Skip to main content
SpringerLink
Log in

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

  • Published:
Plant and Soil Aims and scope Submit manuscript

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 rhiI 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 pRL1JI 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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

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

    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.

    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.

    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.

    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.

    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.

    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 fischeri luciferase. Biochemistry 20, 2444–2449.

    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.

    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.

    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.

    Google Scholar 

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

    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.

    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.

    Google Scholar 

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

    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 AWB 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.

    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.

    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.

    Google Scholar 

  • Johnston AW 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-lhomoserine lactone autoinducers of luminescence in the marine symbiotic bacterium Vibrio fischeri. J. Bacteriol. 176, 7558–7565.

    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. 186, 449–452.

    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.

    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).

  • McClean K H, Winson MK, 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.

    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.

    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.

    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.

    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.

    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.

    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.

    Google Scholar 

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

    Google Scholar 

  • Schlaman H R M, Phillips D A and Kondorosi E 1998 Genetic organization and transcriptional regulation of rhizobial nodulation genes. InThe 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.

    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-l-homoserine lactone molecules, known as autoinducers and as quorum sensing co-transcription factors. J. Bacteriol. 178, 366–371.

    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.

    Google Scholar 

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

    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.

    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.

    Google Scholar 

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

  • Williams P, Baldwin T J and Downie J A 1999 Bacterial crosstalk — communication between bacteria, plant and animal cells. In Society for GeneralMicrobiology 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.

    Google Scholar 

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

    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.

    Google Scholar 

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

    Google Scholar 

Download references

Author information

Author notes

  1. J.K. Lithgow

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

Authors and Affiliations

  1. John Innes Centre, Colney Lane, Norwich, NR4 7UH, UK

    J.K. Lithgow, V. E. Danino, J. Jones & J.A. Downie

Authors
  1. J.K. Lithgow
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. E. Danino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J.A. Downie
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lithgow, J., Danino, V.E., Jones, J. et al. Analysis of N-acyl homoserine-lactone quorum-sensing molecules made by different strains and biovars of Rhizobium leguminosarum containing different symbiotic plasmids. Plant and Soil 232, 3–12 (2001). https://doi.org/10.1023/A:1010333716277

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1010333716277

Search

Navigation