This Article Full Text Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Wilkinson, A. Articles by Downie, J. A. Search for Related Content PubMed PubMed Citation Articles by Wilkinson, A. Articles by Downie, J. A.

N-Acyl-Homoserine Lactone Inhibition of Rhizobial Growth Is Mediated by Two Quorum-Sensing Genes That Regulate Plasmid Transfer

A. Wilkinson, V. Danino, F. Wisniewski-Dyé,^, J. K. Lithgow,^, and J. A. Downie^*

John Innes Centre, Norwich NR4 7UH, United Kingdom

Received 25 March 2002/ Accepted 31 May 2002

The growth of some strains of Rhizobium leguminosarum bv. viciae is inhibited by N-(3-hydroxy-7-cis tetradecenoyl)-L-homoserine lactone (3OH-C_14:1-HSL), which was previously known as the small bacteriocin before its characterization as an N-acyl homoserine lactone (AHL). Tn5-induced mutants of R. leguminosarum bv. viciae resistant to 3OH-C_14:1-HSL were isolated, and mutations in two genes were identified. These genes, bisR and triR, which both encode LuxR-type regulators required for plasmid transfer, were found downstream of an operon containing trb genes involved in the transfer of the symbiotic plasmid pRL1JI. The first gene in this operon is traI, which encodes an AHL synthase, and the trbBCDEJKLFGHI genes were found between traI and bisR. Mutations in bisR, triR, traI, or trbL blocked plasmid transfer. Using gene fusions, it was demonstrated that bisR regulates triR in response to the presence of 3OH-C_14:1-HSL. In turn, triR is then required for the induction of the traI-trb operon required for plasmid transfer. bisR also represses expression of cinI, which is chromosomally located and determines the level of production of 3OH-C_14:1-HSL. The cloned bisR and triR genes conferred 3OH-C_14:1-HSL sensitivity to strains of R. leguminosarum bv. viciae normally resistant to this AHL. Furthermore, bisR and triR made Agrobacterium tumefaciens sensitive to R. leguminosarum bv. viciae strains producing 3OH-C_14:1-HSL. Analysis of patterns of growth inhibition using mutant strains and synthetic AHLs revealed that maximal growth inhibition required, in addition to 3OH-C_14:1-HSL, the presence of other AHLs such as N-octanoyl-L-homoserine lactone and/or N-(3-oxo-octanoyl)-L-homoserine lactone. In an attempt to identify the causes of growth inhibition, a strain of R. leguminosarum bv. viciae carrying cloned bisR and triR was treated with an AHL extract containing 3OH-C_14:1-HSL. N-terminal sequencing of induced proteins revealed one with significant similarity to the protein translation factor Ef-Ts.

Present address: Laboratoire d'Ecologie Microbienne, UMR CNRS 5557, Université Claude Bernard Lyon I, Villeurbanne, France.

Present address: Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield S10 2TN, United Kingdom.

This article has been cited by other articles:

