Profiling acylated homoserine lactones in Yersinia ruckeri and influence of exogenous acyl homoserine lactones and known quorum-sensing inhibitors on protease production

Journal of Applied Microbiology

Volumn 102, Issue 2, 2007, Pages 363-374

  Kastbjerg, V G ^a   Nielsen, K F ^a   Dalsgaard, I ^a   Rasch, M ^a   Bruhn, J B ^a   Givskov, M ^a   Gram, L ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Acylated homoserine lactones; Protease; Quorum sensing; Quorum sensing inhibitors; Yersinia ruckeri

Indexed keywords

ACYLATION; ESTERS; LIQUID CHROMATOGRAPHY; SULFUR;

ACYLATED HOMOSERINE LACTONE; HIGHEST TEMPERATURE; HOMOSERINE LACTONES; LIQUID CHROMATOGRAPHY-HIGH RESOLUTION MASS SPECTROMETRIES; PROTEASE; PROTEASE PRODUCTION; QUORUM-SENSING; QUORUM-SENSING INHIBITORS; SENSING SIGNALS; YERSINIA RUCKERI;

MASS SPECTROMETRY;

N (3 OXOHEPTANOYL)HOMOSERINE LACTONE; N (3 OXONONANOYL)HOMOSERINE LACTONE; N (3 OXOOCTANOYL)HOMOSERINE LACTONE; N ACYLHOMOSERINE LACTONE; PROTEINASE; UNCLASSIFIED DRUG;

AMINO ACID; BACTERIUM; ENZYME; ESTER; INHIBITOR; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PHENOTYPE; SIGNALING; VIRULENCE;

ACYLATION; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BACTERIUM DETECTION; CONTROLLED STUDY; ENZYME SYNTHESIS; FISH; IN VITRO STUDY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PHENOTYPE; QUORUM SENSING; REGULATOR GENE; REGULATORY MECHANISM; SUPERNATANT; TEMPERATURE; YERSINIA RUCKERI;

YERSINIA RUCKERI;

EID: 33846296254     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2006.03109.x     Document Type: Article

References (53)

