Diguanylate cyclase <scp>NicD</scp>‐based signalling mechanism of nutrient‐induced dispersion by <scp><i>P</i></scp><i>seudomonas aeruginosa</i>

Roy, Ankita; Sauer, Karin

doi:10.1111/mmi.12802

Cited by 84 publications

(83 citation statements)

References 77 publications

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“…It has been shown that the expression of bdlA and the siaABCD operon was induced in a wspF mutant (high c-di-GMP) by a factor of 2 or 2 to 5, respectively (7,8). Expression of bdlA was also shown to be low in planktonic cells compared to biofilm growth conditions (49). Two putative FleQ boxes were also found in the promoter regions of different lapA-like genes.…”

Section: Discussionmentioning

confidence: 85%

FleQ DNA Binding Consensus Sequence Revealed by Studies of FleQ-Dependent Regulation of Biofilm Gene Expression in Pseudomonas aeruginosa

2016

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The transcription factor FleQ from Pseudomonas aeruginosa derepresses expression of genes involved in biofilm formation when intracellular levels of the second messenger cyclic diguanosine monophosphate (c-di-GMP) are high. FleQ also activates transcription of flagellar genes, and the expression of these genes is highest at low intracellular c-di-GMP. FleQ thus plays a central role in mediating the transition between planktonic and biofilm lifestyles of P. aeruginosa. Previous work showed that FleQ controls expression of the pel operon for Pel exopolysaccharide biosynthesis by converting from a repressor to an activator upon binding c-di-GMP. To explore the activity of FleQ further, we carried out DNase I footprinting at three additional biofilm gene promoters, those of psl, cdrAB, and PA2440. The expression of cdrAB, encoding a cell surface adhesin, was sufficiently responsive to FleQ to allow us to carry out in vivo promoter assays. The results showed that, similarly to our observations with the pel operon, FleQ switches from a repressor to an activator of cdrAB gene expression in response to c-di-GMP. From the footprinting data, we identified a FleQ DNA binding consensus sequence. A search for this conserved sequence in bacterial genome sequences led to the identification of FleQ binding sites in the promoters of the siaABCD operon, important for cell aggregation, and the bdlA gene, important for biofilm dispersal, in P. aeruginosa. We also identified FleQ binding sites upstream of lapA-like adhesin genes in other Pseudomonas species. IMPORTANCEThe transcription factor FleQ is widely distributed in Pseudomonas species. In all species examined, it is a master regulator of flagellar gene expression. It also regulates diverse genes involved in biofilm formation in P. aeruginosa when intracellular levels of the second messenger c-di-GMP are high. Unlike flagellar genes, biofilm-associated genes are not always easy to recognize in genome sequences. Here, we identified a consensus DNA binding sequence for FleQ. This allowed us to survey Pseudomonas strains and find new genes that are likely regulated by FleQ and possibly involved in biofilm formation. Cyclic diguanosine monophosphate (c-di-GMP) is an intracellular second messenger that is produced by bacteria and has diverse effects on bacterial physiology. c-di-GMP binds to riboswitches and effector proteins to modulate transcription, translation, and protein activities (1, 2). In the opportunistic pathogen Pseudomonas aeruginosa, the transcription factor FleQ binds c-di-GMP to derepress expression of genes for biofilm components (3, 4). Biofilms are surface-attached communities of bacteria embedded in a matrix made of exopolysaccharides, proteins, and DNA. Biofilm infections are particularly difficult to treat because bacteria are protected by the biofilm matrix, making them resistant to antimicrobial treatment compared to planktonic cells (5). Genes controlled by FleQ include pel genes, coding for Pel exopolysaccharide; psl genes, coding for Psl exopolys...

