TheyddV-dosoperon controls biofilm formation through the regulation of genes encoding curli fibers' subunits in aerobically growingEscherichia coli

Tagliabue, Letizia; Maciąg, Anna; Antoniani, Davide; Landini, Paolo

doi:10.1111/j.1574-695x.2010.00702.x

Cited by 27 publications

(22 citation statements)

References 48 publications

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“…5). Mutations in either the pgaA or the yddV gene resulted in a 2.5-fold reduction in surface adhesion in the MG1655 background, in agreement with previous observations (Wang et al, 2004;Tagliabue et al, 2010).…”

Section: Regulation Of Pgaabcd Expression By Dgcssupporting

confidence: 91%

“…Recently, we have shown that YddV can affect the expression of curli-encoding genes (Tagliabue et al, 2010), which, however, are extremely sensitive to perturbations in intracellular c-di-GMP concentrations (Sommerfeldt et al, 2009). In this work, we show that overexpression of YddV, but not of other DGCs, stimulates production of poly-Nacetylglucosamine (PNAG), an EPS able to promote biofilm formation, by triggering expression of pgaABCD, the PNAG biosynthetic operon.…”

Section: Introductionmentioning

confidence: 79%

“…For instance, yddV, arguably the most highly expressed DGC-encoding gene in E. coli (Sommerfeldt et al, 2009), can activate transcription of the csgBA operon, encoding curli subunits (Tagliabue et al, 2010); however, YddV overexpression can stimulate biofilm formation independently of curli production (Méndez-Ortiz et al, 2006), thus suggesting that yddV can induce biofilm formation by acting on additional, not yet identified targets. In order to study the specific effects of YddV on the production of extracellular structures, we cloned the yddV gene into the pGEM-T Easy plasmid, which allows constitutive expression of cloned genes in the absence of IPTG induction.…”

Section: Overexpression Of Dgcsmentioning

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: Regulation Of Pgaabcd Expression By Dgcssupporting

confidence: 91%

Section: Introductionmentioning

confidence: 79%

Section: Overexpression Of Dgcsmentioning

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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“…A salient example is that of HIF-1, which affects mammalian development, metabolism, and tumor formation in response to limitation for molecular oxygen and other redox cues (41,42). Although PAS-domain-dependent, redox-sensitive regulation of exopolysaccharide production and biofilm development have been reported for selected nonpathogenic bacteria (43)(44)(45), the observations presented herein extend this model to the morphogenetic control of the pathogen P. aeruginosa, and specifically to the effects of endogenously produced electron shuttles (Fig. 5E).…”

Section: Colony Matrix Distribution Phenotypes Suggest That Phenazinementioning

confidence: 99%

Electron-shuttling antibiotics structure bacterial communities by modulating cellular levels of c-di-GMP