1. Atkinson, S., Throup, J.P., Stewart, G.S.A.B. and Williams, P. (1999) A hierarchical quorum-sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and clumping. Mol Microbiol 33, 1267-1277.
2. Atkinson, S., Sockett, R.E., Camara, M. and Williams, P. (2006) Quorum sensing and the lifestyle of Yersinia. Curr Issues Mol Biol 8, 1-10.
3. Bertani, G. (1951) Studies on lysogenesis. J Bacteriol 62, 293-300.
4. Bruhn, J.B., Dalsgaard, I., Nielsen, K.F., Buchholtz, C., Larsen, J.L. and Gram, L. (2005a) Quorum sensing signal molecules (acylated homoserine lactones) in Gram-negative fish pathogenic bacteria. Dis Aquat Org 65, 43-52.
5. Bruhn, J.B., Nielsen, K.F., Hjelm, M., Hansen, M., Bresciani, J., Schulz, S. and Gram, L. (2005b) Ecology, inhibitory activity, and morphogenesis of a marine antagonistic bacterium belonging to the Roseobacter clade. Appl Environ Microbiol 71, 7263-7270.
6. Buchholtz, C., Nielsen, K.F., Milton, D.L., Larsen, J.L. and Gram, L. (2006) Profiling of acylated homoserine lactones of Vibrio anguillarum in vitro and in vivo: Influence of growth conditions and serotype. Syst Appl Microbiol (in press).
7. Cao, J.G. and Meighen, E.A. (1989) Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. J Biol Chem 264, 21670-21676.
8. Castang, S., Chantegrel, B., Deshayes, C., Dolmazon, R., Gouet, P., Haser, R., Reverchon, S., Nasser, W. et al. (2004) N-sulfonyl homoserine lactones as antagonists of bacterial quorum sensing. Bioorg Med Chem Lett 14, 5145-5149.
9. Cha, C., Gao, P., Chen, Y.C., Shaw, P.D. and Farrand, S.K. (1999) Production of acyl-homoserine lactone quorum-sensing signals by gram-negative plant-associated bacteria. Mol Plant-Microbe Interact 11, 1119-1129.
10. Clark, D.J. and Maaloe, O. (1967) DNA replication and division cycle in Escherichia coli. J Mol Biol 23, 99-112.
11. Denkin, S.M. and Nelson, D.R. (1999) Induction of protease activity in Vibrio anguillarum by gastrointestinal mucus. Appl Environ Microbiol 65, 3555-3560.
12. Dong, Y.H., Xu, J.L., Li, X.Z. and Zhang, L.H. (2000) AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci USA 97, 3526-3531.
13. Eberl, L., Winson, M.K., Sternberg, C., Stewart, G.S.A.B., Christiansen, G., Chhabra, S.R., Bycroft, B., Williams, P. et al. (1996) Involvement of N-acyl-L-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol Microbiol 20, 127-136.
14. Fernández, L., Secades, P., Lopez, J.R., Marquez, I. and Guijarro, J.A. (2002) Isolation and analysis of a protease gene with an ABC transport system in the fish pathogen Yersinia ruckeri: insertional mutagenesis and involvement in virulence. Microbiology 148, 2233-2243.
15. Fernandez, L., Lopez, J.R., Secades, P., Menendez, A., Marquez, I. and Guijarro, J.A. (2003) In vitro and in vivo studies of the Yrp1 protease from Yersinia ruckeri and its role in protective immunity against Enteric Red Mouth disease of salmonids. Appl Environ Microbiol 69, 7328-7335.
16. Fernández, L., Márquez, I. and Guijarro, J.A. (2004) Identification of specific in vivo-induced (ivi) genes in Yersinia ruckeri and analysis of ruckerbactin, a catecholate siderophore iron acquisition system. Appl Environ Microbiol 70, 5199-5207.
17. Fuqua, W.C., Winans, S.C. and Greenberg, E.P. (1994) Quorum sensing in bacteria - the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176, 269-275.
18. Furones, M.D., Gilpin, M.J., Alderman, D.J. and Munn, C.B. (1990) Virulence of Yersinia ruckeri serotype I is associated with a heat sensitive factor (HSF) in cell extracts. FEMS Microbiol Lett 66, 339-344.
19. Givskov, M.R., De Nys, R., Manefield, M., Gram, L., Maximilien, R., Eberl, L., Molin, S., Steinberg, P.D. et al. (1996) Eukaryotic interference with homoserine lactone-mediated prokaryotic signaling. J Bacteriol 178, 6618-6622.
20. Hentzer, M., Riedel, K., Rasmussen, T.B., Heydorn, A., Andersen, J.B., Parsek, M.R., Rice, S.A., Eberl, L. et al. (2002) Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148, 87-102.
21. Hentzer, M., Wu, H., Andersen, J.B., Riedel, K., Rasmussen, T.B., Bagge, N., Kumar, N., Schembri, M.A. et al. (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22, 3803-3815.
22. Jones, S., Yu, B., Bainton, N.J., Birdsall, M., Bycroft, B.W., Chhabra, S.R., Cox, A.J.R., Golby, P. et al. (1993) The Lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J 12, 2477-2482.
23. Kirwan, J.P., Gould, T.A., Schweizer, H.P., Bearden, S.W., Murphy, R.C. and Churchill, M.E.A. (2006) Quorum-sensing signal synthesis by the Yersinia pestis acyl-homoserine lactone synthase YspI. J Bacteriol 188, 784-788.
24. Koch, B., Lijefors, T., Persson, T., Nielsen, J., Kjelleberg, S. and Givskov, M. (2005) The LuxR receptor: the sites of interaction with quorum-sensing signals and inhibitors. Microbiology 151, 3589-3602.
25. Lilley, B.N. and Bassler, B.L. (2000) Regulation of quorum sensing in Vibrio harveyi by LuxO and Sigma-54. Mol Microbiol 36, 940-954.
26. Lin, Y.-H., Xu, J.-L., Hu, J., Wang, L.-H., Ong, S.L., Leadbetter, J.R. and Zhang, L.-H. (2003) Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes. Mol Microbiol 47, 849-860.
27. Manefield, M., Harris, L., Rice, S.A., De Nys, R. and Kjelleberg, S. (2000) Inhibition of luminescence and virulence in the black tiger prawn (Penaeus monodon) pathogen Vibrio harveyiby intercellular signal antagonists. Appl Environ Microbiol 66, 2079-2084.
