1887

Abstract

-Acyl--homoserine-lactone-producing species are frequently encountered in spoiling foods of vegetable and protein origin. The role of quorum sensing in the food spoiling properties of these bacteria is currently being investigated. A set of homologous genes encoding a putative quorum sensor was identified in the -(3-oxo-hexanoyl)--homoserine lactone (3-oxo-C6-HSL)-producing strain B5a. The 3-oxo-C6-HSL synthase SprI showed 79 % similarity with EsaI from and the putative regulatory protein SprR was 86 % similar to the SpnR of . Proteome analysis suggested that the presence of at least 39 intracellular proteins was affected by the 3-oxo-C6-HSL-based quorum sensing system. The -encoded secretion system was identified as one target gene of the quorum sensing system. LipB was required for the production of extracellular lipolytic and proteolytic activities, thus rendering the production of food-deterioration-relevant exoenzymes indirectly under the control of quorum sensing. Strain B5a caused quorum-sensing-controlled spoilage of milk. Furthermore, chitinolytic activity was controlled by quorum sensing. This control appeared to be direct and not mediated via LipB. The data presented here demonstrate that quorum-sensing-controlled exoenzymic activities affect food quality.

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2003-02-01
2019-12-08
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References

  1. Akatsuka, H., Kawai, E., Omori, K. & Shibatani, T. ( 1995; ). The three genes lipB, lipC, and lipD involved in the extracellular secretion of the Serratia marcescens lipase which lacks an N-terminal signal peptide. J Bacteriol 177, 6381–6389.
    [Google Scholar]
  2. Akatsuka, H., Binet, R., Kawai, E., Wandersman, C. & Omori, K. ( 1997; ). Lipase secretion by bacterial hybrid ATP-binding cassette exporters: molecular recognition of the LipBCD, PrtDEF, and HasDEF exporters. J Bacteriol 179, 4754–4760.
    [Google Scholar]
  3. Andersen, J. B., Heydorn, A., Hentzer, M., Eberl, L., Geisenberger, O., Christensen, B. B., Molin, S. & Givskov, M. ( 2001; ). gfp-based N-acyl homoserine-lactone sensor systems for detection of bacterial communication. Appl Environ Microbiol 67, 575–585.[CrossRef]
    [Google Scholar]
  4. Atkinson, S., Throup, J. P., Stewart, G. S. & 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.
    [Google Scholar]
  5. Awram, P. & Smit, J. ( 1998; ). The Caulobacter crescentus paracrystalline S-layer protein is secreted by an ABC transporter (type I) secretion apparatus. J Bacteriol 180, 3062–3069.
    [Google Scholar]
  6. Ayora, S. & Gotz, F. ( 1994; ). Genetic and biochemical properties of an extracellular neutral metalloprotease from Staphylococcus hyicus subsp. hyicus. Mol Gen Genet 242, 421–430.
    [Google Scholar]
  7. Beck von Bodman, S. & Farrand, S. K. ( 1995; ). Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer. J Bacteriol 177, 5000–5008.
    [Google Scholar]
  8. Beck von Bodman, S., Majerczak, D. R. & Coplin, D. L. ( 1998; ). A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proc Natl Acad Sci U S A 95, 7687–7692.[CrossRef]
    [Google Scholar]
  9. Bertani, G. ( 1951; ). Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62, 293–300.
    [Google Scholar]
  10. Binet, R., Letoffe, S., Ghigo, J. M., Delepelaire, P. & Wandersman, C. ( 1997; ). Protein secretion by Gram-negative bacterial ABC exporters – a review. Gene 192, 7–11.[CrossRef]
    [Google Scholar]
  11. Blum, H., Beier, H. & Gross, H. J. ( 1987; ). Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8, 93–99.[CrossRef]
    [Google Scholar]
  12. Borch, E., Kant-Muermans, M. L. & Blixt, Y. ( 1996; ). Bacterial spoilage of meat and cured meat products. Int J Food Microbiol 33, 103–120.[CrossRef]
    [Google Scholar]
  13. Bucher, G. E. ( 1960; ). Potential bacterial pathogens of insects and their characteristics. J Insect Pathol 2, 172–195.
