The acyl-homoserine lactone (AHL)-type quorum sensing system affects growth rate, swimming motility and virulence in Acidovorax avenae subsp. citrulli

World Journal of Microbiology and Biotechnology

Volumn 27, Issue 5, 2011, Pages 1155-1166

  Fan, Jiaqin ^a   Qian, Guoliang ^a   Chen, Tao ^a   Zhao, Yuqiang ^a   Liu, Fengquan ^a   Walcott, Ron R ^b   Hu, Baishi ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Acidovorax avenae subsp. citrulli; Acyl homoserine lactone; Autoinducer; Bacterial fruit blotch; Quorum sensing

Indexed keywords

ACIDOVORAX AVENAE; ACYL-HOMOSERINE LACTONE; AUTOINDUCER; BACTERIAL FRUIT BLOTCH; QUORUM SENSING;

BACTERIOLOGY; CLONING; FRUITS; GENES; SENSORS;

BACTERIA;

ACIDOVORAX AVENAE SUBSP. CITRULLI; BACTERIA (MICROORGANISMS); CITRULLUS LANATUS VAR. LANATUS; CUCUMIS; NEGIBACTERIA; NICOTIANA TABACUM;

EID: 79955073530     PISSN: 09593993     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11274-010-0562-9     Document Type: Article

References (67)