Okegbe

Fields

Cole

et al. 2017

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

101

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Diverse organisms secrete redox-active antibiotics, which can be used as extracellular electron shuttles by resistant microbes. Shuttlemediated metabolism can support survival when substrates are available not locally but rather at a distance. Such conditions arise in multicellular communities, where the formation of chemical gradients leads to resource limitation for cells at depth. In the pathogenic bacterium Pseudomonas aeruginosa PA14, antibiotics called phenazines act as oxidants to balance the intracellular redox state of cells in anoxic biofilm subzones. PA14 colony biofilms show a profound morphogenic response to phenazines resulting from electron acceptor-dependent inhibition of ECM production. This effect is reminiscent of the developmental responses of some eukaryotic systems to redox control, but for bacterial systems its mechanistic basis has not been well defined. Here, we identify the regulatory protein RmcA and show that it links redox conditions to PA14 colony morphogenesis by modulating levels of bis-(3′,5′)-cyclic-dimeric-guanosine (c-di-GMP), a second messenger that stimulates matrix production, in response to phenazine availability. RmcA contains four Per-Arnt-Sim (PAS) domains and domains with the potential to catalyze the synthesis and degradation of c-di-GMP. Our results suggest that phenazine production modulates RmcA activity such that the protein degrades c-di-GMP and thereby inhibits matrix production during oxidizing conditions. RmcA thus forms a mechanistic link between cellular redox sensing and community morphogenesis analogous to the functions performed by PAS-domain-containing regulatory proteins found in complex eukaryotes.W hen microbial cells cannot import or are physically separated from metabolic electron donors or acceptors, diffusible compounds can act as electron carriers and support survival on these substrates (1, 2). These conditions arise in the presence of poised-potential electrodes or insoluble minerals, such as iron oxides (3-5), and in multicellular communities (biofilms) where the formation of chemical gradients leads to oxidant limitation for cells at depth (6-9). Diverse microbes secrete redoxactive compounds with the capacity to function as electron shuttles (10-12). In the pathogenic bacterium Pseudomonas aeruginosa PA14, electron-shuttling antibiotics called phenazines support survival on poised-potential electrodes and balance the intracellular redox state of cells in anoxic biofilm subzones (1, 9).Similar to those formed by many species of microbes, colonies of PA14 develop intricate wrinkle structures on agar-solidified growth media (13). Phenazines profoundly alter PA14 colony morphogenesis, inhibiting the onset of wrinkle formation and changing the organization of wrinkles (12) (Fig. 1A). Modeling of resource availability within colonies suggests that the earlier increase in the colony surface area-to-volume ratio in phenazine-null (Δphz) mutants maximizes access to oxygen for cells that would otherwise become limited for oxidant (14). Measurements of...

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“…Regulation of curli-encoding genes is extraordinarily complex and responds to a combination of environmental cues, such as low growth temperature (¡30 u C), low osmolarity, slow growth and oxygen availability (Römling et al, 1998a;Gerstel & Römling, 2001Tagliabue et al, 2010a). The signal molecules cAMP (Zheng et al, 2004) and c-di-GMP (Kader et al, 2006;Weber et al, 2006), as well as intracellular concentration of pyrimidine nucleotides (Garavaglia et al, 2012), also have a strong impact on curli gene expression.…”

Section: Introductionmentioning

confidence: 99%

Sulfate assimilation pathway intermediate phosphoadenosine 5′-phosphosulfate acts as a signal molecule affecting production of curli fibres in Escherichia coli

et al. 2014

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The enterobacterium Escherichia coli can utilize a variety of molecules as sulfur sources, including cysteine, sulfate, thiosulfate and organosulfonates. An intermediate of the sulfate assimilation pathway, adenosine 59-phosphosulfate (APS), also acts as a signal molecule regulating the utilization of different sulfur sources. In this work, we show that inactivation of the cysH gene, leading to accumulation of phosphoadenosine 59-phosphosulfate (PAPS), also an intermediate of the sulfate assimilation pathway, results in increased surface adhesion and cell aggregation by activating the expression of the curli-encoding csgBAC operon. In contrast, curli production was unaffected by the inactivation of any other gene belonging to the sulfate assimilation pathway. Overexpression of the cysH gene downregulated csgBAC transcription, further suggesting a link between intracellular PAPS levels and curli gene expression. In addition to curli components, the Flu, OmpX and Slp proteins were also found in increased amounts in the outer membrane compartment of the cysH mutant; deletion of the corresponding genes suggested that these proteins also contribute to surface adhesion and cell surface properties in this strain. Our results indicate that, similar to APS, PAPS also acts as a signal molecule, albeit with a distinct mechanism and role: whilst APS regulates organosulfonate utilization, PAPS would couple availability of sulfur sources to remodulation of the cell surface, as part of a more global effect on cell physiology.

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TheyddV-dosoperon controls biofilm formation through the regulation of genes encoding curli fibers' subunits in aerobically growingEscherichia coli

Cited by 27 publications

References 48 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

Electron-shuttling antibiotics structure bacterial communities by modulating cellular levels of c-di-GMP

Sulfate assimilation pathway intermediate phosphoadenosine 5′-phosphosulfate acts as a signal molecule affecting production of curli fibres in Escherichia coli

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