    [Google Scholar]
  14. Burger, M., Woods, R. G., McCarthy, C. & Beacham, I. R. ( 2000; ). Temperature regulation of protease in Pseudomonas fluorescens LS107d2 by an ECF sigma factor and a transmembrane activator. Microbiology 146, 3149–3155.
    [Google Scholar]
  15. Cha, C., Gao, P., Chen, Y. C., Shaw, P. D. & 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.[CrossRef]
    [Google Scholar]
  16. Chatterjee, A., Murata, H., McEvoy, J. L. & Chatterjee, A. ( 1994; ). Global regulation of pectinases and other degradative enzymes in Erwinia carotovora subsp. carotovora, the incitant of postharvest decay in vegetables. Hort Sci 29, 754–758.
    [Google Scholar]
  17. Clark, J. D. & Maaloe, O. ( 1967; ). DNA replication and the division cycle in Escherichia coli. J Mol Biol 23, 99–112.[CrossRef]
    [Google Scholar]
  18. Costerton, J. W., Stewart, P. S. & Greenberg, E. P. ( 1999; ). Bacterial biofilms: a common cause of persistent infections. Science 284, 1318–1322.[CrossRef]
    [Google Scholar]
  19. Davies, D. G., Parsek, M. R., Pearson, J. P., Iglewski, B. H., Costerton, J. W. & Greenberg, E. P. ( 1998; ). The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280, 295–298.[CrossRef]
    [Google Scholar]
  20. De Lorenzo, V., Herrero, M., Jakubzik, U. & Timmis, K. N. ( 1990; ). Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in Gram-negative eubacteria. J Bacteriol 172, 6568–6572.
    [Google Scholar]
  21. Dunlap, P. V. ( 1999; ). Quorum regulation of luminescence in Vibrio fischeri. J Mol Microbiol Biotechnol 1, 5–12.
    [Google Scholar]
  22. Eberl, L., Winson, M. K., Sternberg, C. & 7 other authors ( 1996; ). Involvement of N-acyl-l-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol Microbiol 20, 127–136.[CrossRef]
    [Google Scholar]
  23. Engebrecht, J. & Silverman, M. ( 1984; ). Identification of genes and gene products necessary for bacterial bioluminescence. Proc Natl Acad Sci U S A 81, 4154–4158.[CrossRef]
    [Google Scholar]
  24. Fuqua, C., Parsek, M. R. & Greenberg, E. P. ( 2001; ). Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35, 439–468.[CrossRef]
    [Google Scholar]
  25. Gal, S. W., Choi, J. Y., Kim, C. Y., Cheong, Y. H., Choi, Y. J., Lee, S. Y., Bahk, J. D. & Cho, M. J. ( 1998; ). Cloning of the 52-kDa chitinase gene from Serratia marcescens KCTC2172 and its proteolytic cleavage into an active 35-kDa enzyme. FEMS Microbiol Lett 160, 151–158.[CrossRef]
    [Google Scholar]
  26. Givskov, M., Eberl, L., Christiansen, G., Benedik, M. J. & Molin, S. ( 1995; ). Induction of phospholipase- and flagellar synthesis in Serratia liquefaciens is controlled by expression of the flagellar master operon flhD. Mol Microbiol 15, 445–454.[CrossRef]
    [Google Scholar]
  27. Givskov, M., De Nys, R., Manefield, M., Gram, L., Maximilien, R., Eberl, L., Molin, S., Steinberg, P. D. & Kjelleberg, S. ( 1996; ). Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J Bacteriol 178, 6618–6622.
    [Google Scholar]
  28. Givskov, M., Ostling, J., Eberl, L., Lindum, P. W., Christensen, A. B., Christiansen, G., Molin, S. & Kjelleberg, S. ( 1998; ). Two separate regulatory systems participate in control of swarming motility of Serratia liquefaciens MG1. J Bacteriol 180, 742–745.
    [Google Scholar]
  29. Görg, A., Obermaier, C., Boguth, G., Harder, A., Scheibe, B., Wildgruber, R. & Weiss, W. ( 2000; ). The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 21, 1037–1053.[CrossRef]
    [Google Scholar]
  30. Gram, L., Christensen, A. B., Ravn, L., Molin, S. & Givskov, M. ( 1999; ). Production of acylated homoserine lactones by psychrotrophic members of the Enterobacteriaceae isolated from foods. Appl Environ Microbiol 65, 3458–3463.
