Abstract
The QS machinery of Pseudomonas aeruginosa, an opportunistic human pathogen, consists of three acyl-homoserine lactone (acyl-HSL) signaling systems, LasR-I, RhlR-I, and QscR. QscR, known as an orphan receptor and a repressor of other QS systems, operates its own regulon using N-3-oxododecanoyl HSL (3OC12), which is synthesized by LasI, as its signal. In this study, we addressed the role of QscR in interspecies communication. We found that QscR auto-activates its own transcription in the presence of 3OC12. In a single population of P. aeruginosa, where 3OC12 is the sole signal available for QscR, the QscR regulon is activated by 3OC12 produced by the LasI-R system. However, the broad signal specificity of QscR allowed it to respond to a non-P. aeruginosa signal, such as N-decanoyl HSL (C10) and N-3-hydroxydecanoyl HSL (3OHC10), which preferentially activated QscR to LasR. The signal extracts from Pseudomonas fluorescens and Burkholeria vietnamiensis also preferentially activated QscR. These non-P. aeruginosa signals activated QscR more strongly than 3OC12, the authentic P. aeruginosa signal. Since a variety of acyl-HSLs are produced in the multi-species habitat of nature, our study provides a clue for the particular situation that allows QscR to secede from the conventional QS cascade in mixed microbial community.
Similar content being viewed by others
References
Choi, Y., Park, H.Y., Park, S.J., Kim, S.K., Ha, C., Im, S.J., and Lee, J.H. (2011). Growth phase-differential quorum sensing regulation of anthranilate metabolism in Pseudomonas aeruginosa. Mol. Cells 32, 57–65.
Chugani, S.A., Whiteley, M., Lee, K.M., D’Argenio, D., Manoil, C., and Greenberg, E.P. (2001). QscR, a modulator of quorumsensing signal synthesis and virulence in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 98, 2752–2757.
Conway, B.A., and Greenberg, E.P. (2002). Quorum-sensing signals and quorum-sensing genes in Burkholderia vietnamiensis. J. Bacteriol. 184, 1187–1191.
Daniels, R., Vanderleyden, J., and Michiels, J. (2004). Quorum sensing and swarming migration in bacteria. FEMS Microbiol. Rev. 28, 261–289.
Farinha, M.A., and Kropinski, A.M. (1990). Construction of broadhost-range plasmid vectors for easy visible selection and analysis of promoters. J. Bacteriol. 172, 3496–3499.
Fuqua, C. (2006). The QscR quorum-sensing regulon of Pseudomonas aeruginosa: an orphan claims its identity. J. Bacteriol. 188, 3169–3171.
Fuqua, C., and Greenberg, E.P. (2002). Listening in on bacteria: acyl-homoserine lactone signalling. Nat. Rev. Mol. Cell. Biol. 3, 685–695.
Hentzer, M., Wu, H., Andersen, J.B., Riedel, K., Rasmussen, T.B., Bagge, N., Kumar, N., Schembri, M.A., Song, Z., Kristoffersen, P., et al. (2003). Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22, 3803–3815.
Khan, S.R., Mavrodi, D.V., Jog, G.J., Suga, H., Thomashow, L.S., and Farrand, S.K. (2005). Activation of the phz operon of Pseudomonas fluorescens 2–79 requires the LuxR homolog PhzR, N-(3-OH-Hexanoyl)-L-homoserine lactone produced by the LuxI homolog PhzI, and a cis-acting phz box. J. Bacteriol. 187, 6517–6527.
Ledgham, F., Ventre, I., Soscia, C., Foglino, M., Sturgis, J.N., and Lazdunski, A. (2003). Interactions of the quorum sensing regulator QscR: interaction with itself and the other regulators of Pseudomonas aeruginosa LasR and RhlR. Mol. Microbiol. 48, 199–210.
Lee, J.H., Lequette, Y., and Greenberg, E.P. (2006). Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol. Microbiol. 59, 602–609.
