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Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones

¹ Department of Applied Biochemistry and Food Science, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, UK
² Department of Pharmaceutical Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
³ MRC Toxicology Unit, University of Leicester, Leicester LE1 9HN, UK

Author for correspondence: Paul Williams. Tel: + 44 115 951 5047. Fax: +44 115 951 5110. e-mail: Paul.Williams@nottingham.ac.uk

ABSTRACT

Quorum sensing relies upon the interaction of a diffusible signal molecule with a transcriptional activator protein to couple gene expression with cell population density. In Gram-negative bacteria, such signal molecules are usually N-acylhomoserine lactones (AHLs) which differ in the structure of their N-acyl side chains. Chromobacterium violaceum, a Gram-negative bacterium commonly found in soil and water, produces the characteristic purple pigmen violacein. Previously the authors described a violacein-negative, mini-Tn5 mutant of C. violaceum (CV026) in which pigment production can be restored by incubation with supernatants from the wild-type strain. To develop this mutant as a general biosensor for AHLs, the natural C. violaceum AHL molecule was first chemically characterized. By using solvent extraction, HPLC and mass spectrometry, a single AHL, N-hexanoyl-L-homoserine lactone (HHL), was identified in wild-type C. violaceum culture supernatants which was absent from CV026. Since the production of violacein constitutes a simple assay for the detection of AHLs, we explored the ability of CV026 to respond to a series of synthetic AHL and N-acylhomocysteine thiolactone (AHT) analogues. In CV026, violacein is inducible by ail the AHL and AHT compounds evaluated with N-acyl side chains from C₄ to C₈ in length, with varying degrees of sensitivity. Although AHL compounds with N-acyl side chains from C₁₀ to C₁₄ are unable to induce violacein production, if an activating AHL (e.g. HHL) is incorporated into the agar, these long-chain AHLs can be detected by their ability to inhibit violacein production. The versatility of CV026 in facilitating detection of AHL mixtures extracted from culture supernatants and separated by thin-layer chromatography is also demonstrated. These simple bioassays employing CV026 thus greatly extend the ability to detect a wide spectrum of AHL signa molecules.

Present address: Institute of Biological Sciences, University of Wales, Aberystwyth, Ceredigion SY23 3DA, UK.

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				V. Denervaud, P. TuQuoc, D. Blanc, S. Favre-Bonte, V. Krishnapillai, C. Reimmann, D. Haas, and C. van Delden Characterization of Cell-to-Cell Signaling-Deficient Pseudomonas aeruginosa Strains Colonizing Intubated Patients J. Clin. Microbiol., February 1, 2004; 42(2): 554 - 562. [Abstract] [Full Text] [PDF]

				M. Teplitski, H. Chen, S. Rajamani, M. Gao, M. Merighi, R. T. Sayre, J. B. Robinson, B. G. Rolfe, and W. D. Bauer Chlamydomonas reinhardtii Secretes Compounds That Mimic Bacterial Signals and Interfere with Quorum Sensing Regulation in Bacteria Plant Physiology, January 1, 2004; 134(1): 137 - 146. [Abstract] [Full Text] [PDF]

				J. Zhu, Y. Chai, Z. Zhong, S. Li, and S. C. Winans Agrobacterium Bioassay Strain for Ultrasensitive Detection of N-Acylhomoserine Lactone-Type Quorum-Sensing Molecules: Detection of Autoinducers in Mesorhizobium huakuii Appl. Envir. Microbiol., November 1, 2003; 69(11): 6949 - 6953. [Abstract] [Full Text] [PDF]

				Z.-Q. Luo, S. Su, and S. K. Farrand In Situ Activation of the Quorum-Sensing Transcription Factor TraR by Cognate and Noncognate Acyl-Homoserine Lactone Ligands: Kinetics and Consequences J. Bacteriol., October 1, 2003; 185(19): 5665 - 5672. [Abstract] [Full Text] [PDF]

				Brazilian National Genome Project Consortium:, A. T. Ribeiro de Vasconcelos, D. F. de Almeida, M. Hungria, C. T. Guimaraes, R. V. Antonio, F. C. Almeida, L. G. P. de Almeida, R. de Almeida, J. A. Alves-Gomes, et al. The complete genome sequence of Chromobacterium violaceum reveals remarkable and exploitable bacterial adaptability PNAS, September 30, 2003; 100(20): 11660 - 11665. [Abstract] [Full Text] [PDF]

