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PubMed2001

Mathematical modelling of quorum sensing in bacteria.

The regulation of density-dependent behaviour by means of quorum sensing is widespread in bacteria, the relevant phenomena including bioluminescence and population expansion by swarming, as well as virulence. The process of quorum sensing is regulated by the production and monitoring of certain molecules (referred to as QSMs); on reaching an apparent threshold concentration of QSMs (reflecting high bacterial density) the bacterial colony in concert 'switches on' the density-dependent trait. In this paper a mathematical model which describes bacterial population growth and quorum sensing in a well mixed system is proposed and studied. We view the population of bacteria as consisting of down-regulated and up-regulated sub-populations, with QSMs being produced at a much faster rate by the up-regulated cells. Using curve fitting techniques for parameter estimation, solutions of the resulting system of ordinary differential equations are shown to agree well with experimental data. Asymptotic analysis in a biologically relevant limit is used to investigate the timescales for up-regulation of an exponentially growing population of bacteria, revealing the existence of bifurcation between limited and near-total up-regulation. For a fixed population of cells steady-state analysis reveals that in general one physical steady-state solution exists and is linearly stable; we believe this solution to be a global attractor. A bifurcation between limited and near-total up-regulation is also discussed in the steady-state limit.

Bacteria↗

PubMed2005

Quorum sensing: the power of cooperation in the world of Pseudomonas.

Work over the past few years has provided evidence that quorum sensing is a generic regulatory mechanism that allows bacteria to launch a unified, coordinated response in a population density-dependent manner to accomplish tasks which would be difficult, if not impossible, to achieve for a single bacterial cell. Quorum sensing systems are widespread among pseudomonads and the one of the human opportunistic pathogen Pseudomonas aeruginosa belongs to the most extensively studied cell-to-cell communication systems. In this organism, quorum sensing is highly complex and is made up of two interlinked N-acyl homoserine lactone (AHL)-dependent regulatory circuits, which are further modulated by a non-AHL-related signal molecule and numerous regulators acting both at the transcriptional and post-transcriptional level. This genetic complexity may be one of the key elements responsible for the tremendous environmental versatility of P. aeruginosa. Work of the past few years showed that quorum sensing is essential for the expression of a battery of virulence factors as well as for biofilm formation in P. aeruginosa and thus represents an attractive target for the design of novel drugs for the treatment of P. aeruginosa infections. Furthermore, the cell-to-cell communication ability was also demonstrated in a number of additional pseudomonads.

4-Butyrolactone↗

PubMed2006

Quorum sensing in Erwinia species.

The term quorum sensing (QS) refers to the ability of bacteria to regulate gene expression according to the accumulation of signalling molecules that are made by every cell in the population. The erwiniae group of bacteria are often phytopathogens and the expression of a number of their important virulence determinants and secondary metabolites is under QS control. The erwiniae utilise two types of QS signalling molecules: N-acyl homoserine lactones and AI-2-type signalling molecules. Here, we review the regulatory networks involving QS in the soft rot erwiniae.

4-Butyrolactone↗

PubMed2003

Quorum sensing in nitrogen-fixing rhizobia.

Members of the rhizobia are distinguished for their ability to establish a nitrogen-fixing symbiosis with leguminous plants. While many details of this relationship remain a mystery, much effort has gone into elucidating the mechanisms governing bacterium-host recognition and the events leading to symbiosis. Several signal molecules, including plant-produced flavonoids and bacterially produced nodulation factors and exopolysaccharides, are known to function in the molecular conversation between the host and the symbiont. Work by several laboratories has shown that an additional mode of regulation, quorum sensing, intercedes in the signal exchange process and perhaps plays a major role in preparing and coordinating the nitrogen-fixing rhizobia during the establishment of the symbiosis. Rhizobium leguminosarum, for example, carries a multitiered quorum-sensing system that represents one of the most complex regulatory networks identified for this form of gene regulation. This review focuses on the recent stream of information regarding quorum sensing in the nitrogen-fixing rhizobia. Seminal work on the quorum-sensing systems of R. leguminosarum bv. viciae, R. etli, Rhizobium sp. strain NGR234, Sinorhizobium meliloti, and Bradyrhizobium japonicum is presented and discussed. The latest work shows that quorum sensing can be linked to various symbiotic phenomena including nodulation efficiency, symbiosome development, exopolysaccharide production, and nitrogen fixation, all of which are important for the establishment of a successful symbiosis. Many questions remain to be answered, but the knowledge obtained so far provides a firm foundation for future studies on the role of quorum-sensing mediated gene regulation in host-bacterium interactions.