Lequette, Y., Lee, J.H., Ledgham, F., Lazdunski, A., and Greenberg, E.P. (2006). A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J. Bacteriol. 188, 3365–3370.
Mattiuzzo, M., Bertani, I., Ferluga, S., Cabrio, L., Bigirimana, J., Guarnaccia, C., Pongor, S., Maraite, H., and Venturi, V. (2011). The plant pathogen Pseudomonas fuscovaginae contains two conserved quorum sensing systems involved in virulence and negatively regulated by RsaL and the novel regulator RsaM. Environ. Microbiol. 13, 145–162.
Newman, J.R., and Fuqua, C. (1999). Broad-host-range expression vectors that carry the L-arabinose-inducible Escherichia coli araBAD promoter and the araC regulator. Gene 227, 197–203.
Oinuma, K., and Greenberg, E.P. (2011). Acyl-homoserine lactone binding to and stability of the orphan Pseudomonas aeruginosa quorum-sensing signal receptor QscR. J. Bacteriol. 193, 421–428.
Pearson, J.P., Passador, L., Iglewski, B.H., and Greenberg, E.P. (1995). A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92, 1490–1494.
Pearson, J.P., Pesci, E.C., and Iglewski, B.H. (1997). Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J. Bacteriol. 179, 5756–5767.
Sambrook, J.E., Fritsch, F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual (Cold Spring Harbor, N. Y., USA: Cold Spring Harbor Laboratory Press)
Schuster, M., and Greenberg, E.P. (2006). A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296, 73–81.
Schuster, M., and Greenberg, E.P. (2007). Early activation of quorum sensing in Pseudomonas aeruginosa reveals the architecture of a complex regulon. BMC Genomics 8, 287.
Schuster, M., Lostroh, C.P., Ogi, T., and Greenberg, E.P. (2003). Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185, 2066–2079.
Schuster, M., Urbanowski, M.L., and Greenberg, E.P. (2004). Promoter specificity in Pseudomonas aeruginosa quorum sensing revealed by DNA binding of purified LasR. Proc. Natl. Acad. Sci. USA 101, 15833–15839.
Smith, R.S., and Iglewski, B.H. (2003). P. aeruginosa quorumsensing systems and virulence. Curr. Opin. Microbiol. 6, 56–60.
Venturi, V. (2006). Regulation of quorum sensing in Pseudomonas. FEMS Microbiol. Rev. 30, 274–291.
Venturi, V., Friscina, A., Bertani, I., Devescovi, G., and Aguilar, C. (2004). Quorum sensing in the Burkholderia cepacia complex. Res. Microbiol. 155, 238–244.
Wagner, V.E., Bushnell, D., Passador, L., Brooks, A.I., and Iglewski, B.H. (2003). Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J. Bacteriol. 185, 2080–2095.
Wagner-Dobler, I., Thiel, V., Eberl, L., Allgaier, M., Bodor, A., Meyer, S., Ebner, S., Hennig, A., Pukall, R., and Schulz, S. (2005). Discovery of complex mixtures of novel long-chain quorum sensing signals in free-living and host-associated marine alphaproteobacteria. Chembiochem 6, 2195–2206.
Whiteley, M., and Greenberg, E.P. (2001). Promoter specificity elements in Pseudomonas aeruginosa quorum-sensing-controlled genes. J. Bacteriol. 183, 5529–5534.
Whiteley, M., Lee, K.M., and Greenberg, E.P. (1999). Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96, 13904–13909.
Author information
Authors and Affiliations
Corresponding author
Additional information
These authors contributed equally to this work.
About this article
Cite this article
Ha, C., Park, S.J., Im, SJ. et al. Interspecies signaling through QscR, a quorum receptor of Pseudomonas aeruginosa . Mol Cells 33, 53–59 (2012). https://doi.org/10.1007/s10059-012-2208-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10059-012-2208-2