Production of acylated homoserine lactones by different serotypes of Vibrio anguillarum both in culture and during infection of rainbow trout

Systematic and Applied Microbiology

Volumn 26, Issue 3, 2003, Pages 338-349

  Buch, Christiane ^a   Sigh, Jens ^b   Nielsen, John ^b   Larsen, Jens Laurits ^b   Gram, Lone ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Acylated homoserine lactones; Infection studies; Quorum sensing; Rainbow trout; Vibrio anguillarum

Indexed keywords

HOMOSERINE; LACTONE DERIVATIVE;

ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIUM CULTURE; CHROMOBACTERIUM; KIDNEY; LISTONELLA ANGUILLARUM; LIVER; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; RAINBOW TROUT; RHIZOBIUM RADIOBACTER; SIGNAL TRANSDUCTION;

AGROBACTERIUM; AGROBACTERIUM TUMEFACIENS; ANIMALIA; BACTERIA (MICROORGANISMS); CHROMOBACTERIUM; CHROMOBACTERIUM VIOLACEUM; LISTONELLA ANGUILLARUM; NEGIBACTERIA; ONCORHYNCHUS MYKISS; SALMONIDAE; VIBRIO; VIBRIO ANGUILLARUM;

EID: 0141593802     PISSN: 07232020     EISSN: None     Source Type: Journal    
DOI: 10.1078/072320203322497365     Document Type: Article

References (56)

