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PubMed2004

Quorum quenching: enzymatic disruption of N-acylhomoserine lactone-mediated bacterial communication in Burkholderia thailandensis.

Many species of gram-negative bacteria communicate by synthesizing, secreting, and responding to N-acylhomoserine lactones (AHLs), a mechanism termed quorum sensing. Several investigations have characterized numerous AHL-degrading enzymes (AiiA lactonases) encoded by environmental isolates of Bacillus spp. The Burkholderia thailandensis quorum system is comprised of at least three AHL synthases (AHSs) and five transcriptional regulators belonging to the LuxIR class of proteins. Expression of the Bacillus anthracis (Ames strain) AiiA lactonase in B. thailandensis completely abolished the accumulation of N-decanoylhomoserine lactone (C(10)-HSL) and N-octanoylhomoserine lactone (C(8)-HSL), reduced N-hexanoylhomoserine lactone (C(6)-HSL) levels, altered both swarming and twitching motility, caused a significant increase in generation time, and affected carbon metabolism. In contrast, heterologous expression of the Bacillus cereus strain A24 AiiA lactonase in B. thailandensis reduced the concentrations of C(6)-HSL, C(8)-HSL, and C(10)-HSL to nondetectable levels; altered both swarming and twitching motility; and caused fluctuations in carbon utilization. Individual disruption of the B. thailandensis AHSs, specifically disruption of the btaI1 and btaI3 genes, which encode the proteins that direct the synthesis of C(8)-HSL and C(6)-HSL, respectively, caused the hyper-beta-hemolysis of sheep erythrocytes on blood agar plates. In contrast, AHL cleavage in B. thailandensis by the Bacillus AiiA lactonases failed to enhance beta-hemolytic activity. The results of this study demonstrate that heterologous expression of Bacillus sp. AiiA lactonases in B. thailandensis reduced AHL accumulation, affected both swarming and twitching motility, increased generation time, altered substrate utilization, and prevented the beta-hemolysis of sheep erythrocytes.

4-Butyrolactone↗
PubMed2004

Enterococcus faecalis senses target cells and in response expresses cytolysin.

Many virulent strains of Enterococcus faecalis produce a two-subunit toxin, termed cytolysin. Cytolysin expression is regulated by one of the subunits (CylL(S)'') through a quorum-sensing autoinduction mechanism. We found that when target cells are absent, the other subunit (CylL(L)'') forms a complex with CylL(S)'', blocking it from autoinducing the operon. When target cells are present, however, CylL(L)'' binds preferentially to the target, allowing free CylL(S)'' to accumulate above the induction threshold. Thus, enterococci use CylL(L)'' to actively probe the environment for target cells, and when target cells are detected, allows the organism to express high levels of cytolysin in response.

Bacterial Proteins↗
PubMed2005

Recognition of host immune activation by Pseudomonas aeruginosa.

It is generally reasoned that lethal infections caused by opportunistic pathogens develop permissively by invading a host that is both physiologically stressed and immunologically compromised. However, an alternative hypothesis might be that opportunistic pathogens actively sense alterations in host immune function and respond by enhancing their virulence phenotype. We demonstrate that interferon-gamma binds to an outer membrane protein in Pseudomonas aeruginosa, OprF, resulting in the expression of a quorum-sensing dependent virulence determinant, the PA-I lectin. These observations provide details of the mechanisms by which prokaryotic organisms are directly signaled by immune activation in their eukaryotic host.

Adhesins, Bacterial↗
PubMed2006

The Pseudomonas aeruginosa universal stress protein PA4352 is essential for surviving anaerobic energy stress.