• McAnulla, C., Edwards, A., Sanchez-Contreras, M., Sawers, R. G., Downie, J. A. (2007). Quorum-sensing-regulated transcriptional initiation of plasmid transfer and replication genes in Rhizobium leguminosarum biovar viciae. Microbiology 153: 2074-2082 [Abstract] [Full Text]  
• Toyofuku, M., Nomura, N., Fujii, T., Takaya, N., Maseda, H., Sawada, I., Nakajima, T., Uchiyama, H. (2007). Quorum Sensing Regulates Denitrification in Pseudomonas aeruginosa PAO1. J. Bacteriol. 189: 4969-4972 [Abstract] [Full Text]  
• Perez-Mendoza, D., Lucas, M., Munoz, S., Herrera-Cervera, J. A., Olivares, J., de la Cruz, F., Sanjuan, J. (2006). The Relaxase of the Rhizobium etli Symbiotic Plasmid Shows nic Site cis-Acting Preference. J. Bacteriol. 188: 7488-7499 [Abstract] [Full Text]  
• Russo, D. M., Williams, A., Edwards, A., Posadas, D. M., Finnie, C., Dankert, M., Downie, J. A., Zorreguieta, A. (2006). Proteins Exported via the PrsD-PrsE Type I Secretion System and the Acidic Exopolysaccharide Are Involved in Biofilm Formation by Rhizobium leguminosarum.. J. Bacteriol. 188: 4474-4486 [Abstract] [Full Text]  
• Zheng, H., Zhong, Z., Lai, X., Chen, W.-X., Li, S., Zhu, J. (2006). A LuxR/LuxI-Type Quorum-Sensing System in a Plant Bacterium, Mesorhizobium tianshanense, Controls Symbiotic Nodulation.. J. Bacteriol. 188: 1943-1949 [Abstract] [Full Text]  
• Perez-Mendoza, D., Sepulveda, E., Pando, V., Munoz, S., Nogales, J., Olivares, J., Soto, M. J., Herrera-Cervera, J. A., Romero, D., Brom, S., Sanjuan, J. (2005). Identification of the rctA Gene, Which Is Required for Repression of Conjugative Transfer of Rhizobial Symbiotic Megaplasmids. J. Bacteriol. 187: 7341-7350 [Abstract] [Full Text]  
• Brom, S., Girard, L., Tun-Garrido, C., Garcia-de los Santos, A., Bustos, P., Gonzalez, V., Romero, D. (2004). Transfer of the Symbiotic Plasmid of Rhizobium etli CFN42 Requires Cointegration with p42a, Which May Be Mediated by Site-Specific Recombination. J. Bacteriol. 186: 7538-7548 [Abstract] [Full Text]  
• Ulrich, R. L. (2004). Quorum Quenching: Enzymatic Disruption of N-Acylhomoserine Lactone-Mediated Bacterial Communication in Burkholderia thailandensis. Appl. Environ. Microbiol. 70: 6173-6180 [Abstract] [Full Text]  
• Muryoi, N., Sato, M., Kaneko, S., Kawahara, H., Obata, H., Yaish, M. W. F., Griffith, M., Glick, B. R. (2004). Cloning and Expression of afpA, a Gene Encoding an Antifreeze Protein from the Arctic Plant Growth-Promoting Rhizobacterium Pseudomonas putida GR12-2. J. Bacteriol. 186: 5661-5671 [Abstract] [Full Text]  
• Hoang, H. H., Becker, A., Gonzalez, J. E. (2004). The LuxR Homolog ExpR, in Combination with the Sin Quorum Sensing System, Plays a Central Role in Sinorhizobium meliloti Gene Expression. J. Bacteriol. 186: 5460-5472 [Abstract] [Full Text]  
• Gonzalez, J. E., Marketon, M. M. (2003). Quorum Sensing in Nitrogen-Fixing Rhizobia. Microbiol. Mol. Biol. Rev. 67: 574-592 [Abstract] [Full Text]  
• Chen, H., Teplitski, M., Robinson, J. B., Rolfe, B. G., Bauer, W. D. (2003). Proteomic Analysis of Wild-Type Sinorhizobium meliloti Responses to N-Acyl Homoserine Lactone Quorum-Sensing Signals and the Transition to Stationary Phase. J. Bacteriol. 185: 5029-5036 [Abstract] [Full Text]  
• Tun-Garrido, C., Bustos, P., Gonzalez, V., Brom, S. (2003). Conjugative Transfer of p42a from Rhizobium etli CFN42, Which Is Required for Mobilization of the Symbiotic Plasmid, Is Regulated by Quorum Sensing. J. Bacteriol. 185: 1681-1692 [Abstract] [Full Text]  
• He, X., Chang, W., Pierce, D. L., Seib, L. O., Wagner, J., Fuqua, C. (2003). Quorum Sensing in Rhizobium sp. Strain NGR234 Regulates Conjugal Transfer (tra) Gene Expression and Influences Growth Rate. J. Bacteriol. 185: 809-822 [Abstract] [Full Text]