Quorum-sensing in Rhizobium

Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology

Volumn 81, Issue 1-4, 2002, Pages 397-407

  Wisniewski Dyé, Florence ^a   Downie, J Allan ^b  

^a UNIVERSITÉ LYON 1   (France)

^b JOHN INNES CENTRE   (United Kingdom)

Author keywords

Autoinducer; Bacteriocin; Legumes; N acyl homoserine lactone; Nodulation; Quorum sensing; Rhizobium; Symbiosis

Indexed keywords

BACTERIAL PROTEIN; BACTERIOCIN; HOMOSERINE; LACTONE; LACTONE DERIVATIVE;

LEGUME; RHIZOBACTERIUM;

ARTICLE; AUTOREGULATION; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCUS; GROWTH INHIBITION; LEGUME; NODULATION; NONHUMAN; OPERON; PLASMID; PRIORITY JOURNAL; RHIZOBIUM LEGUMINOSARUM; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PROKARYOTA; RHIZOBIUM; RHIZOBIUM LEGUMINOSARUM;

EID: 0036419055     PISSN: 00036072     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1020501104051     Document Type: Article

References (77)

1. Andersen JB, Heydorn A, Hentzer M, Eberl L, Geisenberger O, Christensen BB, Molin S & Givskov M (2001) gfp-based N-acyl-homoserine-lactone sensor systems for detection of bacterial communication. Appl. Environ. Microbiol. 67: 575-585.
2. Bassler BL, Wright M, Showalter RE & Silverman MR (1993) Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol. Microbiol. 9: 773-786.
3. Bassler BL, Wright M & Silverman MR (1994) Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol. Microbiol. 13: 273-286.
4. Beck von Bodman S, Hayman GT & Farrand SK (1992) Opine catabolism and conjugal transfer of the nopaline Ti plasmid pTiC58 are coordinately regulated by a single repressor. Proc. Natl. Acad. Sci. USA 89: 643-647.
5. Brewin NJ, Beringer JE, Buchanan-Wollaston AV, Johnston AWB & Hirsch PR (1980) Transfer of symbiotic genes with bacteriocinogenic plasmids in Rhizobium leguminosarum. J. Gen. Microbiol. 116: 261-270.
6. Callahan SM & Dunlap PV (2000) LuxR- and acyl-homoserine-lactone-controlled non-lux genes define a quorum-sensing regulon in Vibrio fischeri. J. Bacteriol. 182: 2811-2822.
7. Cha C, Gao P, Chen Y-C, Shaw PD & Farrand SK (1998) Production of acyl-homoserine lactone quorum-sensing signals by Gram-negative plant-associated bacteria. Mol. Plant-Microbe Interact. 11: 1119-1129.
8. Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL & Hughson FM (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415: 545-549.
9. Cubo MT, Economou A, Murphy G, Johnston AWB & Downie JA (1992) Molecular characterization and regulation of the rhizosphere-expressed genes rhiABCR that can influence nodulation by Rhizobium leguminosarum biovar viciae. J. Bacteriol. 174: 4026-4035.
10. Daniels R, De Vos DE, Desair J, Raedschelders G, Luyten E, Rosemeyer V, Verreth C, Schoeters E, Vanderleyden J & Michiels J (2002) The cin quorum sensing locus of Rhizobium etli CNPAF512 affects growth and symbiotic nitrogen fixation. J. Biol. Chem. 277: 462-468.
11. Dibb NJ, Downie JA & Brewin NJ (1984) Identification of a rhizosphere protein encoded by the symbiotic plasmid of Rhizobium leguminosarum. J. Bacteriol. 158: 621-627.
12. Dong YH, Xu JL, Li XZ & Zhang LH (2000) AiiA, an enzyme that inactivates the acylhomoserinelactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. USA 97: 3526-3531.
13. Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF & Zhang LH (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411: 813-817.
14. Dong YH, Gusti AR, Zhang Q, Xu JL & Zhang LH (2002) Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl. Environ. Microbiol. 68: 1754-1759.
15. Eberhard A, Burlingame AL, Eberhard C, Keenyon GL, Nealson KH & Oppenheimer NJ (1981) Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20: 2444-2449.
