Strain-dependent diversity in the Pseudomonas aeruginosa quorum-sensing regulon

Abstract

Quorum sensing allows bacteria to sense and respond to changes in population density. Acyl-homoserine lactones serve as quorumsensing signals for many Proteobacteria, and acyl-homoserine lactone signaling is known to control cooperative activities. Quorum-controlled activities vary from one species to another. Quorum-sensing controls a constellation of genes in the opportunistic pathogen Pseudomonas aeruginosa, which thrives in a number of habitats ranging from soil and water to animal hosts. We hypothesized that there would be significant variation in quorumsensing regulons among strains of P. aeruginosa isolated from different habitats and that differences in the quorum-sensing regulons might reveal insights about the ecology of P. aeruginosa. As a test of our hypothesis we used RNA-seq to identify quorumcontrolled genes in seven P. aeruginosa isolates of diverse origins. Although our approach certainly overlooks some quorum-sensingregulated genes we found a shared set of genes, i.e., a core quorum-controlled gene set, and we identified distinct, strain-variable sets of quorum-controlled genes, i.e., accessory genes. Some quorumcontrolled genes in some strains were not present in the genomes of other strains. We detected a correlation between traits encoded by some genes in the strain-variable subsets of the quorum regulons and the ecology of the isolates. These findings indicate a role for quorum sensing in extension of the range of habitats in which a species can thrive. This study also provides a framework for understanding the molecular mechanisms by which quorum-sensing systems operate, the evolutionary pressures by which they are maintained, and their importance in disparate ecological contexts.bacterial communication | systems biology | transcription control B acteria use quorum-sensing signals to communicate with each other and control gene expression in a cell density-dependent manner. Many species of Proteobacteria use diffusible acyl-homoserine lactones (AHLs) as quorum-sensing signals. AHLs are produced by signal synthase enzymes and are detected by signalspecific transcriptional regulators. AHL quorum-sensing circuits regulate a wide spectrum of phenotypes in a diverse array of α-, β-, and γ-Proteobacteria (1). Interspecies differences in quorum regulons often are a reflection of the diverse habitats that bacteria occupy, and quorum-controlled phenotypes often play a crucial role in niche persistence. The classic example is quorum control of luminescence in Vibrio fischeri, which allows this bacterium to discriminate between its free-living, low-populationdensity seawater habitat and its high-density symbiotic habitats, the light organs of certain fish and squid (2, 3). It is well established that there are species-specific differences in quorum regulons, but there is little information regarding the possibility of intraspecies strain-specific differences. We hypothesized that, particularly for versatile species that occupy diverse niches, there might be a shared core of quorum-controlled genes an...

Global Analysis of the Burkholderia thailandensis Quorum Sensing-Controlled Regulon

“…This gene is also conserved in B. pseudomallei. Chitin-binding proteins, as well as chitinases, have been identified in the QS regulons of multiple species, including P. aeruginosa (18,58), B. cenocepacia (38,59), and C. violaceum (60). A gene annotated as kdpF is also strongly activated by BtaR3 (28-fold), and is adjacent to and presumably cotranscribed with kdpA (8-fold).…”

“…We prepared cDNA libraries as described elsewhere (18) by using the 949-primer set and isolated RNA. Briefly, a cDNA strand was generated for the RNA.…”

Exploiting Quorum Sensing To Confuse Bacterial Pathogens

“…Complete elimination of QS signals is not always required in order to achieve attenuation of virulence, however, as was seen in S. aureus, where even a delay in agr signaling was sufficient to reduce pathogenicity (224). Additionally, it is becoming increasingly apparent that there can be diversity in the QS regulon between different strains of the same species, as has recently been found in P. aeruginosa (355), in which case QSI may be more effective against certain strains of a pathogen and less effective against others. Thus, the efficacy of QSI will likely be species, and perhaps strain, specific due to the mechanistic intricacies of each individual system and the distinct role that QS plays during infection by different pathogens.…”

Quorum Sensing Is Accompanied by Global Metabolic Changes in the Opportunistic Human Pathogen Pseudomonas aeruginosa

“…Not surprisingly then, several lines of evidence suggest that QS may impinge on the metabolic network of the cell. For example, transcriptomic and proteomic studies have pinpointed QSdependent changes at key branchpoints in central metabolism (24,25), and metabolic functions are represented among the "core" list of QS-regulated genes in P. aeruginosa (7,18,26). However, it is difficult to draw quantitative conclusions about the metabolic consequences of such gene expression changes without measuring the metabolites involved (7,18,(27)(28)(29).…”