A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia

McCarthy, Yvonne; Yang, Liang; Twomey, Kate B.; Saß, Andrea; Tolker‐Nielsen, Tim; Mahenthiralingam, Eshwar; Dow, J. Maxwell; Ryan, Robert P.

doi:10.1111/j.1365-2958.2010.07285.x

Cited by 63 publications

(99 citation statements)

References 46 publications

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“…For these experiments, bacteria were grown in peptone-yeast extract-glycerol medium (NYGB) to an optical density (OD) at 600 nm of 0.8 as described previously (3). RNA was extracted, converted to cDNA, and analyzed on a microarray as described elsewhere (6). The findings revealed a broad regulatory role of Ax21 with effects on transcription of genes encoding proteins involved in transcriptional regulation (including the sigma factor RpoN), antibiotic resistance, and pilus assembly (Table 1; see also Table S1 in the supplemental material).…”

Section: R E T Rmentioning

confidence: 99%

The Ax21 Protein Is a Cell-Cell Signal That Regulates Virulence in the Nosocomial Pathogen Stenotrophomonas maltophilia

McCarthy

Ryan

2011

J Bacteriol

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Stenotrophomonas maltophilia encodes proteins related to the Rax proteins of Xanthomonas oryzae, which are required for the synthesis and secretion of the Ax21 protein. Here we show that Ax21 acts as a cell-cell signal to regulate a diverse range of functions, including virulence, in this nosocomial pathogen.Ax21 is a sulfated protein secreted by Xanthomonas oryzae pv. oryzae that was identified as a trigger of XA21-dependent innate immunity in rice (5). Sulfation and secretion of Ax21 require products of the rax genes (7). The sulfation of Ax21 requires RaxST, a putative tyrosine sulfotransferase, whereas the RaxABC type I secretion system is responsible for secretion of the sulfated protein.The RaxHR two-component system acts to regulate expression of the raxSTAB operon, raxHR, and other rax genes. Mutations in rax genes cause reduced virulence in rice. Interestingly, the expression of these rax genes occurs in a cell density-dependent fashion and requires Ax21. These observations have led to the prediction that Ax21 acts as a diffusible signal that is recognized by RaxHR to control gene expression and virulence in X. oryzae pv. oryzae as a response to bacterial cell density (4). Ax21 is widely conserved in Xanthomonas and the related genera Xylella and Stenotrophomonas, including Stenotrophomonas maltophilia (1, 4, 10), some strains of which are nosocomial human pathogens. A number of laboratories have started to address the molecular bases of antibiotic resistance and factors that contribute to virulence in these hospital-acquired infections (9). Here we have examined the potential role of Ax21 as a cell-cell signal in S. maltophilia.The predicted proteome of S. maltophilia K279a, a clinicalisolate (2), contains proteins that are homologous to Ax21 and a number of Rax proteins of X. oryzae pv. oryzae strain PXO99A. Homologs with the indicated BLASTP

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Section: R E T Rmentioning

confidence: 99%

The Ax21 Protein Is a Cell-Cell Signal That Regulates Virulence in the Nosocomial Pathogen Stenotrophomonas maltophilia

McCarthy

Ryan

2011

J Bacteriol

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“…It is well known that the DSF-QS system regulates certain virulence traits in many bacteria (1,3,9,12,(26)(27)(28)(29). To determine the possible implication of each RpfF variant for virulence regulation, we generated an rpfF deletion mutant for a strain representative of each variant group, i.e., E77 for the RpfF-1 variant group and M30 for the RpfF-2 group.…”

Section: Discussionmentioning

confidence: 99%

“…Thus, DSF molecules have been shown to positively regulate biofilm formation in X. oryzae pv. oryzae (31), B. cenocepacia (9,28), and X. fastidiosa (4,26). On the contrary, in X. campestris pv.…”

Section: Discussionmentioning

confidence: 99%

Two Different rpf Clusters Distributed among a Population of Stenotrophomonas maltophilia Clinical Strains Display Differential Diffusible Signal Factor Production and Virulence Regulation