				A. Carlier, S. Uroz, B. Smadja, R. Fray, X. Latour, Y. Dessaux, and D. Faure The Ti Plasmid of Agrobacterium tumefaciens Harbors an attM-Paralogous Gene, aiiB, Also Encoding N-Acyl Homoserine Lactonase Activity Appl. Envir. Microbiol., August 1, 2003; 69(8): 4989 - 4993. [Abstract] [Full Text] [PDF]

				S. Uroz, C. D'Angelo-Picard, A. Carlier, M. Elasri, C. Sicot, A. Petit, P. Oger, D. Faure, and Y. Dessaux Novel bacteria degrading N-acylhomoserine lactones and their use as quenchers of quorum-sensing-regulated functions of plant-pathogenic bacteria Microbiology, August 1, 2003; 149(8): 1981 - 1989. [Abstract] [Full Text] [PDF]

				Z.-Q. Luo, A. J. Smyth, P. Gao, Y. Qin, and S. K. Farrand Mutational Analysis of TraR. CORRELATING FUNCTION WITH MOLECULAR STRUCTURE OF A QUORUM-SENSING TRANSCRIPTIONAL ACTIVATOR J. Biol. Chem., April 4, 2003; 278(15): 13173 - 13182. [Abstract] [Full Text] [PDF]

				K. Heurlier, V. Denervaud, G. Pessi, C. Reimmann, and D. Haas Negative Control of Quorum Sensing by RpoN ({sigma}54) in Pseudomonas aeruginosa PAO1 J. Bacteriol., April 1, 2003; 185(7): 2227 - 2235. [Abstract] [Full Text] [PDF]

				C. Aguilar, I. Bertani, and V. Venturi Quorum-Sensing System and Stationary-Phase Sigma Factor (rpoS) of the Onion Pathogen Burkholderia cepacia Genomovar I Type Strain, ATCC 25416 Appl. Envir. Microbiol., March 1, 2003; 69(3): 1739 - 1747. [Abstract] [Full Text] [PDF]

				X. He, W. Chang, D. L. Pierce, L. O. Seib, J. Wagner, and C. Fuqua Quorum Sensing in Rhizobium sp. Strain NGR234 Regulates Conjugal Transfer (tra) Gene Expression and Influences Growth Rate J. Bacteriol., February 1, 2003; 185(3): 809 - 822. [Abstract] [Full Text] [PDF]

				A. B. Christensen, K. Riedel, L. Eberl, L. R. Flodgaard, S. Molin, L. Gram, and M. Givskov Quorum-sensing-directed protein expression in Serratia proteamaculans B5a Microbiology, February 1, 2003; 149(2): 471 - 483. [Abstract] [Full Text] [PDF]

				H. ZHU, S. J. THURUTHYIL, and M. D. P. WILLCOX Determination of quorum-sensing signal molecules and virulence factors of Pseudomonas aeruginosa isolates from contact lens-induced microbial keratitis J. Med. Microbiol., December 1, 2002; 51(12): 1063 - 1070. [Abstract] [Full Text] [PDF]

				E. A. Yates, B. Philipp, C. Buckley, S. Atkinson, S. R. Chhabra, R. E. Sockett, M. Goldner, Y. Dessaux, M. Camara, H. Smith, et al. N-Acylhomoserine Lactones Undergo Lactonolysis in a pH-, Temperature-, and Acyl Chain Length-Dependent Manner during Growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa Infect. Immun., October 1, 2002; 70(10): 5635 - 5646. [Abstract] [Full Text] [PDF]

				B. J. Pellock, M. Teplitski, R. P. Boinay, W. D. Bauer, and G. C. Walker A LuxR Homolog Controls Production of Symbiotically Active Extracellular Polysaccharide II by Sinorhizobium meliloti J. Bacteriol., September 15, 2002; 184(18): 5067 - 5076. [Abstract] [Full Text] [PDF]