16. Eberl L, Winson MK, Sternberg C, Stewart GS, Christiansen G, Chhabra SR, Bycroft B, Williams P, Molin S & Givskov M (1996) Involvement of N-acyl-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol. Microbiol. 20: 127-136.
17. Eberl L (1999) N-acyl homoserine lactone-mediated gene regulation in gram-negative bacteria. Syst. Appl. Microbiol. 22: 493-506.
18. Economou A, Hawkins FKL, Downie JA & Johnston AWB (1989) Transcription of rhiA, a gene on a Rhizobium leguminosarum bv. viciae Sym plasmid, requires rhiR and is repressed by flavonoids that induce nod genes. Mol. Microbiol. 3: 87-93.
19. Engebrecht J, Nealson K & Silverman M (1983) Bacterial luminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 32: 773-781.
20. Engebrecht J & Silverman M (1984) Identification of genes and gene products necessary for bacterial luminescence. Proc. Natl. Acad. Sci. USA 81: 4154-4158.
21. Flavier AB, Ganova-Raeva LM, Schell MA & Denny TP (1997) Hierarchical atoinduction in Ralstonia solanacearum: control of acyl-homoserine lactone production by a novel autoregulatory system responsive to 3-hydroxypalmitic acid methyl ester. J. Bacteriol. 179: 7089-7097.
22. Fray RG, Throup JP, Daykin M, Wallace A, Williams P, Stewart GSAB & Grieson D (1999) Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria. Nature Biotech. 17: 1017-1020.
23. Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosenthal A & Perret X (1997) Molecular basis of symbiosis between Rhizobium and legumes. Nature 387: 394-401.
24. Fuqua WC, Winans SC & Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176: 269-275.
25. Fuqua C & Greenberg EP (1998) Self perception in bacteria: quorum sensing with acylated homoserine lactones. Curr. Opin. Microbiol. 1: 183-189.
26. Gill RE & Cull MG (1986) Control of developmental gene expression by cell-to-cell interactions in Myxococcus xanthus. J Bacteriol. 168: 341-347.
27. Gilson L, Kuo A & Dunlap PV (1995) AinS and a new family of autoinducer synthesis proteins. J. Bacteriol. 177: 6946-6951.
28. Goel AK, Sindhu SS & Dadarwal KR (1999) Bacteriocin-producing native rhizobia of green gram (Vigna radiata) having competitive advantage in nodule occupancy. Microbiol. Res. 154: 43-48.
29. Gray KM, Pearson JP, Downie JA, Boboye BEA & Greenberg EP (1996) Cell-to-cell signaling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of a stationary phase and rhizosphere-expressed genes. J. Bacteriol. 178: 372-376.
30. Hirsch PR (1979) Plasmid-determined bacteriocin production by Rhizobium leguminosarum. J. Gen. Microbiol. 113: 219-228.
31. Hirsch PR, van Montagu M, Johnston AWB, Brewin NJ & Schell J (1980) Physical identification of bacteriocinogenic, nodulation plasmids in strains of Rhizobium leguminosarum. J. Gen. Microbiol. 120: 403-412.
32. Holden MTG, Chhabra SR, de Nys R, Stead P, Bainton NJ, Hill PJ, Manefield M, Kumar N, Labatte M, England D, Rice S, Givskov M, Salmond GPC, Stewart GSAB, Bycroft BW, Kjelleberg S & Williams P (1999) Quorum-sensing cross-talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other Gram-negative bacteria. Mol. Microbiol. 33: 1254-1266.
33. Horinouchi S & Beppu T (1990) Autoregulatory factors of secondary metabolism and morphogenesis in actinomycetes. Crit. Rev. Biotechnol. 10: 191-204.
34. Johnston AWB, Beynon JL, Buchanan-Wollaston AV, Stetchell SM, Hirsch P & Beringer JE (1978) High frequency transfer of nodulating ability between strains and species of Rhizobium. Nature 276: 634-636.
35. Hwang I, Li P-L, Zhang L, Piper KR, Cook DM, Tate ME & Farrand SK (1994) TraI, a LuxI homologue, is responsible for production of conjugation factor, the Ti plasmid N-acylhomoserine lactone autoinducer. Proc. Natl. Acad. Sci. USA 91: 4639-4643.