et al. 2014

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The quorum-sensing (QS) system present in the emerging nosocomial pathogen Stenotrophomonas maltophilia is based on the signaling molecule diffusible signal factor (DSF). Production and detection of DSF are governed by the rpf cluster, which encodes the synthase RpfF and the sensor RpfC, among other components. Despite a well-studied system, little is known about its implication in virulence regulation in S. maltophilia. Here, we have analyzed the rpfF gene from 82 S. maltophilia clinical isolates. Although rpfF was found to be present in all of the strains, it showed substantial variation, with two populations (rpfF-1 and rpfF-2) clearly distinguishable by the N-terminal region of the protein. Analysis of rpfC in seven complete genome sequences revealed a corresponding variability in the N-terminal transmembrane domain of its product, suggesting that each RpfF variant has an associated RpfC variant. We show that only RpfC-RpfF-1 variant strains display detectable DSF production. Heterologous rpfF complementation of ⌬rpfF mutants of a representative strain of each variant suggests that RpfF-2 is, however, functional and that the observed DSF-deficient phenotype of RpfC-RpfF-2 variant strains is due to permanent repression of RpfF-2 by RpfC-2. This is corroborated by the ⌬rpfC mutant of the RpfC-RpfF-2 representative strain. In line with this observations, deletion of rpfF from the RpfC-RpfF-1 strain leads to an increase in biofilm formation, a decrease in swarming motility, and relative attenuation in the Caenorhabditis elegans and zebrafish infection models, whereas deletion of the same gene from the representative RpfC-RpfF-2 strain has no significant effect on these virulence-related phenotypes. Q uorum sensing (QS) is a bacterial cell-cell communication process that allows bacteria to synchronize particular behaviors on a population-wide scale. Within current knowledge, QS in Stenotrophomonas maltophilia depends on the diffusible signal factor QS (DSF-QS) system, which is based mainly on the fatty acid DSF (cis-11-methyl-2-dodecenoic acid) (1, 2). DSF synthesis is fully dependent on RpfF, an enoyl coenzyme A hydratase encoded by the rpf (regulation of pathogenicity factors) cluster, a set of genes that includes all of the components necessary for the synthesis and detection of DSF molecules. In addition to RpfF, rpf encodes the aconitase RpfA, the fatty acid ligase RpfB, the two-component sensor-effector hybrid system RpfC, and the cytoplasmic regulator element RpfG (1, 2). The DSF-QS system was first described in the phytopathogen Xanthomonas campestris pv. campestris, where it plays an important role in virulence regulation (3). Since then, this system has been described in several members of the order Xanthomonadales, including the genera Xanthomonas, Xylella, and Stenotrophomonas, as well as in members of the order Burkholderiales (1, 3-5). The specific functions regulated by the DSF-QS system are dependent on the species, but it has been suggested that it controls several virulence-related phenotypes (6...

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“…McCarthy et al (80) provided evidence that four-day-old B. cenocepacia wild type biofilms grown in flow chambers contained substantial amounts of extracellular DNA as a part of the biofilm matrix. In contrast, biofilms formed by a quorum-sensing-defective B. cenocepacia mutant never passed the initial microcolony stage, and the thin biofilms showed little staining by propidium iodide, indicating that extracellular DNA was not generated in large quantities (80).…”

Section: Quorum-sensing Can Play Important Roles In Biofilm Formationmentioning

confidence: 99%

Biofilm Development

2015

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During the past decade we have gained much knowledge about the molecular mechanisms that are involved in initiation and termination of biofilm formation. In many bacteria, these processes appear to occur in response to specific environmental cues and result in, respectively, induction or termination of biofilm matrix production via the second messenger molecule c-di-GMP. In between initiation and termination of biofilm formation we have defined specific biofilm stages, but the currently available evidence suggests that these transitions are mainly governed by adaptive responses, and not by specific genetic programs. It appears that biofilm formation can occur through multiple pathways and that the spatial structure of the biofilms is species dependent as well as dependent on environmental conditions. Bacterial subpopulations, e.g., motile and nonmotile subpopulations, can develop and interact during biofilm formation, and these interactions can affect the structure of the biofilm. The available evidence suggests that biofilm formation is programmed in the sense that regulated synthesis of extracellular matrix components is involved. Furthermore, our current knowledge suggests that biofilm formation mainly is governed by adaptive responses of individual bacteria, although group-level activities are also involved.

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A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia

Cited by 63 publications

References 46 publications

The Ax21 Protein Is a Cell-Cell Signal That Regulates Virulence in the Nosocomial Pathogen Stenotrophomonas maltophilia

The Ax21 Protein Is a Cell-Cell Signal That Regulates Virulence in the Nosocomial Pathogen Stenotrophomonas maltophilia

Two Different rpf Clusters Distributed among a Population of Stenotrophomonas maltophilia Clinical Strains Display Differential Diffusible Signal Factor Production and Virulence Regulation

Biofilm Development

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