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Journal of Bacteriology, June 1999, p. 3816-3823, Vol. 181, No. 12
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Analysis of Quorum-Sensing-Dependent Control of Rhizosphere-Expressed (rhi) Genes in Rhizobium leguminosarum bv. viciae

Belen Rodelas,^1, James K. Lithgow,¹ Florence Wisniewski-Dye,¹ Andrea Hardman,² Adam Wilkinson,^1, Anastassios Economou,^1,§ Paul Williams,² and J. Allan Downie^1,*

John Innes Centre, Colney, Norwich NR4 7UH,¹ and School of Pharmaceutical Sciences, University of Nottingham, Nottingham, NG7 2RD,² United Kingdom

Received 26 January 1999/Accepted 16 April 1999

The rhi genes of Rhizobium leguminosarum biovar viciae are expressed in the rhizosphere and play a role in the interaction with legumes, such as the pea. Previously (K. M. Gray, J. P. Pearson, J. A. Downie, B. E. A. Boboye, and E. P. Greenberg, J. Bacteriol. 178:372-376, 1996) the rhiABC operon had been shown to be regulated by RhiR and to be induced by added N-(3-hydroxy-7-cis-tetradecenoyl)-L-homoserine lactone (3OH,C_14:1-HSL). Mutagenesis of a cosmid carrying the rhiABC and rhiR gene region identified a gene (rhiI) that affects the level of rhiA expression. Mutation of rhiI slightly increased the number of nodules formed on the pea. The rhiI gene is (like rhiA) regulated by rhiR in a cell density-dependent manner. RhiI is similar to LuxI and other proteins involved in the synthesis of N-acyl-homoserine lactones (AHLs). Chemical analyses of spent culture supernatants demonstrated that RhiI produces N-(hexanoyl)-L-homoserine lactone (C₆-HSL) and N-(octanoyl)-L-homoserine lactone (C₈-HSL). Both of these AHLs induced rhiA-lacZ and rhiI-lacZ expression on plasmids introduced into an Agrobacterium strain that produces no AHLs, showing that rhiI is positively regulated by autoinduction. However, in this system no induction of rhiA or rhiI with 3OH,C_14:1-HSL was observed. Analysis of the spent culture supernatant of the wild-type R. leguminosarum bv. viciae revealed that at least seven different AHLs are made. Mutation of rhiI decreased the amounts of C₆-HSL and C₈-HSL but did not block their formation, and in this background the rhiI mutation did not significantly affect the expression levels of the rhiI gene or rhiABC genes or the accumulation of RhiA protein. These observations suggest that there are additional loci involved in AHL production in R. leguminosarum bv. viciae and that they affect rhiI and rhiABC expression. We postulate that the previously observed induction of rhiA by 3OH,C_14:1-HSL may be due to an indirect effect caused by induction of other AHL production loci.

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^* Corresponding author. Mailing address: John Innes Centre, Colney Lane, Norwich NR4 7UH, United Kingdom. Phone: 1603 452571. Fax: 1603 456844. E-mail: downie{at}bbsrc.ac.uk.

Present address: Departmento de Microbiologia, Facultad de Farmacia, Universidad de Granada, 18071 Granada, Spain.

Present address: MRC Laboratory of Molecular Biology, Cambridge CBQ 2H, United Kingdom.

^§ Present address: IMBB-Forth and Department of Biology, University of Crete, P.O. Box 1527, 711 10 Iraklio-Crete, Greece.

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Journal of Bacteriology, June 1999, p. 3816-3823, Vol. 181, No. 12
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

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