28. Manefield, M., Welch, M., Givskov, M., Salmond, G.P.C. and 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.
29. Manny, A.J., Kjelleberg, S., Kumar, N., Read R., de Nys, R.W. and Steinberg, P. (1997) Reinvestigation of the sulfuric acid-catalysed cyclisation of brominated 2-alkyllevulinic acids to 3-alkyl-5-methylene-2(5H)-furanones. Tetrahedron 53, 15813-15826.
30. McClean, K.H., Winson, M.K., Fish, L., Taylor, A., Chhabra, S.R., Camara, M., Daykin, M., Lamb, J.H. et al. (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143, 3703-3711.
31. Milton, D.L. (2006) Quorum sensing in vibrios: Complexity for diversification. Int J Med Microbiol 296, 61-71.
32. Milton, D.L., Hardman, A., Camara, M., Chhabra, S.R., Bycroft, B.W., Stewart, G.S.A.B. and Williams, P. (1997) 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.
33. Nealson, K.H. (1977) Autoinduction of bacterial luciferase. Arch Microbiol 112, 73-79.
34. Olsen, J.A., Severinsen, R., Rasmussen, T.B., Hentzer, M., Givskov, M. and Nielsen, J. (2002) Synthesis of new 3-and 4-substituted analogues of acyl homoserine lactone quorum sensing autoinducers. Bioorg Med Chem Lett 12, 325-328.
35. Passador, L., Cook, J.M., Gambello, M.J., Rust, L. and Iglewski, B.H. (1993) Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science (Wash D C) 260, 1127-1130.
36. Persson, T., Hansen, T.H., Rasmussen, T.B., Skinderso, M.E., Givskov, M. and Nielsen, J. (2005) Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Org Biomol Chem 3, 253-262.
37. Pirhonen, M., Flego, D., Heikinheimo, R. and Palva, E.T. (1993) A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. EMBO J 12, 2467-2476.
38. Rasch, M., Buch, C., Austin, B., Slierendrecht, W.J., Ekmann, K.S., Larsen, J.L., Johansen, C., Riedel, K. et al. (2004) An inhibitor of bacterial quorum sensing reduces mortalities caused by vibriosis in rainbow trout (Oncorhynchus mykiss, Walbaum). Syst Appl Microbiol 27, 350-359.
39. Rasch, M., Andersen, J.B., Nielsen, K.F., Flodgaard, L.R., Christensen, H., Givskov, M. and Gram, L. (2005) Involvement of bacterial quorum-sensing signals in spoilage of bean sprouts. Appl Environ Microbiol 71, 3321-3330.
40. Rasch, M., Rasmussen, T.B., Andersen, J.B., Persson, T., Nielsen, J., Givskov, M. and Gram, L. (2006) Well-known quorum sensing inhibitors do not affect bacterial quorum sensing regulated bean sprout spoilage. J Appl Microbiol (in press) DOI: 10.1111/j.1365-2672.2006.03121.x.
41. Rasmussen, T.B., Bjarnsholt, T., Skindersoe, M.E., Hentzer, M., Kristoffersen, P., Kote, M., Nielsen, J., Eberl, L. et al. (2005a) Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J Bacteriol 187, 1799-1814.
42. Rasmussen, T.B., Skindersoe, M.E., Bjarnsholt, T., Phipps, R.K., Christensen, K.B., Jensen, P.O., Andersen, J.B., Koch, B. et al. (2005b) Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 151, 1325-1340.
43. Ravn, L., Christensen, A.B., Molin, S., Givskov, M. and Gram, L. (2001) Methods for detecting acylated homoserine lactones produces by Gram-negative bacteria and their application in studies of AHL-production kinetics. J Microbiol Methods 44, 239-251.
44. Reimmann, C., Ginet, N., Michel, L., Keel, C., Michaux, P., Krishnapillai, V., Zela, M., Heurlier, K. et al. (2002) Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1. Microbiology 148, 923-932.
45. Secades, P. and Guijarro, J.A. (1999) Purification and characterization of an extracellular protease from the fish pathogen Yersinia ruckeri and effect of culture conditions on production. Appl Environ Microbiol 65, 3969-3975.
46. Smith, K.M., Bu, Y.G. and Suga, H. (2003) Induction and inhibition of Pseudomonas aeruginosa quorum sensing by synthetic autoinducer analogs. Chem Biol 10, 81-89.
47. Swift, S., Karlyshev, A.V., Fish, L., Durant, E.L., Winson, M.K., Chhabra, S.R., Williams, P., MacIntyre, S. et al. (1997) Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: Identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules. J Bacteriol 179, 5271-5281.
48. Swift, S., Lynch, M.J., Fish, L., Kirke, D.F., Tomas, J.M., Stewart, G.S.A.B. and Williams, P. (1999) Quorum sensing-dependent regulation and blockade of exoprotease production in Aeromonas hydrophila. Infect Immun 67, 5192-5199.
49. Temprano, A., Yugueros, J., Hernanz, C., Sánchez, M., Berzal, B., Luengo, J.M. and Naharro, G. (2001) Rapid identification of Yersinia ruckeriby PCR amplification of yruI-yruR quorum sensing. J Fish Dis 24, 253-261.
50. Teplitski, M., Robinson, J.B. and Bauer, W.D. (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.
51. Teplitski, M., Chen, H.C., Rajamani, S., Gao, M.S., Merighi, M., Sayre, R.T., Robinson, J.B., Rolfe, B.G. et al. (2004) Chlamydomonas reinhardtii secretes compounds that mimic bacterial signals and interfere with quorum sensing regulation in bacteria. Plant Physiol (Rockv) 134, 137-146.
52. Throup, J.P., Bainton, N.J., Bycroft, B.W., Williams, P. and Stewart, G.S.A.B. (1995) Signalling in bacteria beyond bioluminescence. In Bioluminescence and Chemiluminescence: Fundamental and Applied Aspects ed. Cambell, A.K., Kricka, L.J. and Stanley, P.E. pp. 89-92. Chichester: Wiley.
53. Windle, H.J.P. and Kelleher, D. (1997) Identification and characterization of a metalloprotease activity from Helicobacter pylori. Infect Immun 65, 3132-3137.