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Analysis of N-acyl homoserine-lactone quorum-sensing molecules made by different strains and biovars of Rhizobium leguminosarum containing different symbiotic plasmids

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Interactions in the Root Environment: An Integrated Approach

Part of the book series: Developments in Plant and Soil Sciences ((DPSS,volume 96))

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Abstract

Strains of Rhizobium leguminosarum use a cell density-dependent gene regulatory system to assess their population density. This is achieved by the accumulation of N-acyl-homoserine lactones (AHLs) in the environment during growth of the bacteria and these AHLs stimulate the induction of various bacterial genes that are up-regulated in the late-exponential and stationary phases of growth. A genetically well-characterised strain of R. leguminosarum biovar viciae was found to have four genes, whose products synthesise different AHLs. We have analysed AHL production by four genetically distinct isolates of R. leguminosarum, three of bv. viciae and one of bv. phaseoli. Distinct differences were seen in the pattern of AHLs produced by the bv. viciae strains compared with bv. phaseoli and the increased levels and diversity of AHLs found in bv. viciae strains can be attributed to the rhil gene, which is located on the symbiotic (Sym) plasmid and is up-regulated when the bacteria are grown in the rhizosphere. Additional complexity to the profile of AHLs is found to be associated with highly transmissible plasmid pRL1 J1 of R. leguminosarum bv. viciae, but this is not observed with some other strains, including those carrying different transmissible plasmids. In addition to AHLs produced by the products of genes on the symbiotic plasmid, there is clear evidence for the presence of other AHL production loci. Expression levels and patterns of AHLs can change markedly in different growth media. These results indicate that there is a network of quorum-sensing loci in different strains of R. leguminosarum and these loci may play a role in adapting to rhizosphere growth and plasmid transfer.

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References

  • Beringer J E 1974 R factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84, 188–198.

    Article  CAS  PubMed  Google Scholar 

  • Brewin N J, Beringer J E, Buchanan-Wollaston A V, Johnston A W B and Hirsch P R 1980 Transfer of symbiotic genes with bacteriocinogenic plasmids in Rhizobium leguminosarum. J. Gen. Microbiol. 116, 261–270.

    CAS  Google Scholar 

  • Brewin N J, Wood E A, Johnston A W B, Dibb N J, and Hombrecher G 1982 Recombinant nodulation plasmids in Rhizobium leguminosarum. J. Gen. Microbiol. 128, 1817–1827.

    Google Scholar 

  • Cha C, Gao P, Chen Y C, Shaw P D and Farrand S K 1998 Production of acyl-homoserine lactone quorum-sensing signals by gram-negative plant-associated bacteria. Mol. Plant-Microbe Interact. 11, 1119–1129.

    Article  CAS  PubMed  Google Scholar 

  • Cubo M T, Economou A, Murphy G, Johnston A W B and Downie J A 1992 Molecular characterisation and regulation of the rhizosphere-expressed genes rhiABCR that can influence nodulation by Rhizobium leguminosarum biovar viciae. J. Bacteriol. 174, 4026–4035.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Downie J A 1998 Functions of rhizobial nodulation genes. In The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. Eds H P Spaink, A Kondorosi and P J J Hooykaas. pp 387–402. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Chapter  Google Scholar 

  • Downie J A, Knight C D, Johnston A W B and Rossen L 1985 Identification of genes and gene products involved in the nodulation of peas by Rhizobium leguminosarum. Mol. Gen. Genet. 198, 225–262.

    Article  Google Scholar 

  • Eberhard A, Burlingame A L, Eberhard C, Kenyon G L, Nealson K H and Oppenheimer N J 1981 Structural identification of autoinducer of Photobacterium fischen luciferase. Biochemistry 20, 2444–2449.

    Article  CAS  PubMed  Google Scholar 

  • Farrand S K 1993 Conjugal transfer of Agrobacterium plasmids. In Bacterial Conjugation. Ed D B Clewell. pp 255–291. Plenum Press, NY, USA.

    Chapter  Google Scholar 

  • Freiberg C, Fellay R, Bairoch A, Broughton W J, Rosenthal A and Perret X 1997 Molecular basis of symbiosis between Rhizobium and legumes. Nature 387, 394–401.

    Article  CAS  PubMed  Google Scholar 

  • Fuqua C and Winans S C 1994 A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumour metabolite. J. Bacteriol. 176, 2796–2806.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fuqua C, Winans S C and Greenberg E P 1996 Census and consensus in bacterial ecosystems: the luxR-LuxI family of quorum-sensing transcriptional regulators. Annu. Rev. Microbiol. 50, 727–751.