Nitrogen Fixation↗

PubMed2006

Analysis of the hierarchy of quorum-sensing regulation in Pseudomonas aeruginosa.

Quorum-sensing in Pseudomonas aeruginosa is known to regulate several aspects of pathogenesis, including virulence factor production, biofilm development, and antimicrobial resistance. Recent high-throughput analysis has revealed the existence of several layers of regulation within the QS-circuit. To address this complexity, mutations in genes encoding known or putative transcriptional regulators that were also identified as being regulated by the las and/or rhl QS systems were screened for their contribution in mediating several phenotypes, for example motility, secreted virulence products, and pathogenic capacity in a lettuce leaf model. These studies have further elucidated the potential contribution to virulence of these genes within the QS regulon.

Bacterial Physiological Phenomena↗

PubMed1997

Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa.

The production of several virulence factors by Pseudomonas aeruginosa is controlled according to cell density through two quorum-sensing systems, las and rhl. The las system is comprised of the transcriptional activator protein LasR and of LasI, which directs the synthesis of the autoinducer PAI-1. Similarly, the rhl system consists of the transcriptional activator protein RhlR and of RhlI, which directs synthesis of the autoinducer PAI-2 (formerly referred to as factor 2). To study the interrelation between the two P. aeruginosa quorum-sensing systems, we fused a lacZ reporter gene to lasR, rhlR, and rhlA and monitored expression of these three genes under various conditions. Our data indicate that lasR and rhlR are expressed in a growth-dependent manner, with activation of each gene occurring during the last half of log-phase growth. We also show that the las quorum-sensing system controls the rhl quorum-sensing system in two ways. First, we found that LasR and PAI-1 activated rhlR transcription. Second, we showed that PAI-1 blocked PAI-2 from binding to RhlR, thereby inhibiting the expression of rhlA. Our data thus indicate that the las system exerts two levels of control on RhlR, transcriptional and posttranslational.

4-Butyrolactone↗

PubMedDate not supplied

Modeling the quorum sensing regulatory network of human-pathogenic Pseudomonas aeruginosa.

The biochemical network underlying quorum sensing in human-pathogenic Pseudomonas aeruginosa is one of the best characterized. Mathematical modeling is required to untangle the complexity of its architecture and dynamics. We present a qualitative model of the P. aeruginosa quorum-sensing network including interactions between the las and rhl modules, the signaling molecule PQS and the regulatory proteins Mvfr and VfR. Simulations exemplify the model to reproduce natural network behavior and suggest quorum-sensing responses to pharmacological interference.

4-Butyrolactone↗

PubMed2005

[Detection of quorum-sensing pathway and construction of LuxS gene deletion mutants of group B Streptococcus].

OBJECTIVE: To detect the possible presence of AI-2 quorum-sensing pathway and construct group B Streptococcus (GBS) mutants with deletion of LuxS gene related to quorum-sensing pathway. METHOD: V. harveyi BB170 was employed as the reporter strain to detect AI-2 pathway in GBS, and identification of LuxS homologous gene in GBS type V strain 2603 was performed by software-based analysis. LuxS gene deletion mutant Delta LusX was then constructed in GBS by means of allelic exchange and verified by Southern hybridization analysis. RESULTS: A component in the secretions of GBS could induce bioluminescence activity in the reporter strain, suggesting the presence of AI-2 quorum-sensing pathway in GBS. luxS homologous gene was detected in GBS and LuxS gene deletion mutants was successfully constructed in GBS Ia 515 and V 2603 strains. CONCLUSION: This study establishes a bacterial model for studying the role of LuxS molecule in AI-2 quorum-sensing pathway in GBS and provides new insights into virulence regulation mechanism of GBS.

Bacterial Adhesion↗

PubMed2006

Genetic and phenotypic diversity of quorum-sensing systems in clinical and environmental isolates of Vibrio cholerae.

Vibrio cholerae is the causative agent of cholera, a severe and devastating diarrheal disease. V. cholerae lives naturally in various aquatic habitats during interepidemic periods. Recent studies reveal that quorum-sensing systems, which exist in many bacteria and help them monitor their population densities and regulate various cellular functions, control V. cholerae pathogenesis, biofilm formation, and protease production. In this study we surveyed quorum-sensing systems in 16 geographically diverse V. cholerae strains from epidemic-causing O1 and O139 strains as well as non-O1/non-O139 and environmental isolates and discovered an unexpectedly high rate of dysfunctional components. We also found that a functional quorum-sensing system conferred a survival advantage on bacteria in biofilms when the bacteria were exposed to seawater, though quorum sensing was less important to survival in a planktonic state under the same conditions. These findings suggest that variations in quorum-sensing systems are due to environmental selective pressures and might be beneficial to V. cholerae's fitness under certain conditions found in its natural reservoirs.

