A Distinct QscR Regulon in the Pseudomonas aeruginosa Quorum-Sensing Circuit

Department of Microbiology, University of Washington, Seattle 98195-7242, USA.
Journal of Bacteriology (Impact Factor: 2.81). 06/2006; 188(9):3365-70. DOI: 10.1128/JB.188.9.3365-3370.2006
Source: PubMed


The opportunistic pathogen Pseudomonas aeruginosa possesses two complete acyl-homoserine lactone (acyl-HSL) signaling systems. One system consists of LasI and LasR, which generate a 3-oxododecanoyl-homoserine lactone signal and respond to that signal, respectively. The other system is RhlI and RhlR, which generate butanoyl-homoserine lactone and respond to butanoyl-homoserine lactone, respectively. These quorum-sensing systems control hundreds of genes. There is also an orphan LasR-RhlR homolog, QscR, for which there is no cognate acyl-HSL synthetic enzyme. We previously reported that a qscR mutant is hypervirulent and showed that QscR transiently represses a few quorum-sensing-controlled genes. To better understand the role of QscR in P. aeruginosa gene regulation and to better understand the relationship between QscR, LasR, and RhlR control of gene expression, we used transcription profiling to identify a QscR-dependent regulon. Our analysis revealed that QscR activates some genes and represses others. Some of the repressed genes are not regulated by the LasR-I or RhlR-I systems, while others are. The LasI-generated 3-oxododecanoyl-homoserine lactone serves as a signal molecule for QscR. Thus, QscR appears to be an integral component of the P. aeruginosa quorum-sensing circuitry. QscR uses the LasI-generated acyl-homoserine lactone signal and controls a specific regulon that overlaps with the already overlapping LasR- and RhlR-dependent regulons.

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    • "As a result, as QscR dissociates from LasR and RhlR, and transcription-activating complexes LasR-3OC12- HSL and RhlR-C4-HSL are formed [58] [59]. This mode of action explains the reason why rhlAB operon is repressed by QscR during exponential phase [57] "
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    • "This hierarchy however is modulated by environmental conditions and growth substrates [13]. The las system is itself under the control of the local repressor gene rsaL [14] as well as peripheral regulators including Vfr [15], QscR [16], [17], VqsR [18], VqsM [19] and the small RNA binding protein RsmA [20]. "
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    ABSTRACT: In Pseudomonas aeruginosa, the production of many secreted virulence factors is controlled by a quorum-sensing (QS) circuit, constituted of transcriptional activators (LasR, RhlR, PqsR) and their cognate signaling molecules (3-oxo-C12-HSL, C4-HSL, PQS). QS is a cooperative behavior that is beneficial to a population but can be exploited by "QS-cheaters", individuals which do not respond to the QS-signal, but can use public goods produced by QS-cooperators. In order to identify QS-deficient clones we designed a genetic screening based on a lasB-lacZ fusion. We isolated one clone (PT1617) deficient in QS-dependent gene expression and virulence factor production despite wild type lasR, rhlR and pqsR alleles. Whole genome sequencing of PT1617 revealed a 3,552 bp deletion encompassing ORFs PA2228-PA2229-PA2230 and the pslA gene. However, complementation of PT1617 by plasmid-encoded copies of these ORFs, did not restore QS. Unexpectedly, gene expression levels of ORFs PA2228, PA2227 (vqsM) and PA2222, located adjacent to the deletion, were 10 to 100 fold higher in mutant PT1617 than in PAO1. When expressed from a constitutive promoter on a plasmid, PA2226, alone was found to be sufficient to confer a QS-negative phenotype on PAO1 as well as on PA14. Co-expression of PA2226 and PA2225 in PAO1 further prevented induction of the type III secretion system. In summary, we have identified a novel genetic locus including ORF2226 termed qsrO (QS-repressing ORF), capable of down-regulating all three known QS-systems in P. aeruginosa.
    PLoS ONE 02/2014; 9(2):e87814. DOI:10.1371/journal.pone.0087814 · 3.23 Impact Factor
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    • "In the latter case, they regulate target genes by " eaves-dropping " on exogenously provided AHL signals produced by neighboring bacteria (Ahmer, 2004). Two well studied such LuxR solos are QscR from P. aeruginosa which responds to endogenously produced AHLs (Chugani et al., 2001; Lequette et al., 2006) and SdiA of Salmonella enterica and Escherichia coli which eavesdrop on AHLs produced by neighboring bacteria (Ahmer et al., 1998; Michael et al., 2001; Ahmer, 2004; Yao et al., 2006). A sub-family of these LuxR solos only found in PAB have lost the capacity to bind AHLs and instead evolved the ability to respond to low-molecular weight plant compounds. "
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    ABSTRACT: A future challenge will be understanding the extensive communication that most likely takes place in bacterial interspecies and interkingdom signaling between plants and bacteria. A major bacterial inter-cellular signaling system in Gram-negative bacteria is LuxI/R quorum sensing (QS) based on the production (via the LuxI-family proteins) and detection (via the LuxR-family proteins) of N-acyl homoserine lactones (AHLs) signaling molecules. LuxR proteins which have the same modular structure of QS LuxRs but are devoid of a cognate LuxI AHL synthase are called solos. LuxR solos have been shown to be responsible to respond to exogenous AHLs produced by neighboring cells as well endogenously produced AHLs. It is now also evident that some LuxR proteins have evolved from the ability to binding AHLs and respond to other molecules/signals. For example, recent research has shown that a sub-family of LuxR solos responds to small molecules produced by plants. This indicates the presence of a uni-directional interkingdom signaling system occurring from plants to bacteria. In addition LuxR solos have now been also implicated to respond to endogenously produced signals which are not AHLs. In this Mini Review article we will discuss current trends and implications of the role of LuxR solos in bacterial responses to other signals using proteins related to AHL QS systems.
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