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Cross-regulation between the response regulators PhoB and TctD allows for the integration of diverse environmental signals in Pseudomonas aeruginosa

ABSTRACT: Two-component systems (TCS) serve as basic stimulus-response coupling mechanisms to allow organisms to sense and respond to a large variety of environmental conditions. In the opportunistic pathogen Pseudomonas aeruginosa, more than 100 genes encode TCS components. To avoid unwanted cross-talk between TCSs, the signaling cascades are usually very specific, with one sensor talking to its cognate response regulator. However, cross-regulation may provide effective means to integrate different environmental stimuli into a harmonized output response and thus to coordinate gene expression in response to complex and challenging habitats. Here, we applied a protein-fragment complementation assay (PCA) and identified a direct interaction of two response regulators of the OmpR/PhoB subfamily, namely PhoB and TctD in P. aeruginosa in vivo. Transcriptional profiling and ChIP-seq analysis uncovered adjacent bipartite binding motifs of the two response regulators in 8 promoter regions, of which 6 showed a common PhoB-TctD binding motif with a fixed spacing between the two motifs. We further demonstrate that phosphate limitation exhibits a PhoB-dependent activating activity on the expression of those genes, whereas the presence of a preferred carbon source inhibits gene expression in a TctD-dependent manner. Thus, the perception and the integration of two important environmental signals are achieved by a titration of the relative amounts of two phosphorylated response regulators that inversely regulate a common subset of genes. In conclusion, our results shed light on the general principles underlying two-component signal transduction pathways and the exploitation of cross-regulation to adapt bacterial behavior to complex environments.

ORGANISM(S): Pseudomonas aeruginosa UCBPP-PA14

PROVIDER: GSE64056 | GEO | 2015/06/08

SECONDARY ACCESSION(S): PRJNA269980

REPOSITORIES: GEO

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Project description:Membrane protein and phospholipid (PL) compositions change in response to environmental cues and during infections. Covalent modification (e.g., unsaturation and cyclopropanation) and remodeling the acyl chain length of PLs is an important bacterial adaptation mechanism. However, little is known about which bacterial pathways are regulated in response to the alteration of PL composition. Here, we show that P. aeruginosa PlaF, which modulates membrane PL composition, is important for biofilm biogenesis, and we performed whole-cell quantitative proteomics of P. aeruginosa wild-type and ∆plaF biofilms to identify pathways regulated by PlaF. The results revealed profound alterations in the abundance of 14 two-component systems (TCS), including the PprA-PprB, which controls the transition to biofilm. Activation of PprA-the PprB system observed by proteomics was confirmed by mRNA quantification. Furthermore, we have observed a unique phosphorylation pattern of transcriptional regulators, transporters and metabolic enzymes, and differential production of nine proteases in ∆plaF, indicating that PlaF-mediated virulence adaptation involves complex transcriptional and post-transcriptional regulation. Moreover, proteomics revealed that the pyoverdin-mediated iron uptake pathway proteins were depleted in ∆plaF, which agrees with decreased concentrations of extracellular pyoverdine and intracellular iron in ∆plaF and is likely responsible for its prolonged lag phase due to reduced iron uptake. Conversely, the accumulation of proteins from alternative iron-uptake systems in ∆plaF suggests that PlaF may function as a switch between different iron-acquisition pathways. The observation that ∆plaF accumulates PL-acyl chain modifying enzymes and PlsX, an initiator of de novo PL synthesis, reveals novel insights into the relationship between degradation, covalent modification and biosynthesis of PLs for membrane homeostasis. Although the precise mechanism by which PlaF simultaneously affects multiple pathways remains to be elucidated, we suggest that PlaF-catalyzed degradation of PLs is a signal which is amplified by proteins of TCS, phosphorylation and proteolytic degradation systems to elicit the global adaptive response in P. aeruginosa.

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Cross-regulation between the response regulators PhoB and TctD allows for the integration of diverse environmental signals in Pseudomonas aeruginosa

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