During infection of the cystic fibrosis (CF) lung, Pseudomonas aeruginosa microcolonies are embedded in the anaerobic CF mucus. This anaerobic environment seems to contribute to the formation of more robust P. aeruginosa biofilms and to an increased antibiotic tolerance and therefore promotes persistent infection. This study characterizes the P. aeruginosa protein PA4352, which is important for survival under anaerobic energy stress conditions. PA4352 belongs to the universal stress protein (Usp) superfamily and harbors two Usp domains in tandem. In Escherichia coli, Usp-type stress proteins are involved in survival during aerobic growth arrest and under various other stresses. A P. aeruginosa PA4352 knockout mutant was tested for survival under several stress conditions. We found a decrease in viability of this mutant compared to the P. aeruginosa wild type during anaerobic energy starvation caused by the missing electron acceptors oxygen and nitrate. Consistent with this phenotype under anaerobic conditions, the PA4352 knockout mutant was also highly sensitive to carbonyl cyanide m-chlorophenylhydrazone, the chemical uncoupler of the electron transport chain. Primer extension experiments identified two promoters upstream of the PA4352 gene. One promoter is activated in response to oxygen limitation by the oxygen-sensing regulatory protein Anr. The center of a putative Anr binding site was identified 41.5 bp upstream of the transcriptional start site. The second promoter is active only in the stationary phase, however, independently of RpoS, RelA, or quorum sensing. This is the second P. aeruginosa Usp-type stress protein that we have identified as important for survival under anaerobic conditions, which resembles the environment during persistent infection.

Adaptation, Physiological↗
PubMed2003

Speed versus accuracy in collective decision making.

We demonstrate a speed versus accuracy trade-off in collective decision making. House-hunting ant colonies choose a new nest more quickly in harsh conditions than in benign ones and are less discriminating. The errors that occur in a harsh environment are errors of judgement not errors of omission because the colonies have discovered all of the alternative nests before they initiate an emigration. Leptothorax albipennis ants use quorum sensing in their house hunting. They only accept a nest, and begin rapidly recruiting members of their colony, when they find within it a sufficient number of their nest-mates. Here we show that these ants can lower their quorum thresholds between benign and harsh conditions to adjust their speed-accuracy trade-off. Indeed, in harsh conditions these ants rely much more on individual decision making than collective decision making. Our findings show that these ants actively choose to take their time over judgements and employ collective decision making in benign conditions when accuracy is more important than speed.

Animal Communication↗
PubMed2001

Extracellular sensing and signalling pheromones switch-on thermotolerance and other stress responses in Escherichia coli.

The findings reviewed here overturn a major tenet of bacterial physiology, namely that stimuli which switch-on inducible responses are always detected by intracellular sensors, with all other components and stages in induction also being intracellular. Such an induction mechanism even applies to quorum-sensed responses, and some others which involve functioning of extracellular components, and had previously been believed to occur in all cases. In contrast, for the stress responses reviewed here, triggering is by a quite distinct process, pairs of extracellular components being involved, with the stress sensing component (the extracellular sensing component, ESC) and the signalling component, which derives from it and induces the stress (the extracellular induction component, EIC), being extracellular and the stimulus detection occurring in the growth medium. The ESCs and EICs can also be referred to as extracellular sensing and signalling pheromones, since they are not only needed for induction in the stressed culture, but can act as pheromones in the same region activating other organisms which fail to produce the extracellular component (EC) pair. They can also diffuse to other regions and there act as pheromones influencing unstressed organisms or those which fail to produce such ECs. The cross-talk occurring due to such interactions, can then switch-on stress responses in such unstressed organisms and in those which cannot form the ESC/EIC pair. Accordingly, the ESC/EIC pairs can bring about a form of intercellular communication between organisms. If the unstressed organisms, which are induced to stress tolerance by such extracellular components, are facing impending stress challenge, then the pheromonal activities of the ECs provide an early warning system against stress. The specific ESC/EIC pairs switch-on numerous responses; often these pairs are proteins, but non-protein ECs also occur and for a few systems, full induction needs two ESC/EIC pairs. Most of the above ECs needed for response induction are highly resistant to irreversible inactivation by lethal agents and conditions and, accordingly, many killed cultures still contain ESCs or EICs. If these killed cultures come into contact with unstressed living organisms, the ECs again act pheromonally, altering the tolerance to stress of the living organisms. It has been claimed that bacteria sense increased temperature using ribosomes or the DnaK gene product. The work reviewed here shows that, for thermal triggering of thermotolerance and acid tolerance in E. coli, it is ESCs which act as thermometers.

Culture Media↗
PubMed1999

Bacterial tactic responses.