    Article  CAS  PubMed  Google Scholar 

  • Gambello MJ, Kaye S and Iglewski BH 1993 LasR of Pseudomonas aeruginosa is a transcriptional activator of the alkaline protease gene (Apr) And an enhancer of exotoxin-A expression. Infection and Immunity 61, 1180–1184.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gray K M, Pearson J P, Downie J A, Boboye B E A, Greenberg E P 1996 Cell-to-cell signalling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of a stationary phase and rhizosphere-expressed genes. J. Bacteriol. 178, 372–376.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hirsch P R 1979 Plasmid-determined bacteriocin production by Rhizobium leguminosarum. J. Gen. Microbiol. 113, 219–228.

    Article  CAS  Google Scholar 

  • Hirsch P R, Van Montagu M, Johnston A W B, Brewin N J and Schell J 1980 Physical identification of bacteriocinogenic, nodulation plasmids in strains of Rhizobium leguminosarum. J. Gen. Microbiol. 120, 403–412.

    Google Scholar 

  • Hombrecher G, Götz R, Dibb N J, Downie J A, Johnston A W B and Brewin N J 1984 Cloning and mutagenesis of nodulation genes from Rhizobium leguminosarum TOM, a strain with extended host range. Mol. Gen. Genet 184, 293–298.

    Article  Google Scholar 

  • Hynes M F and Finan T M 1998 General genetic knowledge. In The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. Eds H P Spaink, A Kondorosi and P J J Hooykaas. pp 25–43. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Chapter  Google Scholar 

  • Johnston A W B, Beynon J L, Buchanan-Wollaston A V, Setchell S M, Hirsch P and Beringer J E 1978 High frequency transfer of nodulating ability between strains and species of Rhizobium. Nature 276, 634–636.

    Article  Google Scholar 

  • Johnston A W B, Hombrecher G, Brewin N J and Cooper N C 1982 Two transmissible plasmids in Rhizobium leguminosarum strain 300. J. Gen. Microbiol. 128, 85–93.

    Google Scholar 

  • Kuo A, Blough N V and Dunlap P V 1994 Multiple N-acyl-l-homoserine lactone autoinducers of luminescence in the marine symbiotic bacterium Vibrio fischen. J. Bacteriol. 176, 7558–7565.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lamb J W, Hombrecher G and Johnston A W B 1982 Plasmid-determined nodulation and nitrogen-fixation abilities in Rhizobium phaseoli. Mol. Gen. Genet. 186186, 449—52.

    Article  Google Scholar 

  • Latifi A, Foglino M, Tananka K, Williams P and Lazdunski A 1996 A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhlR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol. Microbiol. 21, 1137–1146.

    Article  CAS  PubMed  Google Scholar 

  • Lithgow J K, Wilkinson A, Hardman A, Rodelas B, Wisniewski-Dyé F, Williams P and Downie J A 2000 The regulatory locus cinRI in Rhizobium leguminosarum controls a network of quorum sensing loci. Mol. Microbiol. (in press).

    Google Scholar 

  • McClean K H, Winson M K, Fish L, Taylor A, Chhabra S R, Camara M, Daykin M, Lamb J H, Swift S, Bycroft B W, Stewart G S A B and Williams P 1997 Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology-UK 143, 3703–3711.

    Article  CAS  Google Scholar 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pesci E C, Pearson J P, Seed P C and Iglewski B H 1997 Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 179, 3127–3132.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Piper K R, Beck von Bodman S and Farrand S K 1993 Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 362, 448–450.

    Article  CAS  PubMed  Google Scholar 

  • Piper K R, Beck von Bodman S, Hwang I and Farrand S K 1999 Hierarchical gene regulatory systems arising from fortuitous gene associations: controlling quorum sensing by the opine regulon in Agrobacterium. Mol. Microbiol. 32, 1077–1089.

    Article  CAS  PubMed  Google Scholar 

  • Priem W J E and Wijffelman C A 1984 Selection of strains cured of the Rhizobium leguminosarum Sym plasmid pRL1JI by using small bacteriocin. FEMS Lett. 25, 247–251.