1. Agodi, A., Stefani, S., Corsaro, C., Campanile, F., Gribaldo, S., Sichel, G.: Study of amelanic pigment of Proteus mirabilis. Res. Microbiol. 147, 167-174 (1996).
2. Austin, B., Austin, D. A.: Bacterial fish pathogens: disease in farmed and wild fish, 2 edn. Chichester, United Kingdom: Ellis Horwood Ltd. (1993).
3. Baehner, R. L., Nathan, D. G.: Leukocyte oxidase: Defective activity in chronic granulomatous disease. Science 155, 835-836 (1967).
4. Bainton, N.J., Bycroft, B.W., Chhabra, S.R., Stead, P., Gledhill, L., Hill, P.J., Rees, C.E., Winson, M.K., Salmond, G.P., Stewart, G.S.: A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic biosynthesis in Erwinia. Gene 116, 87-91 (1992).
5. Bassler, B. L., Wright, M., Showalter, R. E., Silverman, M. R.: Intercellular signaling in Vibrio harveyi: Sequence and function of genes regulating expression of luminescence. Mol. Microbiol. 9, 773-786 (1993).
6. Bertani, G.: Studies on lysogenesis; The mode of phage liberation by lysogenic Escherichia coli. J. Bacteriol. 62, 293-300 (1951).
7. Cao, J.-G., Meighen, E. A.: Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. J. Biol. Chem. 264, 21670-21676 (1989).
8. Cao, J.-G., Wei, Z.-Y., Meighen, E. A.: The lux autoinducer-receptor interaction in Vibrio harveyi: binding parameters and structural requirements for the autoinducer. Biochem. J. 312, 439-444 (1995).
9. Cha, C., Gao, P., Chen, Y.-C., Shaw, P.D., Farrand, S.K.: Production of acyl-homoserine lactone quorum-sensing signals by Gram-negative plant associated bacteria. Mol. Plant-Microbe Inter. 11, 1119-1129 (1998).
10. Chhabra, S.R., Harty, C., Hooi, D.S., Daykin, M., Williams, P., Telford, G., Pritchard, D.I., Bycroft, B.W.: Synthetic analogues of the bacterial signal (quorum sensing) molecule N-(3-oxododecanoyl)-1-homoserine lactone as immune modulators. J. Med. Chem. 46, 97-104 (2003).
11. Clark, D.J., Maaløe, O.: DNA Replication and the division cycle in Escherichia coli. J. Mol. Biol. 23, 99-112 (1966).
12. Croxatto, A., Chalker, V.J., Lauritz, J., Jass, J., Hardman, A. M., Williams, P., Camara, M., Milton, D.L.: VanT, a homologue of Vibrio harveyi LuxR, regulates serine, metalloprotease, pigment, and biofilm production in Vibrio anguillarum. J. Bacteriol. 184, 1617-1629 (2002).
13. Dechatelet, L.R., Shirley, P.S.: Evaluation of chronic granulomatous disease by a chemiluminescence assay of microliter quantities of whole blood. Clin. Chem. 27, 1739-1741 (1981).
14. Eberl, L., Winson, M.K., Sternberg, C., Stewart, G.S., Christiansen, G., Chhabra, S.R., Bycroft, B., Williams, P., Molin, S., Givskov, M.: Involvement of N-acyl-L-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol. Microbiol. 20, 127-136 (1996).
15. Eberl, L.: N-acyl homoserinelactone-mediated gene regualtion in Gram-negative bacteria. Syst. Appl. MicrobioL. 22, 493-506 (1999).
16. Fuqua, W.C., Winans, S.C.: 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 (1994a).
17. Fuqua, W.C., Winans, S.C., Greenberg, E.P.: Quorum sensing in bacteria: The LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176, 269-275 (1994b).
18. Gram, L., Christensen, A.B., Ravn, L., Molin, S., Givskov, M.: Production of acylated homoserine lactones by psychrotrophic members of the Enterobacteriaceae isolated from foods. Appl. Environ. Microbiol. 65, 3458-3463 (1999).
19. Greenberg, E.P.: Quorum sensing in Gram-negative bacteria. ASM News 63, 371-377 (1997).
20. Hentzer, M., Riedel, K., Rasmussen, T.B., Heydorn, A., Andersen, J.B., Parsek, M.R., Rice, S.A., Eberl, L., Molin, S., Hoiby, N., Kjelleberg, S., Givskov, M.: Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound: Microbiology 148, 87-102 (2002).
21. Jones, S., Yu, B., Bainton, N.J., Birdsall, M., Bycroft, B.W., Chhabra, S.R., Cox, A.J.R., Golby, P., Reeves, P.J., Stephens, S., Winson, M.K., Salmond, G.P.C., Stewart, G.S.A.B., Williams, P.: The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO Journal 12, 2477-2482 (1993).