Many, if not most, bacterial species swim. The synthesis and operation of the flagellum, the most complex organelle of a bacterium, takes a significant percentage of cellular energy, particularly in the nutrient limited environments in which many motile species are found. It is obvious that motility accords cells a survival advantage over non-motile mutants under normal, poorly mixed conditions and is an important determinant in the development of many associations between bacteria and other organisms, whether as pathogens or symbionts and in colonization of niches and the development of biofilms. This survival advantage is the result of sensory control of swimming behaviour. Although too small to sense a gradient along the length of the cell, and unable to swim great distances because of buffetting by Brownian motion and the curvature resulting from a rotating flagellum, bacteria can bias their random swimming direction towards a more favourable environment. The favourable environment will vary from species to species and there is now evidence that in many species this can change depending on the current physiological growth state of the cell. In general, bacteria sense changes in a range of nutrients and toxins, compounds altering electron transport, acceptors or donors into the electron transport chain, pH, temperature and even the magnetic field of the Earth. The sensory signals are balanced, and may be balanced with other sensory pathways such as quorum sensing, to identify the optimum current environment. The central sensory pathway in this process is common to most bacteria and most effectors. The environmental change is sensed by a sensory protein. In most species examined this is a transmembrane protein, sensing the external environment, but there is increasing evidence for additional cytoplasmic receptors in many species. All receptors, whether sensing sugars, amino acids or oxygen, share a cytoplasmic signalling domain that controls the activity of a histidine protein kinase, CheA, via a linker protein, CheW. A reduction in an attractant generally leads to the increased autophosphorylation of CheA. CheA passes its phosphate to a small, single domain response regulator, CheY. CheY-P can interact with the flagellar motor to cause it to change rotational direction or stop. Signal termination either via a protein, CheZ, which increases the dephosphorylation rate of CheY-P or via a second CheY which acts as a phosphate sink, allows the cell to swim off again, usually in a new direction. In addition to signal termination the receptor must be reset, and this occurs via methylation of the receptor to return it to a non-signalling conformation. The way in which bacteria use these systems to move to optimum environments and the interaction of the different sensory pathways to produce species-specific behavioural response will be the subject of this review.

Animals↗
PubMed2002

Control of Escherichia coli growth rate through cell density.

The transition from the exponential to the stationary phase of Escherichia coli cultures has been investigated regarding nutrient availability. This analysis strongly suggests that the declining of the cell division rate is not caused by mere nutrient limitation but also by an immediate sensing of cell concentration. In addition, both the growth rate and the final biomass achieved by a batch culture can be manipulated by altering its density during the early exponential phase. This result, which has been confirmed by using different experimental approaches, supports the hypothesis that the E. coli quorum sensing is not only determined by the release of soluble cell-to-cell communicators. Cell-associated sensing elements might also be involved in modulating the bacterial growth even in the presence of non-limiting (although declining) nutrient concentrations, thus promoting their economical utilisation in dense populations.

Escherichia coli↗
PubMed2004

Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria.

There are two basic types of bacterial communication systems--those in which the signal is directed solely at other organisms and those in which the signal is sensed by the producing organism as well. The former are involved primarily in conjugation; the latter in adaptation to the environment. Gram-positive bacteria use small peptides for both types of signaling, whereas Gram-negative bacteria use homoserine lactones. Since adaptation signals are autoinducers the response is population-density-dependent and has been referred to as "quorum-sensing". Gram-negative bacteria internalize the signals which act upon an intracellular receptor, whereas Gram-positive bacteria use them as ligands for the extracellular receptor of a two-component signaling module. In both cases, the signal activates a complex adaptation response involving many genes.

Amino Acid Sequence↗
PubMed2002

Histidine protein kinases: key signal transducers outside the animal kingdom.

Histidine protein kinases (HPKs) are a large family of signal-transduction enzymes that autophosphorylate on a conserved histidine residue. HPKs form two-component signaling systems together with their downstream target proteins, the response regulators, which have a conserved aspartate in a so-called 'receiver domain' that is phosphorylated by the HPK. Two-component signal transduction is prevalent in bacteria and is also widely used by eukaryotes outside the animal kingdom. The typical HPK is a transmembrane receptor with an amino-terminal extracellular sensing domain and a carboxy-terminal cytosolic signaling domain; most, if not all, HPKs function as dimers. They show little similarity to protein kinases that phosphorylate serine, threonine or tyrosine residues, but may share a distant evolutionary relationship with these enzymes. In excess of a thousand known genes encode HPKs, which are important for multiple functions in bacteria, including chemotaxis and quorum sensing, and in eukaryotes, including hormone-dependent developmental processes. The proteins divide into at least 11 subfamilies, only one of which is present in eukaryotes, suggesting that lateral gene transfer gave rise to two-component signaling in these organisms.