Amino Acid Sequence↗

PubMed2001

Pseudomonas aeruginosa mutations in lasI and rhlI quorum sensing systems result in milder chronic lung infection.

To understand the importance of quorum sensing in chronic Pseudomonas aeruginosa lung infection, the in vivo pathogenic effects of the wild-type P. aeruginosa PAO1 and its double mutant, PAO1 lasI rhlI, in which the signal-generating parts of the quorum sensing systems are defective were compared. The rat model of P. aeruginosa lung infection was used in the present study. The rats were killed on days 3, 7, 14 and 28 after infection with the P. aeruginosa strains. The results showed that during the early stages of infection, the PAO1 double mutant induced a stronger serum antibody response, higher production of pulmonary interferon gamma, and more powerful blood polymorphonuclear leukocyte (PMN) chemiluminescence compared to its wild-type counterpart. On days 14 and 28 post-infection, significantly milder lung pathology, a reduction in the number of mast cells present in the lung foci, a reduced number of lung bacteria, and minor serum IgG and IgG1 responses but increased lung interferon gamma production were detected in the group infected with the PAO1 double mutant when compared with the PAO1-infected group. Delayed immune responses were observed in the PAO1-infected group and they might be associated with the production of virulence factors that are controlled by the quorum sensing systems. The conclusion of this study is that functional lasI and rhlI genes of P. aeruginosa PAO1 play a significant role during lung infection.

Animals↗

PubMed2001

The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule.

Many bacteria control gene expression in response to cell population density, and this phenomenon is called quorum sensing. In Gram-negative bacteria, quorum sensing typically involves the production, release and detection of acylated homoserine lactone signalling molecules called autoinducers. Vibrio harveyi, a Gram-negative bioluminescent marine bacterium, regulates light production in response to two distinct autoinducers (AI-1 and AI-2). AI-1 is a homoserine lactone. The structure of AI-2 is not known. We have suggested previously that V. harveyi uses AI-1 for intraspecies communication and AI-2 for interspecies communication. Consistent with this idea, we have shown that many species of Gram-negative and Gram-positive bacteria produce AI-2 and, in every case, production of AI-2 is dependent on the function encoded by the luxS gene. We show here that LuxS is the AI-2 synthase and that AI-2 is produced from S-adenosylmethionine in three enzymatic steps. The substrate for LuxS is S-ribosylhomocysteine, which is cleaved to form two products, one of which is homocysteine, and the other is AI-2. In this report, we also provide evidence that the biosynthetic pathway and biochemical intermediates in AI-2 biosynthesis are identical in Escherichia coli, Salmonella typhimurium, V. harveyi, Vibrio cholerae and Enterococcus faecalis. This result suggests that, unlike quorum sensing via the family of related homoserine lactone autoinducers, AI-2 is a unique, 'universal' signal that could be used by a variety of bacteria for communication among and between species.

4-Butyrolactone↗

PubMed2001

Detection, purification and characterisation of quorum-sensing signal molecules in plant-associated bacteria.

Quorum sensing (also called autoinduction) is a term that describes an environmental sensing system that allows bacteria to monitor their own population density. Autoinduction relies upon the interaction of a small diffusible signal molecule (the autoinducer) with a transcriptional activator protein to couple gene expression with cell population density. These signal molecules diffuse from bacterial cells and accumulate in the environment as a function of cell growth. Once a threshold concentration is reached, these signals serve as co-inducers to regulate the transcription of (a) set(s) of target genes. In Gram-negative bacteria, most autoinducers belong to the family of N-acylhomoserine lactones (AHLs). The detection of AHLs (or AHL-like activities) has been greatly facilitated by the development of sensitive bioassays that allow fast screening of microorganisms for diffusible signal molecules. AHL or diketopiperazine-mediated cell-cell signalling play roles in regulating different bacterial functions, such as antibiotic biosynthesis, production of virulence factors, exopolysaccharide biosynthesis, bacterial swarming, plasmid conjugal transfer and transition into the stationary phase. Several bacterial species that interact with plants produce AHL-like compounds. In this review, we will summarise the current knowledge about the detection, characterisation and purification of quorum-sensing molecules from plant-associated bacteria. We will also discuss some of the future prospects and biotechnological applications of autoinducers.

