pgaABCD regulation by the yddV gene also takes place in a mutant carrying a partial deletion of the csrA gene, which encodes the main regulator of pgaABCD expression, suggesting that YddV does not regulate pgaABCD through modulation of CsrA activity. Our results demonstrate that PNAG production does not simply respond to intracellular c-di-GMP concentration, but specifically requires the DGC activity of the YddV protein, thus supporting the notion that in E. coli, c-di-GMP biosynthesis by a given DGC protein triggers regulatory events that lead to activation of specific sets of EPS biosynthetic genes or proteins. INTRODUCTIONMost bacteria are able to switch between two different 'lifestyles': single cells (planktonic mode) and biofilm, i.e. a sessile microbial community. Biofilm and planktonic cells differ significantly in their physiology, in their gene expression pattern and even in their morphology. In particular, biofilm cells are characterized by production of adhesion factors and extracellular polysaccharides (EPS), resistance to environmental stresses, and lower sensitivity to antibiotics compared with planktonic cells (Costerton et al., 1995;Anderl et al., 2000;Harrison et al., 2007Harrison et al., , 2009).Transition from planktonic cells to biofilm is regulated by environmental and physiological cues, relayed to the bacterial cell by signal molecules or 'second messengers'. A second messenger, bis-(39,59)-cyclic diguanylic acid, better known as cyclic-di-GMP (c-di-GMP), plays a pivotal role in biofilm formation and maintenance by stimulating production of EPS and adhesion factors (Ross et al., 1991;Simm et al., 2004;Kader et al., 2006;Weber et al., 2006). In addition, c-di-GMP biosynthesis affects important cellular processes, such as morphological differentiation and cell replication in Caulobacter crescentus (Paul et al., 2004), cell motility (Méndez-Ortiz et al., 2006; Jonas et al., 2008) and virulence factor production (Kulasakara et al., 2006;Hammer & Bassler, 2009). In Enterobacteria, c-di-GMP seems to be involved in regulation of adhesion factors, such as curli and cellulose, important for adaptation and survival outside the warm-blooded hos...

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Section: Overexpression Of Dgcssupporting

confidence: 81%

Section: Discussionmentioning

confidence: 58%

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The diguanylate cyclase YddV controls production of the exopolysaccharide poly-N-acetylglucosamine (PNAG) through regulation of the PNAG biosynthetic pgaABCD operon

et al. 2010

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“…For instance in Escherichia coli, CsgD is a key transcriptional regulator for curli production as well as a master regulator of biofilm formation. CsgD was shown to directly repress gene expression of flagella components, and activate the synthesis of extracellular polysaccharides, thereby switching from planktonic growth to the biofilm mode (Zogaj et al, 2001;Pesavento et al, 2008). Moreover, CsgD modulates adrA upregulation, which encodes one of the enzymes for cyclic di-GMP synthesis (Ogasawara et al, 2010).…”

Section: Regulation Of Crenarchaeal Biofilm Formationmentioning

confidence: 99%

Lrs14 transcriptional regulators influence biofilm formation and cell motility of Crenarchaea

et al. 2013

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Like bacteria, archaea predominately exist as biofilms in nature. However, the environmental cues and the molecular mechanisms driving archaeal biofilm development are not characterized. Here we provide data suggesting that the transcriptional regulators belonging to the Lrs14-like protein family constitute a key regulatory factor during Sulfolobus biofilm development. Among the six lrs14-like genes encoded by Sulfolobus acidocaldarius, the deletion of three led to markedly altered biofilm phenotypes. Although Dsaci1223 and Dsaci1242 deletion mutants were impaired in biofilm formation, the Dsaci0446 deletion strain exhibited a highly increased extracellular polymeric substance (EPS) production, leading to a robust biofilm structure. Moreover, although the expression of the adhesive pili (aap) genes was upregulated, the genes of the motility structure, the archaellum (fla), were downregulated rendering the Dsaci0446 strain non-motile. Gel shift assays confirmed that Saci0446 bound to the promoter regions of fla and aap thus controlling the expression of both cell surface structures. In addition, genetic epistasis analysis using Dsaci0446 as background strain identified a gene cluster involved in the EPS biosynthetic pathway of S. acidocaldarius. These results provide insights into both the molecular mechanisms that govern biofilm formation in Crenarchaea and the functionality of the Lrs14-like proteins, an archaea-specific class of transcriptional regulators.

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“…The fliZ gene, which is co-transcribed with fliA, encodes a protein which acts as a positive regulator of motility, and as an inhibitor of the expression of curli fimbriae, which are required for surface-attached growth (Pesavento et al, 2008;Saini et al, 2008). The fliLMNOPQR operon encodes structural components of the flagellum and the flagellin export apparatus (Chilcott and Hughes, 2000).…”

mentioning

confidence: 99%

NsrR targets in the Escherichia coli genome: new insights into DNA sequence requirements for binding and a role for NsrR in the regulation of motility

Partridge

Bodenmiller

Humphrys

et al. 2009

Molecular Microbiology

128

133

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SummaryThe Escherichia coli NsrR protein is a nitric oxidesensitive repressor of transcription. The NsrRbinding site is predicted to comprise two copies of an 11 bp motif arranged as an inverted repeat with 1 bp spacing. By mutagenesis we confirmed that both 11 bp motifs are required for maximal NsrR repression of the ytfE promoter. We used chromatin immunoprecipitation and microarray analysis (ChIPchip) to show that NsrR binds to 62 sites close to the 5Ј ends of genes. Analysis of the ChIP-chip data suggested that a single 11 bp motif (with the consensus sequence AANATGCATTT) can function as an NsrR-binding site in vivo. NsrR binds to sites in the promoter regions of the fliAZY, fliLMNOPQR and mqsR-ygiT transcription units, which encode proteins involved in motility and biofilm development. Reporter fusion assays confirmed that NsrR negatively regulates the fliA and fliL promoters. A mutation in the predicted 11 bp NsrR-binding site in the fliA promoter impaired repression by NsrR and prevented detectable binding in vivo. Assays on softagar confirmed that NsrR is a negative regulator of motility in E. coli K12 and in a uropathogenic strain; surface attachment assays revealed decreased levels of attached growth in the absence of NsrR.

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Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli

Cited by 322 publications

References 54 publications

The diguanylate cyclase YddV controls production of the exopolysaccharide poly-N-acetylglucosamine (PNAG) through regulation of the PNAG biosynthetic pgaABCD operon

The diguanylate cyclase YddV controls production of the exopolysaccharide poly-N-acetylglucosamine (PNAG) through regulation of the PNAG biosynthetic pgaABCD operon

Lrs14 transcriptional regulators influence biofilm formation and cell motility of Crenarchaea

NsrR targets in the Escherichia coli genome: new insights into DNA sequence requirements for binding and a role for NsrR in the regulation of motility

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