Amino Acid Motifs↗
PubMed2005

Environmentally controlled invasion of cancer cells by engineered bacteria.

Bacteria can sense their environment, distinguish between cell types, and deliver proteins to eukaryotic cells. Here, we engineer the interaction between bacteria and cancer cells to depend on heterologous environmental signals. We have characterized invasin from Yersinia pseudotuburculosis as an output module that enables Escherichia coli to invade cancer-derived cells, including HeLa, HepG2, and U2OS lines. To environmentally restrict invasion, we placed this module under the control of heterologous sensors. With the Vibrio fischeri lux quorum sensing circuit, the hypoxia-responsive fdhF promoter, or the arabinose-inducible araBAD promoter, the bacteria invade cells at densities greater than 10(8)bacteria/ml, after growth in an anaerobic growth chamber or in the presence of 0.02% arabinose, respectively. In the process, we developed a technique to tune the linkage between a sensor and output gene using ribosome binding site libraries and genetic selection. This approach could be used to engineer bacteria to sense the microenvironment of a tumor and respond by invading cancerous cells and releasing a cytotoxic agent.

Adhesins, Bacterial↗
PubMed2002

Characterization of comQ and comX, two genes required for production of ComX pheromone in Bacillus subtilis.

Many microbes use secreted peptide-signaling molecules to stimulate changes in gene expression in response to high population density, a process called quorum sensing. ComX pheromone is a modified 10-amino-acid peptide used by Bacillus subtilis to modulate changes in gene expression in response to crowding. comQ and comX are required for production of ComX pheromone. We found that accumulation of ComX pheromone in culture supernatant paralleled cell growth, indicating that there was no autoinduction of production of ComX pheromone. We overexpressed comQ and comX separately and together and found that overexpression of comX alone was sufficient to cause an increase in production of ComX pheromone and early induction of a quorum-responsive promoter. These results indicate that the extracellular concentration of ComX pheromone plays a major role in determining the timing of the quorum response and that expression of comX is limiting for production of ComX pheromone. We made alanine substitutions in the residues that comprise the peptide backbone of ComX pheromone. Analysis of these mutants highlighted the importance of the modification for ComX pheromone function and identified three residues (T50, G54, and D55) that are unlikely to interact with proteins involved in production of or response to ComX pheromone. We have also identified and mutated a putative isoprenoid binding domain of ComQ. Mutations in this domain eliminated production of ComX pheromone, consistent with the hypothesis that ComQ is involved in modifying ComX pheromone and that the modification is likely to be an isoprenoid.

Amino Acid Sequence↗
PubMed1996

Control of cell division in Escherichia coli: regulation of transcription of ftsQA involves both rpoS and SdiA-mediated autoinduction.

The conditioning of culture medium by the production of growth-regulatory substances is a well-established phenomenon with eukaryotic cells. It has recently been shown that many prokaryotes are also capable of modulating growth, and in some cases sensing cell density, by production of extracellular signaling molecules, thereby allowing single celled prokaryotes to function in some respects as multicellular organisms. As Escherichia coli shifts from exponential growth to stationary growth, many changes occur, including cell division leading to formation of short minicells and expression of numerous genes not expressed in exponential phase. An understanding of the coordination between the morphological changes associated with cell division and the physiological and metabolic changes is of fundamental importance to understanding regulation of the prokaryotic cell cycle. The ftsQA genes, which encode functions required for cell division in E. coli, are regulated by promoters P1 and P2, located upstream of the ftsQ gene. The P1 promoter is rpoS-stimulated and the second, P2, is regulated by a member of the LuxR subfamily of transcriptional activators, SdiA, exhibiting features characteristic of an autoinduction (quorum sensing) mechanism. The activity of SdiA is potentiated by N-acyl-homoserine lactones, which are the autoinducers of luciferase synthesis in luminous marine bacteria as well as of pathogenesis functions in several pathogenic bacteria. A compound(s) produced by E. coli itself during growth in Luria Broth stimulates transcription from P2 in an SdiA-dependent process. Another substance(s) enhances transcription of rpoS and (perhaps indirectly) of ftsQA via promoter P1. It appears that this bimodal control mechanism may comprise a fail-safe system, such that transcription of the ftsQA genes may be properly regulated under a variety of different environmental and physiological conditions.