4-Butyrolactone↗

PubMed1996

A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS.

In Pseudomonas aeruginosa, the production of many virulence factors and secondary metabolites is regulated in concert with cell density through quorum sensing. Two quorum-sensing regulons have been identified in which the LuxR homologues LasR and RhlR are activated by N-(3-oxododecanoyl)-L-homoserine lactone (OdDHL) and N-butanoyl-L-homoserine lactone (BHL) respectively. The lasR and rhlR genes are linked to the luxl homologues lasl and rhll, which are responsible for synthesis of OdDHL and BHL, respectively. As lasRl and rhlRl are both involved in regulating synthesis of exoenzymes such as elastase, we sought to determine the nature of their interrelationship. By using lacZ transcriptional fusions in both homologous (P. aeruginosa) and heterologous (Escherichia coli) genetic backgrounds we provide evidence that (i) lasR is expressed constitutively throughout the growth cycle, (ii) rhlR expression is regulated by LasR/OdDHL, and (iii) that RhlR/BHL regulates rhll. We also show that expression of the stationary-phase sigma factor gene rpoS is abolished in a P. aeruginosa lasR mutant and in the pleiotropic BHL-negative mutant PANO67. Furthermore, our data reveal that kin E. coli, an rpoS-lacZ fusion is regulated directly by RhlR/BHL. Taken together, these results indicate that P. aeruginosa employs a multilayered hierarchical quorum-sensing cascade involving RhlR/BHL and LasR/OdDHL, interlinked via RpoS, to integrate the regulation of virulence determinants and secondary metabolites with adaptation and survival in the stationary phase.

Bacterial Proteins↗

PubMed2006

Regulation of quorum sensing in Pseudomonas.

Bacteria use small signal molecules in order to monitor their population density and coordinate gene regulation in a process called quorum sensing. In Gram-negative bacteria, the most common signal molecules are acylated homoserine lactones. Several Pseudomonas species produce acylated homoserine lactones that control important functions including pathogenicity and plant growth promotion. Many reports indicate that the quorum sensing systems of Pseudomonas are significantly regulated and interconnected with regulons of other global regulators. The integration of quorum sensing into additional regulatory circuits increases the range of environmental and metabolic signals beyond that of cell density, as well as further tuning the timing of the response. This review will focus on the regulation of quorum sensing in Pseudomonas, highlighting a complex response that might serve a given species to adapt in its particular environment.

Bacterial Physiological Phenomena↗

PubMed2006

The HD-GYP domain of RpfG mediates a direct linkage between the Rpf quorum-sensing pathway and a subset of diguanylate cyclase proteins in the phytopathogen Xanthomonas axonopodis pv citri.

Bacteria use extracellular levels of small diffusible autoinducers to estimate local cell-density (quorum-sensing) and to regulate complex physiological processes. The quorum-sensing signal transduction pathway of Xanthomonas spp. phytopathogens has special features that distinguish it from that of other pathogens. This pathway consists of RpfF, necessary for the production of the unique autoinducer 'diffusible signalling factor' (DSF), and RpfC and RpfG, a two-component system necessary for the DSF-dependent production of extracellular pathogenicity factors and cellular dispersion. Yeast two-hybrid and direct in vitro assays were used to identify interactions involving the Rpf group of proteins. We show that RpfC, a protein consisting of N-terminal transmembrane, histidine kinase, response-regulator and C-terminal histidine phosphotransfer domains interacts with both RpfG, a protein consisting of an N-terminal response regulator domain and a C-terminal HD-GYP domain, and with RpfF. We also show that RpfC interacts with the only known homologue of 'conditioned medium factor', which is involved in quorum-sensing in Dictyostelium discoideum under conditions of nutritional stress. Furthermore, RpfCG is shown to interact with a second two-component system made up of NtrB and NtrC homologues. Finally we show that the recently characterized HD-GYP phosphodiesterase domain of RpfG interacts directly with diguanylate cyclase GGDEF domain-containing proteins coded by the Xanthomonas axonopodis pv. citri genome, which in other bacteria produce cyclic diGMP, an important second messenger involved in the regulation of complex bacterial processes including biofilm production, virulence and motility. These results demonstrate a direct physical linkage between quorum-sensing and cyclic diGMP signalling pathways in bacteria.

Amino Acid Sequence↗

PubMed2006

Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis.