22. Kuo, A., Callerhan, S.M., Dunlap, P.V.: Modulation of luminescence operon expression by N-octanoyl-L-homoserine lactone in ainS mutants of Vibrio fischeri. J. Bacteriol. 178, 971-976 (1996).
23. Larsen, J.L., Rasmussen, H.B., Dalsgaard, I.: Studies of Vibrio anguillarum strains from different sources with emphasis on ecological and pathobiological propoperties. Appl. Environ. Microbiol. 54, 2264-2267 (1988).
24. Larsen, J.L., Pedersen, K., Dalsgaard, I.: Vibrio anguillarum serovars associated with vibriosis in fish. J. Fish Dis. 12, 259-267 (1994).
25. Latifi, A., Winson, M.K., Foglino, M., Bycroft, B.W., Stewart, G.S.A.B., Lazdunski, A., Williams, P.: Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Mol. Microbiol. 17, 333-343 (1995).
26. Lawrence, R.N., Dunn, W.R., Bycroft, B.W., Camara, M., Chhabra, S.R., Williams, P., Wilson, V.G.: The Pseudomonas aeruginosa quorum-sensing signal molecule, N-(3-oxododecanoyl)-L-homoserine lactone, inhibits porcine arterial smooth muscle contraction. Brit. J. Pharm. 128, 845-848 (1999).
27. Lynch, M.J., Swift, S., Kirke, D.F., Keevil, C.W., Dodd, C.E.R., Williams, P.: The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Env. Microbiol. 4, 18-28 (2002).
28. Manefield, M., Lachlan, H., Rice, S.A., De Nys, R., Kjelleberg, S.: Inhibition of luminescence and virulence in the Black Tiger Prawn (Penaeus monodon) pathogen Vibrio harveyi by intercellular signal antagonists. Appl. Environ. Microbiol. 66, 2079-2084 (2000).
29. Mathesius, U., Mulders, S., Gao, M., Teplitski, M., Caetano-Anolles, G., Rolfe, B.G., Bauer, W.D. Extensive and specific responses of a eucaryote to bacterial quorum-sensing signals. Proc. Natl. Acad. Sci. (PNAS Early edition) (2002).
30. Meighen, E.A.: Molecular biology of bacterial bioluminescence. Microbiol. Rev. 55, 123-142 (1991).
31. Meighen, E.A.: Genetics of bacterial bioluminescence. Ann. Rev. Genet. 28, 117-139 (1994).
32. Milton, D.L., Hardman, A.M., Camara, M., Chhabra, S.R., Bycroft, B.W., Stewart, G.S.A.B., Williams, P.: Quorum sensing in Vibrio anguillarum: Characterization of the vanI/vanR locus and identification of the autoinducer N-(3-Oxodecanoyl)-L-Homoserine Lactone. J. Bacteriol. 179, 3004-3012 (1997).
33. Milton, D.L., Chalker, V.J., Kirke, D., Hardman, A.M., Camara, M., Williams, P.: The luxM homologue VanM from Vibrio anguillarum directs the synthesis of N-(3-Hydroxy-hexanoyl)homoserine lactone and N-hexanoylhomoserine lactone. J. Bacteriol. 183, 3537-3547 (2001).
34. Norqvist, A., Hagstrom, A., Wolf-Watz, H.: Protection of rainbow trout against vibriosis and furunculosis by the use of attenuated strains of Vibrio anguillarum. Appl. Environ. Microbiol. 55, 1400-1405 (1989).
35. Pearson, J.P., Gray, K.M., Passador, L., Tucker, K.D., Eberhard, A., Iglewski, B.H., Greenberg, E. P.: Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc. Natl. Acad. Sci. USA 91, 197-201 (1994).
36. Pearson, J.P., Passador, L., Iglewski, B.H., Greenberg, E.P.: A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Microbiology 92, 1490-1494 (1995).
37. Pedersen, K., Gram, L., Austin, D.A., Austin, B.: Pathogenicity of Vibrio anguillarum serogroup O1 strains compared to plasmids, outer membrane protein profiles and siderophore production. J. Appl. Microbiol. 82, 365-371 (1997).
38. Pedersen, K., Grisez, L., Van Houdt, R., Tianen, T., Ollevier, F., Larsen, J.L.: Extended serotyping scheme for Vibrio anguillarum with the definition and characterization of seven provisional O-serogroups. Curr. Microbiol. 38, 1983-1989 (1999).
39. Ravn, L., Christensen, A.B., Molin, S., Givskov, M., Gram, L.: Methods for detecting acylated homoserine lactones produced by Gram-negative bacteria and their application in studies of AHL-production kinetics. J. Microbiol. Met. 44, 239-251 (2001).
40. Ravn, L., Christensen, A.B., Molin, S., Givskov, M., Gram, L.: Influence of food preservation parameters and associate microbiota on production rate, profile and stability of acylated homoserine lactones from foodderived Enterobacteriaceae. Int. J. Food Microbiol. (in Press) (2003).