36. Laue RE, Jiang Y, Chhabra SR, Jacob S, Stewart GSAB, Hardman A, Downie JA, O'Gara F & Williams P (2000) The biocontrol strain Pseudomonas fluorescens F113 produces the Rhizobium small bacteriocin, N-(3-hydroxy-7-cis-tetradecenoyl)homoserine lactone, via HdtS, a putative novel N-acylhomoserine lactone synthase. Microbiology 146: 2469-2480.
37. Leadbetter JR & Greenberg EP (2000) Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax paradoxus. J. Bacteriol. 182: 6921-6926.
38. Lilley BN & Bassler BL (2000) Regulation of quorum sensing in Vibrio harveyi by LuxO and Sigma-54. Mol. Microbiol. 36: 940-954.
39. Lithgow JK, Wilkinson A, Hardman A, Rodelas B, Wisniewski-Dyé F, Williams P & Downie JA (2000) The regulatory locus cinRI in Rhizobium leguminosarum controls a network of quorum-sensing loci. Mol. Microbiol. 37: 81-97.
40. Lithgow JK, Danino VE, Jones J & Downie JA (2001) 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.
41. Loh JT, Yuen-Tsai JPY, Stacey MG, Lohar D, Welborn A & Stacey G (2001) Population density-dependent regulation of the Bradyrhizobium japonicum nodulation genes. Mol. Microbiol. 42: 37-46.
42. Lotz W & Mayer F (1982) Isolation and characterization of a bacteriophage tail-like bacteriocin from a strain of Rhizobium. J. Virol. 9: 160-173.
43. Manefield M, de Nys R, Kumar N, Read R, Givskov M, Steinberg P & Kjelleberg S (1999) Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145: 283-291.
44. Manefield M, Welch M, Givskov M, Salmond GPC & Kjelleberg S (2001) Halogenated furanones from the red alga, Delisea pulchra, inhibit carbapenem antibiotic synthesis and exoenzyme virulence factor production in the phytopathogen Erwinia carotovora. FEMS Microbiol. Lett. 205: 131-138.
45. McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, Swift S, Bycroft BW, Stewart GSAB & Williams P (1997) Quorum-sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143: 3703-3711.
46. McKenney D, Brown KE & Allison DG (1995) Influence of Pseudomonas aeruginosa exoproducts on virulence factor production in Burkholderia cepacia: evidence of interspecies communication. J. Bacteriol. 177: 6989-6992.
47. Nealson KH, Platt T & Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J. Bacteriol. 104: 313-322.
48. Oresnik IJ, Twelker S & Hynes MF (1999) Cloning and characterization of a Rhizobium leguminosarum gene encoding a bacteriocin with similarities to RTX toxins. Appl. Environ. Microbiol. 65: 2833-2840.
49. Passador L, Cook JM, Gambello MJ, Rust L & Iglewski BH (1993) Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260: 1127-1130.
50. Pesci EC, Milbank JBJ, Pearson JP, McKnight S, Kende AS, Greenberg EP & Iglewski BH (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96: 11229-11234.
51. Pirhonen M, Flego D, Heikinheimo R & Palva ET (1993) A small diffusible molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. EMBO J. 12: 2467-2476.
52. Priem WJE & Wijffelman CA (1984) Selection of strains cured of the Rhizobium leguminosarum Sym-plasmid pRL1JI by using small bacteriocin. FEMS Microbiol. Lett. 25: 247-251.
53. Puskas A, Greenberg EP, Kaplan S & Schaefer AL (1997) A quorum-sensing system in the free-living photosynthetic bacterium Rhodobacter sphaeroides. J. Bacteriol. 179: 7530-7537.
54. Reverchon S, Bouillant ML, Salmond G & Nasser W (1998) Integration of the quorum-sensing system in the regulatory networks controlling virulence factor synthesis in Erwinia chrysanthemi. Mol Microbiol. 29: 1407-1418.
55. Rodelas B, Gonzalez-Lopez J, Salmeron V, Martinez-Toledo MV & Pozo C (1998) Symbiotic effectiveness and bacteriocin production by Rhizobium leguminosarum bv viceae isolated from agricultural soils in Spain. Appl. Soil Ecol. 8: 51-60.
56. Rodelas B, Lithgow JK, Wisniewski-Dyé F, Hardman A, Wilkinson A, Economou A, Williams P & Downie JA (1999) Analysis of quorum-sensing-dependent control of rhizosphere-expressed (rhi) genes in Rhizobium leguminosarum bv. viciae. J. Bacteriol. 181: 3816-3823.