Nosocomial infections caused by Staphylococcus epidermidis are characterized by biofilm formation on implanted medical devices. Quorum-sensing regulation plays a major role in the biofilm development of many bacterial pathogens. Here, we describe luxS, a quorum-sensing system in staphylococci that has a significant impact on biofilm development and virulence. We constructed an isogenic DeltaluxS mutant strain of a biofilm-forming clinical isolate of S. epidermidis and demonstrated that luxS signaling is functional in S. epidermidis. The mutant strain showed increased biofilm formation in vitro and enhanced virulence in a rat model of biofilm-associated infection. Genetic complementation and addition of autoinducer 2-containing culture filtrate restored the wild-type phenotype, demonstrating that luxS repressed biofilm formation through a cell-cell signaling mechanism based on autoinducer 2 secretion. Enhanced production of the biofilm exopolysaccharide polysaccharide intercellular adhesin in the mutant strain is presumably the major cause of the observed phenotype. The agr quorum-sensing system has previously been shown to impact biofilm development and biofilm-associated infection in a way similar to that of luxS, although by regulation of different factors. Our study indicates a general scheme of quorum-sensing regulation of biofilm development in staphylococci, which contrasts with that observed in many other bacterial pathogens.

Animals↗

PubMed2005

Quorum-sensing mutations affect attachment and stability of Burkholderia cenocepacia biofilms.

Biofilm formation in Burkholderia cenocepacia has been shown to rely in part on acylhomoserine lactone-based quorum sensing. For many other bacterial species, it appears that both the initial adherence and the later stages of biofilm maturation are affected when quorum sensing pathways are inhibited. In this study, we examined the effects of mutations in the cepIR and cciIR quorum-sensing systems of Burkholderia cenocepacia K56-2 with respect to biofilm attachment and antibiotic resistance. We also examined the role of the cepIR system in biofilm stability and structural development. Using the high-throughput MBEC assay system to produce multiple equivalent biofilms, the biomasses of both the cepI and cepR mutant biofilms, measured by crystal violet staining, were less than half of the value observed for the wild-type strain. Attachment was partially restored upon providing functional gene copies via multicopy expression vectors. Surprisingly, neither the cciI mutant nor the double cciI cepI mutant was deficient in attachment, and restoration of the cciI gene resulted in less attachment than for the mutants. Meanwhile, the cciR mutant did show a significant reduction in attachment, as did the cciR cepIR mutant. While there was no change in antibiotic susceptibility with the individual cepIR and cciIR mutants, the cepI cciI mutant biofilms were more sensitive to ciprofloxacin. A significant increase in sensitivity to removal by sodium dodecyl sulfate was seen for the cepI and cepR mutants. Flow cell analysis of the individual cepIR mutant biofilms indicated that they were both structurally and temporally impaired in attachment and development. These results suggest that biofilm structural defects might be present in quorum-sensing mutants of B. cenocepacia that affect the stability and resistance of the adherent cell mass, providing a basis for future studies to design preventative measures against biofilm formation in this species, an important lung pathogen of cystic fibrosis patients.

Anti-Bacterial Agents↗

PubMed2006

Quorum-sensing antagonistic activities of azithromycin in Pseudomonas aeruginosa PAO1: a global approach.

The administration of macrolides such as azithromycin for chronic pulmonary infection of cystic fibrosis patients has been reported to be of benefit. Although the mechanisms of action remain obscure, anti-inflammatory effects as well as interference of the macrolide with Pseudomonas aeruginosa virulence factor production have been suggested to contribute to an improved clinical outcome. In this study we used a systematic approach and analyzed the impact of azithromycin on the global transcriptional pattern and the protein expression profile of P. aeruginosa PAO1 cultures versus those in untreated controls. The most remarkable result of this study is the finding that azithromycin exhibited extensive quorum-sensing antagonistic activities. In accordance with the inhibition of the quorum-sensing systems, virulence factor production was diminished and the oxidative stress response was impaired, whereas the type III secretion system was strongly induced. Moreover, P. aeruginosa motility was reduced, which probably accounts for the previously observed impaired biofilm formation capabilities of azithromycin-treated cultures. The interference of azithromycin with quorum-sensing-dependent virulence factor production, biofilm formation, and oxidative stress resistance in P. aeruginosa holds great promise for macrolide therapy in cystic fibrosis. Clearly quorum-sensing antagonist macrolides should be paid more attention in the management of chronic P. aeruginosa infections, and as quorum-sensing antagonists, macrolides might gain vital importance for more general application against chronic infections.

Anti-Bacterial Agents↗