1. Andersson RA, Eriksson ARB, Heikinheimo R, Mae A, Pirhonen M, Koiv V, HyytiǍinen H, Tuikkala A, Palvae T (2000) Quorum sensing in the plant pathogen Erwiniacarotovora subsp. carotovora: the role of expREcc. Mol Plant Microbe Interact 13(4): 384-393.
2. Atkinson S, Chang CY, Sockett RE, Cámara M, Williams P (2006) Quorum sensing in Yersinia enterocolitica controls swimming and swarming motility. J Bacteriol 188: 1451-1461.
3. Balestrino D, Haagensen JA, Rich C, Forestier C (2005) Characterization of type 2 quorum sensing in Klebsiella pneumoniae and relationship with biofilm formation. J Bacteriol 187: 2870-2880.
4. Bassler BL (1999) How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr Opin Microbiol 2: 582-587.
5. Burdman S, Kots N, Kritzman G, Kopelowitz J (2005) Molecular, physiological, and host-range characterization of Acidovorax avenae subsp. citrulli isolates from watermelon and melon in Israel. Plant Dis 89: 1339-1347.
6. Chen L, Hu BS, Qian GL, Wang C, Yang WF, Han ZC, Liu FQ (2009a) Identification and molecular characterization of twin-arginine translocation system (Tat) in Xanthomonas oryzae pv. oryzae strain PXO99. Arch Microbiol 191: 163-170.
7. Chen T, Qian GL, Yang XL, Ma JY, Hu BS, Liu FQ (2009b) Detection of quorum sensing signal molecule of Acidovorax avenae subsp. citrulli and its regulation on pathogenicity. Chin J Agri Biotechnol 6: 49-53.
8. Chesnokova O, Coutinho JB, Khan IH, Mikhail MS, Kado CI (1997) Characterization of flagella genes of Agrobacterium tumefaciens, and the effect of a bald strain on virulence. Mol Microbiol 23: 579-590.
9. Daniels MJ, Barber CE, Turner PC, Sawczyc MK, Byrde RJW, Fielding AH (1984) Cloning of genes involved in pathogenicity of Xanthomonas campestris pv. campestris using the broad host range cosmid pLAFR1. EMBO J 3: 3323-3328.
10. De Kievit TR, Iglewski BH (2000) Bacterial quorum sensing in pathogenic relationships. Infect Immun 68: 4839-4849.
11. Dong YH, Xu JL, Li XZ, Zhang LH (2000) AiiA, an enzyme that inactivates the acylhomoserine lactone quorumsensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci USA 97: 3526-3531.
12. 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.
13. Feldman M, Bryan R, Rajan S, Scheffler L, Brunnert S, Tang H, Prince A (1998) Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun 66: 43-51.
14. Fessehaie A, Walcott RR (2005) Biological control to protect watermelon blossoms and seed from infection by Acidovoraxavenae subsp. citrulli. Phytopathol 95(4): 413-419.
15. Fray RG, Throup JP, Daykin M, Wallace A, Williams P, Stewart GSAB, Grierson D (1999) Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria. Nat Biotechnol 17: 1017-1020.
16. Fuqua C, Greenberg EP (1998) Self perception in bacteria: quorum sensing with acylated homoserine lactones. Curr Opin Microbiol 1: 183-189.
17. Fuqua WC, Winans SC (1994) A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite. J Bacteriol 176: 2796-2806.
18. Gao Y, Song JX, Hu BS, Zhang L, Liu QQ, Liu FQ (2009) The luxS gene is involved in AI-2 production, pathogenicity, and some phenotypes in Erwinia amylovora. Curr Microbiol 58: 1-10.
19. Greenberg EP (1997) Quorum sensing in gram-negative bacteria. ASM News 63: 371-377.
20. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212: 77-86.
21. Hopkins DL, Cucuzza JD, Watterson JC (1996) Wet seed treatments for the control of bacterial fruit blotch of watermelon. Plant Dis 80: 529-532.
22. Hu XJ, Roberts DP, Jiang ML, Zhang YB (2005) Decreased incidence of disease caused by Sclerotinia sclerotiorum and improved plant vigor of oilseed rape with Bacillus subtilis Tu-100. Appl Microbiol Biotechnol 68: 802-807.
23. Huang JJ, Han JI, Zhang LH, Leadbetter JR (2003) Utilization of acyl-homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 69: 05941-05949.
24. Huber B, Riedel K, Riedel K, Hentzer M, Heydorn A, Gotschlich A, Givskov M, Molin S, Eberl L (2001) The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147: 2517-2528.
25. Hussain MBBM, Zhang HB, Xu JL, Liu QG, Jiang ZD, Zhang LH (2008) The acyl-homoserine lactone-type quorum sensing modulates cell motility and virulence of Eriwinia charysanthemi pv. zeae. J Bacteriol 190(3): 1045-1053.
26. Khajanchi BK, Sha J, Kozlova EV, Erova TE, Suarez G, Sierra JC, Popov VL, Horneman AJ, Chopra AK (2009) N-Acylhomoserine lactones involved in quorum sensing control the type VI secretion system biofilm formation, protease production and in vivo virulence in a clinical isolate of Aeromonas hydrophila. Microbiol 155: 3518-3531.
27. Koutsoudis MD, Tsaltas D, Minogue TD, Von Bodman SB (2006) Quorum sensing regulation governs bacterial adhesion, biofilm development, and host colonization in Pantoea stewartii subspecies stewartii. Proc Natl Acad Sci 103(15): 5983-5988.
28. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM II, Peterson KM (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176.
29. Lázaro M, Fabio R, Geneviève D, Brion D (2005) Autoinduction in Erwinia amlyvora: evidence of an acyl-homoserine lactone signal in the fire blight pathogen. J Bacteriol 187(9): 3206-3213.
30. Lemon KP, Higgins DE, Kolter R (2007) Flagellar motility is critical for Listeria monocytogenes biofilm formation. J Bacteriol 189(12): 4418-4424.
31. Lin YH, Xu JL, Hu J, Wang LH, Ong SL, Leadbetter JR, Zhang LH (2003) Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes. Mol Microbiol 47: 849-860.
32. Maddula VS, Zhang Z, Pierson EA, Pierson LS (2006) Quorum sensing and phenazines are involved in Biofilm formation by Pseudomonas chlororaphis (aureofaciens) strain 30-84. Microb Ecol 52(2): 289-301.
33. Mäe A, Montesano M, Koiv V, Tapio-Palva E (2001) Transgenic plants producing the bacterial pheromone N-acyl-homoserine lactone exhibit enhanced resistance to the bacterial phytopathogen Erwinia carotovora. Mol Plant Microbe Interact 14: 1035-1042.
34. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
35. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55: 165-199.