				A. Wilkinson, V. Danino, F. Wisniewski-Dye, J. K. Lithgow, and J. A. Downie N-Acyl-Homoserine Lactone Inhibition of Rhizobial Growth Is Mediated by Two Quorum-Sensing Genes That Regulate Plasmid Transfer J. Bacteriol., August 15, 2002; 184(16): 4510 - 4519. [Abstract] [Full Text] [PDF]

				L. Gram, H.-P. Grossart, A. Schlingloff, and T. Kiorboe Possible Quorum Sensing in Marine Snow Bacteria: Production of Acylated Homoserine Lactones by Roseobacter Strains Isolated from Marine Snow Appl. Envir. Microbiol., August 1, 2002; 68(8): 4111 - 4116. [Abstract] [Full Text] [PDF]

				S. Aendekerk, B. Ghysels, P. Cornelis, and C. Baysse Characterization of a new efflux pump, MexGHI-OpmD, from Pseudomonas aeruginosa that confers resistance to vanadium Microbiology, August 1, 2002; 148(8): 2371 - 2381. [Abstract] [Full Text] [PDF]

				B. Taminiau, M. Daykin, S. Swift, M.-L. Boschiroli, A. Tibor, P. Lestrate, X. De Bolle, D. O'Callaghan, P. Williams, and J.-J. Letesson Identification of a Quorum-Sensing Signal Molecule in the Facultative Intracellular Pathogen Brucella melitensis Infect. Immun., June 1, 2002; 70(6): 3004 - 3011. [Abstract] [Full Text] [PDF]

				C. Reimmann, N. Ginet, L. Michel, C. Keel, P. Michaux, V. Krishnapillai, M. Zala, K. Heurlier, K. Triandafillu, H. Harms, et al. Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1 Microbiology, April 1, 2002; 148(4): 923 - 932. [Abstract] [Full Text] [PDF]

				M. Manefield, T. B. Rasmussen, M. Henzter, J. B. Andersen, P. Steinberg, S. Kjelleberg, and M. Givskov Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover Microbiology, April 1, 2002; 148(4): 1119 - 1127. [Abstract] [Full Text] [PDF]

				F. Wisniewski-Dye, J. Jones, S. R. Chhabra, and J. A. Downie raiIR Genes Are Part of a Quorum-Sensing Network Controlled by cinI and cinR in Rhizobium leguminosarum J. Bacteriol., March 15, 2002; 184(6): 1597 - 1606. [Abstract] [Full Text] [PDF]

				A. Croxatto, V. J. Chalker, J. Lauritz, J. Jass, A. Hardman, P. Williams, M. Camara, and D. L. Milton VanT, a Homologue of Vibrio harveyi LuxR, Regulates Serine, Metalloprotease, Pigment, and Biofilm Production in Vibrio anguillarum J. Bacteriol., March 15, 2002; 184(6): 1617 - 1629. [Abstract] [Full Text] [PDF]

				N. A. Burgess, D. F. Kirke, P. Williams, K. Winzer, K. R. Hardie, N. L. Meyers, J. Aduse-Opoku, M. A. Curtis, and M. Camara LuxS-dependent quorum sensing in Porphyromonas gingivalis modulates protease and haemagglutinin activities but is not essential for virulence Microbiology, March 1, 2002; 148(3): 763 - 772. [Abstract] [Full Text] [PDF]

				R. G. FRAY Altering Plant-Microbe Interaction Through Artificially Manipulating Bacterial Quorum Sensing Ann. Bot., March 1, 2002; 89(3): 245 - 253. [Abstract] [Full Text] [PDF]

				S. Heeb, C. Blumer, and D. Haas Regulatory RNA as Mediator in GacA/RsmA-Dependent Global Control of Exoproduct Formation in Pseudomonas fluorescens CHA0 J. Bacteriol., February 15, 2002; 184(4): 1046 - 1056. [Abstract] [Full Text] [PDF]

				J. T. Byers, C. Lucas, G. P. C. Salmond, and M. Welch Nonenzymatic Turnover of an Erwinia carotovora Quorum-Sensing Signaling Molecule J. Bacteriol., February 15, 2002; 184(4): 1163 - 1171. [Abstract] [Full Text] [PDF]