    Article  CAS  Google Scholar 

  • Rodelas B, Lithgow J K, Wisniewski-Dye F, Hardman A, Wilkinson A, Economou A, Williams P and Downie J A 1999 Analysis of quorum-sensing-dependent control of rhizosphere-expressed (rhi) genes in Rhizobium leguminosarum bv. viciae. J. Bacteriol. 181, 3816–3823.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rosemeyer V, Michels J, Verreth C and Vanderleyden J 1998 luxI-and luxR-homologous genes of Rhizobium etli CNPAF512 contribute to synthesis of autoinducer molecules and nodulation of Phaseolus vulgaris. J. Bacteriol. 180, 815–821.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schlaman H R M, Phillips D A and Kondorosi E 1998 Genetic organization and transcriptional regulation of rhizobial nodulation genes. In The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. Eds H P Spaink, A Kondorosi and P J J Hooykaas. pp 361–386. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Chapter  Google Scholar 

  • Schripsema J, de Rudder K E E, van Vliet T B, Lankhorst P P, de Vroom E, Kijne J W and Van Brussel A A N 1996 Bacteriocin small of Rhizobiom leguminosarum belongs to the class of N-acyl-1-homoserine lactone molecules, known as autoinducers and as quorum sensing co-transcription factors. J. Bacteriol. 178, 366–371.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Swift S, Throup J P, Williams P, Salmond G P C and Stewart G S A B 1996 Quorum sensing: A population-density component in the determination of bacterial phenotype. Trends Biochem. Sci. 21, 214–219.

    Article  CAS  PubMed  Google Scholar 

  • Thorne S H and Williams H D 1999 Cell density-dependent starvation survival of Rhizobium leguminosarum bv phaseoli: Identification of the role of an N-acyl homoserine lactone in adaptation to stationary-phase survival. J. Bacteriol. 181, 981–990.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wijffelman C A, Pees E, Van Brussel A A N and Hooykaas P J J 1983 Repression of small bacteriocin excretion in Rhizobium leguminosarum and Rhizobium trifolii by transmissible plasmids. Mol. Gen. Genet. 192, 171–176.

    Article  CAS  Google Scholar 

  • Wijffelman C A, Pees E, Van Brussel A A N, Okker R J H and Lugtenberg B J J 1985 Genetic and functional analysis of the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Arch. Microbiol. 143, 225–232.

    Article  CAS  Google Scholar 

  • Wilkinson A 1998 Acyl-homoserine lactone signalling in Rhizobium leguminosarum. Ph.D. Thesis, University of East Anglia.

    Google Scholar 

  • Williams P, Baldwin T J and Downie J A 1999 Bacterial crosstalk — communication between bacteria, plant and animal cells. In Society for General Microbiology Symposium 57: Microbial signalling and communication. Eds R R England, G Hobbs, N J Bainton and D McL Roberts, pp 1–35. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Winarno R and Lie T A 1979 Competition between Rhizobium strains in nodule formation: interactions between nodulating and non-nodulating strains. Plant Soil 51, 135–142.

    Article  Google Scholar 

  • Winson M K, Camra M, Latifi A, Foglino M, Chhabra S R, Daykin M, Bally M, Chapon V, Salmnd G P C, Bycroft B W, Lazdunski A, Stewart G S A B and Williams P 1995 Multiple N-acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92, 9427–9431.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Young J P W 1985 Rhizobium population genetics: enzyme polymorphism in isolates from peas, clover, beans and lucerne grown at the same site. J. Gen. Microbiol. 131, 2399–2408. Zhang L and Kerr A 1991 A diffusible compound can enhance conjugal transfer of the Ti plasmid in Agrobacterium tumefaciens. J. Bacteriol. 173, 1867-1872.

    CAS  Google Scholar 

  • Zhang L, Murphy P J, Kerr A and Tate M E 1993 Agrobacterium conjugation and gene regulation by N-acyl-1-homoserine lactones. Nature 362, 446–448.

    Article  CAS  PubMed  Google Scholar 

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David S. Powlson Geoff L. Bateman Keith G. Davies John L. Gaunt Penny R. Hirsch

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Lithgow, J.K., Danino, V.E., Jones, J., Downie, J.A. (2002). Analysis of N-acyl homoserine-lactone quorum-sensing molecules made by different strains and biovars of Rhizobium leguminosarum containing different symbiotic plasmids. In: Powlson, D.S., Bateman, G.L., Davies, K.G., Gaunt, J.L., Hirsch, P.R. (eds) Interactions in the Root Environment: An Integrated Approach. Developments in Plant and Soil Sciences, vol 96. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-0566-1_1

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  • DOI: https://doi.org/10.1007/978-94-010-0566-1_1

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  • Print ISBN: 978-94-010-3925-3

  • Online ISBN: 978-94-010-0566-1

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