Bacterial Proteins↗
PubMed2003

From motility to virulence: Sensing and responding to environmental signals in Vibrio cholerae.

Sensing its changing environment is key for Vibrio cholerae when making the transition from an aquatic lifestyle to one more suited to a human host. An inverse correlation between motility and virulence gene expression has been reported, with the NADH : ubiquinone oxidoreductase system which powers motility by generating a sodium-motive force, playing a pivotal role. Recent studies have demonstrated that bile inhibits activity of the transcription factor ToxT, a protein responsible for direct activation of numerous virulence gene promoters. In addition, recent technological advances have allowed for the analysis of in-vivo-induced genes and assessment of their timing of expression. Use of recombinase-based in vivo expression technology has revealed that the toxin-coregulated pilus (a colonization factor) is expressed before cholera toxin. Components of an acid-tolerance response system have also been found using this method as well as signature-tagged mutagenesis. Finally, a role for quorum sensing in regulation of virulence gene expression has recently been established.

Cholera↗
PubMed2003

Arthrobacter strain VAI-A utilizes acyl-homoserine lactone inactivation products and stimulates quorum signal biodegradation by Variovorax paradoxus.

Many Proteobacteria produce acyl-homoserine lactones (acyl-HSLs) and employ them as dedicated cell-to-cell signals in a process known as quorum sensing. Previously, Variovorax paradoxus VAI-C was shown to utilize diverse acyl-HSLs as sole sources of energy and nitrogen. We describe here the properties of a second isolate, Arthrobacter strain VAI-A, obtained from the same enrichment culture that yielded V. paradoxus VAI-C. Although strain VAI-A grew rapidly and exponentially on a number of substrates, it grew only slowly and aberrantly (i.e., linearly) in media amended with oxohexanoyl-HSL as the sole energy source. Increasing the culture pH markedly improved the growth rate in media containing this substrate but did not abolish the aberrant kinetics. The observed growth was remarkably similar to the known kinetics of the pH-influenced half-life of acyl-HSLs, which decay chemically to yield the corresponding acyl-homoserines. Strain VAI-A grew rapidly and exponentially when provided with an acyl-homoserine as the sole energy or nitrogen source. The isolate was also able to utilize HSL as a sole source of nitrogen but not as energy for growth. V. paradoxus, known to release HSL as a product of quorum signal degradation, was examined for the ability to support the growth of Arthrobacter strain VAI-A in defined cocultures. It did. Moreover, the acyl-HSL-dependent growth rate and yield of the coculture were dramatically superior to those of the monocultures. This suggested that the original coenrichment of these two organisms from the same soil sample was not coincidental and that consortia may play a role in quorum signal turnover and mineralization. The fact that Arthrobacter strain VAI-A utilizes the two known nitrogenous degradation products of acyl-HSLs, acyl-homoserine and HSL, begins to explain why none of the three compounds are known to accumulate in the environment.

4-Butyrolactone↗
PubMed2003

A plasmid-borne Rap-Phr system of Bacillus subtilis can mediate cell-density controlled production of extracellular proteases.

Bacillus subtilis uses two-component signal transduction systems to sense intra- and extracellular stimuli to adapt to fluctuating environmental situations. Regulator aspartate phosphatases (Raps) have important roles in these processes, as they can dephosphorylate certain response-regulators, and are themselves subject to cell-density-controlled inhibition by secreted Phr (phosphate regulator) peptides. Eleven chromosomal genes encode this family of phosphatases, but in addition, certain strains contain endogenous plasmids with genes for homologous Rap-Phr systems. Plasmid pTA1060 encodes Rap60 and its antagonistic signalling molecule Phr60. Strikingly, expression of Rap60 in B. subtilis 168 strongly repressed the production of proteolytic enzymes. In fact, the transcription of the aprE gene, encoding a major extracellular protease, was shown to be decreased upon Rap60 expression, whereas this effect could be antagonized by the extracellular addition of synthetic Phr60 pentapeptide. Finally, transcription studies suggest that Rap60 dephosphorylates a component of the phosphorelay and is coupled to aprE transcription by the transition-state regulator AbrB. In conclusion, these data show that endogenous plasmids contain functional Rap-Phr systems and for the first time, that Rap-Phr systems can mediate cell-density controlled production of secreted proteases. This quorum-sensing mechanism might enable B. subtilis to suppress protease production under conditions of low cell densities when nutrients are still available in sufficient amounts.