36. Mobley HL, Belas R, Lockatell V, Chippendale G, Trifillis AL, Johnson DE, Warren JW (1996) Construction of a flagellum-negative mutant of Proteus mirabilis: effect on internalization by human renal epithelial cells and virulence in a mouse model of ascending urinary tract infection. Infect Immun 64: 5332-5340.
37. Novick RP, Muir TW (1999) Virulence gene regulation by peptides in staphylococci and other Gram-positive bacteria. Curr Opin Microbiol 2: 40-45.
38. Palumbo J, Yuen G, Jochum C, Tatum K, Kobayashi D (2005) Mutagenesis of b-1, 3-glucanase genes in Lysobacter enzymogenes strain C3 results in reduced biological control activity towards Bipolaris leaf spot of tall fescue and Pythium damping off of sugarbeet. Phytopathology 95: 701-707.
39. Park SY, Lee SJ, Oh TK, Oh JW, Koo BT, Yum DY, Lee JK (2003) AhlD, an N-acylhomoserine lactonase in Arthrobacter sp., and predicted homologues in other bacteria. Microbiology 149: 1541-1550.
40. Pesci EC, Pearson JP, Seed PC, Iglewski BH (1997) Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179(10): 3127-3132.
41. Quinones B, Pujol CJ, Lindow SE (2004) Regulation of AHL production and its contribution to Epiphytic fitness in Pseudomonas syringae. Mol Plant Microbe Interact 17(5): 521-531.
42. Quiñones B, Dulla G, Lindow SE (2005) Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae. Mol Plant Microbe Interact 18(7): 682-693.
43. Ray SK, Rajeshwari R, Sonti RV (2000) Mutants of Xanthomonas oryzae pv. oryzae deficient in general secretory pathway are virulence deficient and unable to secrete xylanase. Mol Plant Microbe Interact 13: 394-401.
44. Reimmann C, Ginet N, Michel C, Keel C, Michanux P, Zala M, Heurlier K, Triandafillu K, Harms H, Défago G, Haas D (2002) Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1. Microbiology 148: 923-932.
45. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory mannual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
46. Schaad NW, Sowell G, Goth RW, Colwell RR, Webb RE (1978) Pseudomonas pseudoalcaligenes subsp. citrulli subsp. nov. Int J Syst Bact 28: 117-125.
47. Shaw PD, Ping G, Daly SL, Cha C, Cronan JE Jr, Rinehart KL, Farrand SK (1997) Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc Natl Acad Sci 94: 6036-6041.
48. Simon R, Priefer U, Pühler A (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 1: 787-796.
49. Somodi GC, Jones JB, Hopkins DL, Stall RE, Kucharek TA, Hodge NC, Watterson JC (1991) Occurrence of bacterial watermelon fruit blotch in Florida. Plant Dis 75: 1053-1056.
50. Tang JL, Feng JX, Li QQ, Wen HX, Zhou DL, Wilson TJG (1996) Cloning and characterization of the rpfC gene of Xanthomonas oryzae pv. oryzae: involvement in exopolysaccharide production and virulence to rice. Mol Plant Microbe Interact 9: 664-666.
51. Von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41: 455-482.
52. Walcott RR, Gitaitis RD (2000) Detection of Acidovorax avenae subsp. citrulli in watermelon seed using immunomagetic separation and the polymerase chain reaction. Plant Dis 84: 470-474.
53. Walcott RR, Langston DB Jr, Sanders FH Jr, Gitaitis RD (2000) Investigating intraspecific variation of Acidovorax avenae subsp. citrulli using DNA fingerprinting and whole fatty cell acid analysis. Phytopathology 90: 191-196.
54. Walcott RR, Fessehaie A, Castro AC (2004) Differences in pathogenicity between two genetically distinct groups of Acidovorax avenae subsp. citrulli on cucurbit hosts. J Phytopathol 152: 277-285.
55. Wang Y, Zheng HM, Yang MH, Zhong ZT, Zhu J (2007) Screening for autoinducer synthase gene in Sinorhizobium meliloti and analysis of the autoinducer produced by recombinant expression in Escherichia coli. Acta Microbiol Sin 47(5): 838-842.
56. Wang P, Zhong ZT, Zhou J, Cai T, Zhu J (2008) Exopolysaccharide biosynthesis is important for Mesorhizobium tianshanense: plant host interaction. Arch Microbiol 189: 525-530.
57. Want WZ, Morohoshi T, Ikenoya M, Someya N, Ikeda T (2010) AiiM, a novel class of N-acylhomoerine lactonase from the leaf-associated bacterium Microbacterium testaceum. Appl Environ Microbiol 76: 2524-2530.
58. Waters C, Bassler B (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21: 319-346.
59. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP (2001) Quorum-sensing in gram-negative bacteria. FEMS Microbiol Rev 25: 365-404.
60. Willems A, Goor M, Thielemans S, Gillis M, Kersters K, Ley JD, De Ley J (1992) Transfer of several phytopathogenic Pseudomonas species to Acidovorax as Acidovorax avenae subsp. avenae subsp. nov., comb. nov., Acidovorax avenae subsp. citrulli, Acidovorax avenae subsp. cattleyae, and Acidovorax konjaci. Int J Syst Bact 42: 107-119.
61. Williams P, Camara M, Hardman A, Swift S, Milton D, Hope VJ, Winzer K, Middleton B, Pritchard DI, Bycroft BW (2000) Quorum sensing and the population dependent control of virulence. Philos Trans R Soc Lond B Biol Sci 355: 667-680.
62. Withers H, Swift S, Williams P (2001) Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria. Curr Opin Microbiol 4: 186-193.
63. Yin XT, Xu L, Fan SS, Xu LN, Li DC, Liu ZY (2010) Isolation and characterization of an AHL lactonase gene from Bacillus amyloliquefaciens. World J Microbiol Biotechnol 26: 1361-1367.
64. Zhang HB, Wang LH, Zhang LH (2002) Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens. Proc Natl Acad Sci 99(7): 4638-4643.
65. Zheng HM, Zhong ZT, Lai X, Chen WX, Li SP, Zhu J (2006) A LuxR/LuxI-type quorum sensing system in a plant bacterium, Mesorhizobium tianshanense, controls symbiotic nodulation. J Bacteriol 188: 1943-1949.
66. Zhou H, Yao F, Roberts DP, Lessie TG (2003) AHL-deficient mutants of Burkholderia ambifaria BC-F have decreased antifungal activity. Curr Microbiol 47(3): 174-179.
67. Zhu J, Chai Y, Zhong Z, Li S, Winans SC (2003) Agrobacterium bioassay strain for ultrasensitive detection of N-acylhomoserine lactone-type quorum-sensing molecules: detection of autoinducers in Mesorhizobium huakuii. Appl Environ Microbiol 69: 6949-6953.