41. Redfield, R.J.: Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10, 365-370 (2002).
42. Saleh, A., Figarella, C., Kammouni, W., Marchand-Pinatel, S., Lazdunski, A., Tubul, A., Brun, P., Merten, M.D.: Pseudomonas aeruginosa quorum-sensing signal molecule, N-(3-oxododecanoyl)-L-homoserine lactone inhibits expression of P2Y receptors in cystic fibrosis tracheal gland cells. Infect. Immun. 67, 5076-5082 (1999).
43. Secombes, C.J.: Isolation of salmonid macrophages and analysis of their killing activity. In Techniques in fish immunology. pp. 137-155. Edited by Stolen, J.S., Fletcher, T.C., Anderson, D.P., Roberson, B.S., Van Muiswinkel, W. B. Fairhaven: SOS Publications (1990).
44. Seed. P.C., Passador, L., Iglewski, B.H.: Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas autoinducer PAI: An autoinduction regulation hierarchy. J. Bacteriol. 177, 654-659 (1995).
45. Shaw, P.D., Ping, G., Daly, S.L., Cha, C., Cronan, J.E. JR., Rinehart, K.L., Farrand, S.K.: Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Biochemistry 94, 6036-6041 (1997).
46. Skov, M.N., Pedersen, K., Larsen, J.L.: Comparison of pulsed-field gel-electrophoresis, ribotyping, and plasmid profiling for typing of Vibrio anguillarum serovar O1. Appl. Environ. Microbiol. 61, 1540-1545 (1995).
47. Smith, R.S., Harris, S.G., Phipps, R., Iglewski, B:. The Pseudomonas aeruginosa quorum-sensing molecule N-(3-oxododecanoyl)homoserine lactone contributes to virulence and induces inflammation in vivo. J. Bacteriol. 184, 1132-1139 (2002).
48. Swift, S., Karlyshev, A.V., Fish, L., Durnat, E.L., Winson, M.K., Chhabra, S.R., Williams, P., Macintyre, S., Stewart, G.S.A.B.: Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: Identification of the LuxRI homologues AhyRI and AsaRI and their cognate N-Acylhomoserine lactone signal molecules. J. Bacteriol. 179, 5271-5281 (1997).
49. Swift, S., Lynch, M.J., Fish, L., Kirke, D., Thomas, J.M., Stewart, G.S.A.B., Williams, P.: Quorum sensing-dependent regulation and blockade of exoprotease production in Aeromonas hydrophila. Infect. Immun. 67, 5192-5199 (1999).
50. Telford, G., Wheeler, D., Williams, P., Tomkins, P.T., Appleby, P., Sewell, H., Stewart, G.S.A.B., Bycroft, B.W., Pritchard, D.I.: The Pseudomonas aeruginosa quorum-sensing signal molecule, N-(3-oxododecanoyl)-L-homoserine lactone has immunomodulatory activity. Infect. Immun. 66, 36-42 (1998).
51. Throup, J.P., Bainton, N.J., Bycroft, B.W., Williams, P., Stewart, G.S.A.B.: Signalling in bacteria beyond bioluminescence. In Bioluminescence and Chemiluminescence: fundamental and applied aspects. pp. 89-92. Edited by Cambell, A.K., Kricka, L.J., Stanley, P.E. Chichester, UK: Whiley (1995a).
52. Throup, J.P., Camara, M., Briggs, G.S., Winson, M.K., Chhabra, S.R., Bycroft, B.W., Williams, P., Stewart, G.S.A.B.: Characterisation of the yenI/yenR locus from Yersinia enterocolitica mediating the synthesis of two N-acylhomoserine lactone signal molecules. Mol. Microbiol. 17, 345-356 (1995b).
53. Whitehead, N.A., Barnard, A.M.L., Slater, H., Simpson, N.J.L., Salmond, G.P.C.: Quorum-sensing in Gram-negative bacteria. FEMS Microbiol. Rev. 25, 365-404 (2001).
54. Winson, M.K., Camara, M., Latifi, A., Foglino, M., Chhabra, S.R., Daykin, M., Bally, M., Chapron, V., Salmond, G.P.C., Bycroft, B.W., Lazdunski, A., Stewart, G.S.A.B., Williams, P.: Multiple N-acyl-L-homoserin lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Microbiology 92, 9427-9431 (1995).
55. Wood, D.W., Pierson, L.S.: The phz gene of Pseudomonas aureofaciens 30-84 is responsible for the production of a diffusible signal required for phenazine antibiotic production. Gene 168, 49-53 (1996).
56. Zughaier, S.M., Ryley, H.C., Jackson, S.K.: A melanin pigment purified from an epidemic strain of Burkholderia cepacia attenuates monocyte respiratory burst activity by scavenging superoxide anion. Infect. Immun. 67, 908-913 (1999).