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Section: Discussionmentioning

confidence: 85%

FleQ DNA Binding Consensus Sequence Revealed by Studies of FleQ-Dependent Regulation of Biofilm Gene Expression in Pseudomonas aeruginosa

2016

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“…This is supported by the findings that dispersed cells differ significantly from biofilm cells with respect to gene expression, protein production, and posttranslational modification [2,9,44,47-49]. Compared to biofilm cells, dispersed cells are furthermore characterized by decreased levels of the intracellular signaling molecule c-di-GMP and increased production of matrix degrading enzymes [27,38-40,50,51]. While dispersion has often been described to coincide with increased motility of the escaping bacteria, several studies demonstrated that motility is not required for dispersion [42,44,52,53], suggesting that motility may be an indicator of dispersed cells returning to the planktonic mode of growth, but is not part of the mechanism enabling dispersion.…”

Section: All Biofilm Escapes Are Not Created Equalmentioning

confidence: 84%

Escaping the biofilm in more than one way: desorption, detachment or dispersion

Petrova

Sauer

2016

Current Opinion in Microbiology

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202

163

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Biofilm bacteria have developed escape strategies to avoid stresses associated with biofilm growth, respond to changing environmental conditions, and disseminate to new locations. An ever-expanding body of research suggests that cellular release from biofilms is distinct from a simple reversal of attachment and reversion to a planktonic mode of growth, with biofilm dispersion involving sensing of specific cues, regulatory signal transduction, and consequent physiological alterations. However, dispersion is only one of many ways to escape the biofilm mode of growth. The present review is aimed at distinguishing this active and regulated process of dispersion from the passive processes of desorption and detachment by highlighting the regulatory processes and distinct phenotypes specific to dispersed cells.

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“…2) (82, 83). Upon signal (i.e., glutamate) sensing, the DGC NicD, a seven-transmembrane receptor, becomes dephosphorylated, leading to enhanced DGC activity and resulting in a transient increase in c-di-GMP levels (84). NicD contributes to BdlA activation in two ways, by elevating c-di-GMP levels and via phosphorylation.…”

Section: Dispersal Of P Aeruginosa Biofilms Induced By Exogenous No mentioning

confidence: 99%

Origin and Impact of Nitric Oxide in Pseudomonas aeruginosa Biofilms

Cutruzzolà

Frankenberg‐Dinkel

2016

J Bacteriol

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bThe formation of the organized bacterial community called biofilm is a crucial event in bacterial physiology. Given that biofilms are often refractory to antibiotics and disinfectants to which planktonic bacteria are susceptible, their formation is also an industrially and medically relevant issue. Pseudomonas aeruginosa, a well-known human pathogen causing acute and chronic infections, is considered a model organism to study biofilms. A large number of environmental cues control biofilm dynamics in bacterial cells. In particular, the dispersal of individual cells from the biofilm requires metabolic and morphological reprogramming in which the second messenger bis-(3=-5=)-cyclic dimeric GMP (c-di-GMP) plays a central role. The diatomic gas nitric oxide (NO), a well-known signaling molecule in both prokaryotes and eukaryotes, is able to induce the dispersal of P. aeruginosa and other bacterial biofilms by lowering c-di-GMP levels. In this review, we summarize the current knowledge on the molecular mechanisms connecting NO sensing to the activation of c-di-GMP-specific phosphodiesterases in P. aeruginosa, ultimately leading to c-di-GMP decrease and biofilm dispersal. PSEUDOMONAS AERUGINOSA: A MODEL SYSTEM FOR BIOFILM RESEARCH

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Diguanylate cyclase NicD‐based signalling mechanism of nutrient‐induced dispersion by Pseudomonas aeruginosa

Cited by 84 publications

References 77 publications

FleQ DNA Binding Consensus Sequence Revealed by Studies of FleQ-Dependent Regulation of Biofilm Gene Expression in Pseudomonas aeruginosa

FleQ DNA Binding Consensus Sequence Revealed by Studies of FleQ-Dependent Regulation of Biofilm Gene Expression in Pseudomonas aeruginosa

Escaping the biofilm in more than one way: desorption, detachment or dispersion

Origin and Impact of Nitric Oxide in Pseudomonas aeruginosa Biofilms

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