57. Rosemeyer V, Michiels J, Verreth C & 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.
58. Schripsema J, deRudder KEE, vanVliet TB, Lankhorst PP, deVroom E, Kijne JW & vanBrussel AAN (1996) Bacteriocin small of Rhizobium leguminosarium 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.
59. Schwinghamer EA & Brockwell J (1978) Competitive advantage of bacteriocin and phage-producing strains of Rhizobium trifolii in mixed culture. Soil Biol. Biochem. 10: 383-387.
60. Shadel GS & Baldwin TO (1991) The Vibrio fischeri LuxR protein is capable of bidirectional stimulation of transcription and both positive and negative regulation of the luxR gene. J. Bacteriol. 173: 568-574.
61. Shaw PD, Ping G, Daly SL, Cha C, Cronan JE, Rinehart KL & Farrand SK (1997) Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin layer chromatography. Proc. Natl. Acad. Sci. USA 94: 6036-6041.
62. Sourjik V, Muschler P, Scharf B & Schmitt R (2000) VisN and VisR are global regulators of chemotaxis, flagellar, and motility genes in Sinorhizobium (Rhizobium) meliloti. J Bacteriol. 182: 782-788.
63. Teplitski M, Robinson JB & Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol. Plant Microbe Interact. 13: 637-648.
64. Thorne SH & Williams HD (1997) Adaptation to nutrient starvation in Rhizobium leguminosarum bv. phaseoli: analysis of survival, stress resistance, and changes in macromolecular synthesis during entry to and exit from stationary phase. J. Bacteriol. 179: 6894-6901.
65. Thorne SH & Williams HD (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.
66. van Brussel AA, Zaat SA, Wijffelman CA, Pees E & Lugtenberg BJ (1985) Bacteriocin small of fast-growing rhizobia is chloroform soluble and is not required for effective nodulation. J. Bacteriol. 162: 1079-1082.
67. Whiteley M, Lee KM & Greenberg EP (1999) Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96: 13904-13909.
68. Whiteley M, Parsek MR & Greenberg (2000) Regulation of quorum sensing by RpoS in Pseudomonas aeruginosa. J. Bacteriol. 182: 4356-4360.
69. Wijffelman CA, Pees E, van Brussel AAN & Hooykaas PJJ (1983) Repression of small bacteriocin excretion in Rhizobium leguminosarum and Rhizobium trifolii by transmissible plasmids. Mol. Gen. Genet. 192: 171-176.
70. Wilkinson A, Danino V, Wisniewski-Dyé F, Lithgow JK & Downie JA (2002) N-acyl-homoserine lactone inhibition of rhizobial growth is mediated by two quorum-sensing genes that regulate plasmid transfer. J. Bacteriol. in press.
71. Winson MK, Camara M, Latifi A, Foglino M, Chhabra SR, Daykin M, Bally M, Chapon V, Salmond GPC, Bycroft BW, Lazdunski A, Stewart GSAB & 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.
72. Winson MK, Swift S, Fish L, Throup JP, Jørgensen F, Chhabra SR, Bycroft B, Williams P & Stewart GSAB (1998) Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum-sensing. FEMS Microbiol. Lett. 163: 185-192.
73. Winzer K, Hardie KR & Williams P (2002a) Bacterial cell-to-cell communication: sorry, can't talk now - gone to lunch ! Curr. Opin. Microbiol. 5: 216-222.
74. Winzer K, Hardie KR, Burgess N, Doherty N, Kirke D, Holden MTG, Linforth R, Cornell KA, Taylor AJ, Hill PJ & Williams P (2002b) LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone. Microbiology 148: 909-922.
75. Wisniewski-Dyé F, Jones J, Chhabra SR & Downie JA (2002) raiIR genes are part of a quorum-sensing network controlled by CinI and CinR in Rhizobium leguminosarum J. Bacteriol. 184: 1597-1606.
76. Young JPW & Wexler M (1988) Sym plasmid and chromosomal genotypes are correlated in field populations of Rhizobium leguminosarum. J. Gen. Microbiol. 134: 2371-2391.
77. Zhang L, Murphy PJ, Kerr A & Tate ME (1993) Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones. Nature 362: 446-448.