Bacillus subtilis↗
PubMed2004

Gene expression in Bacillus subtilis surface biofilms with and without sporulation and the importance of yveR for biofilm maintenance.

Five independent DNA microarray experiments were used to study the gene expression profile of a 5-day Bacillus subtilis air-liquid interface biofilm relative to planktonic cells. Both wild-type B. subtilis and its sporulation mutant (DeltaspoIIGB::erm) were investigated to discern the important biofilm genes (in the presence and absence of sporulation). The microarray results indicated that suspension cells were encountering anaerobic conditions, and the air-liquid interface biofilm was metabolically active. For the statistically significant differential expression (P < 0.05), there were 342 genes induced and 248 genes repressed in the wild-type biofilm, whereas 371 genes were induced and 128 genes were repressed in the sporulation mutant biofilm. The microarray results were confirmed with RNA dot blotting. A small portion of cells (1.5%) in the wild-type biofilm formed spores and sporulation genes were highly expressed. In the biofilm formed by the sporulation mutant, competence genes (comGA, srfAA, srfAB, srfAD, and comS) were induced which indicate a role for quorum sensing (bacterial gene expression controlled by sensing their population) in biofilms. There were 53 genes consistently induced in the biofilms of both the wild-type strain and its spoIIGB mutant-those genes have functions for transport, metabolism, antibiotic production-and 26 genes with unknown functions. Besides the large number of genes with known functions induced in the biofilm (121 genes in the wild-type biofilm and 185 genes in the sporulation mutant biofilm), some genes with unknown functions were also induced (221 genes in the wild-type biofilm and 186 genes in the sporulation mutant biofilm), such as the yve operon which appears to be involved in polysaccharide synthesis and the ybc operon which inhibits the growth of competitors for nutrients. A knockout mutant of yveR was constructed, and the mutant showed major defects in biofilm maintenance. Both the wild-type strain and its sporulation mutant formed normal biofilms, suggesting complete sporulation is not necessary for biofilm formation. The expression profiles of these two strains share more repressed genes than induced genes, suggesting that the biofilm cells repress similar pathways in response to starvation and high cell density.

Bacillus subtilis↗
PubMed2004

A proteomic approach to study Salmonella typhi periplasmic proteins altered by a lack of the DsbA thiol: disulfide isomerase.

Two-dimensional electrophoresis (2-DE) was used to analyze the pleiotropic effects of a deficiency in DsbA, a periplasmic disulfide-bond oxidoreductase, in Salmonella typhi. With this aim, the dsbA gene was cloned and assayed for activity in a dsbA-null mutant of Escherichia coli. A dsbA/chloramphenicol acetylase construct was then used to disrupt the wild-type gene of S. typhi. The resultant dsbA-null mutant of S. typhi, like the E. coli mutant, exhibited a lack of flagellation and of glucose-1-phosphatase activity. Periplasmic extracts from the parental and mutant strains were analyzed by 2-DE using standard denaturing and nondenaturing conditions. Differences in protein expression were more marked in nondenaturing conditions. Ninety-nine protein spots were analyzed by peptide mass fingerprinting, and 65 spots were identified by searching a S. typhi database. Twenty-five spots were exclusively detected in the wild-type strain, 10 were found only in the mutant strain, and 21 were common to both strains. We observed a lack of DsbA, glucose-1-phosphatase and flagellin in the dsbA-null mutant, which explains two of the observed phenotypes. The AI-2 autoinducer-producing protein LuxS, which is involved in quorum-sensing signalling was also absent.

Bacterial Proteins↗