    [Google Scholar]
  31. Hanna, S. L., Sherman, N. E., Kinter, M. T. & Goldberg, J. B. ( 2000; ). Comparison of proteins expressed by Pseudomonas aeruginosa strains representing initial and chronic isolates from a cystic fibrosis patient: an analysis by 2-D gel electrophoresis and capillary column liquid chromatography-tandem mass spectrometry. Microbiology 146, 2495–2508.
    [Google Scholar]
  32. Hansen, L. H., Sørensen, S. J. & Jensen, L. B. ( 1997; ). Chromosomal insertion of the entire Escherichia coli lactose operon, into two strains of Pseudomonas, using a modified mini-Tn5 delivery system. Gene 186, 167–173.[CrossRef]
    [Google Scholar]
  33. Herrera-Estrella, A. & Chet, I. ( 1999; ). Chitinases in biological control. EXS 87, 171–184.
    [Google Scholar]
  34. Herrero, M., De Lorenzo, V. & Timmis, K. N. ( 1990; ). Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in Gram-negative bacteria. J Bacteriol 172, 6557–6567.
    [Google Scholar]
  35. Horng, Y. T., Deng, S. C., Daykin, M. & 7 other authors ( 2002; ). The LuxR family protein SpnR functions as a negative regulator of N-acylhomoserine lactone-dependent quorum sensing in Serratia marcescens. Mol Microbiol 45, 1655–1671.[CrossRef]
    [Google Scholar]
  36. Huber, B., 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.
    [Google Scholar]
  37. Jones, S., Yu, B., Bainton, N. J. & 11 other authors ( 1993; ). The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J 12, 2477–2482.
    [Google Scholar]
  38. Jørgensen, L. V., Huss, H. H. & Dalgaard, P. ( 2000; ). The effect of biogenic amine production by single bacterial cultures and metabiosis on cold-smoked salmon. J Appl Microbiol 89, 920–934.[CrossRef]
    [Google Scholar]
  39. Kalbe, C., Marten, P. & Berg, G. ( 1996; ). Strains of the genus Serratia as beneficial rhizobacteria of oilseed rape with antifungal properties. Microbiol Res 151, 433–439.[CrossRef]
    [Google Scholar]
  40. Kawai, E., Akatsuka, H., Idei, A., Shibatani, T. & Omori, K. ( 1998; ). Serratia marcescens S-layer protein is secreted extracellularly via an ATP-binding cassette exporter, the Lip system. Mol Microbiol 27, 941–952.[CrossRef]
    [Google Scholar]
  41. Kessler, B., De Lorenzo, V. & Timmis, K. N. ( 1992; ). A general system to integrate lacZ fusions into the chromosomes of Gram-negative eubacteria: regulation of the Pm promoter of the TOL plasmid studied with all controlling elements in monocopy. Mol Gen Genet 233, 293–301.[CrossRef]
    [Google Scholar]
  42. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef]
    [Google Scholar]
  43. Lane, D. J. ( 1991; ). 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics, pp. 115–175. Edited by E. Stackebrandt & M. Goodfellow. London: Wiley.
  44. Latifi, A., Winson, M. K., Foglino, M., Bycroft, B. W., Stewart, G. S., Lazdunski, A. & Williams, P. ( 1995; ). 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.[CrossRef]
    [Google Scholar]
  45. Liao, C. H. ( 1989; ). Analysis of pectate lyases produced by soft rot bacteria associated with spoilage of vegetables. Appl Environ Microbiol 55, 1677–1683.
    [Google Scholar]
  46. Lindberg, A. M., Ljungh, A., Ahrne, S., Lofdahl, S. & Molin, G. ( 1998; ). Enterobacteriaceae found in high numbers in fish, minced meat and pasteurised milk or cream and the presence of toxin encoding genes. Int J Food Microbiol 39, 11–17.[CrossRef]
    [Google Scholar]
  47. Lindum, P. W., Anthoni, U., Christophersen, C., Eberl, L., Molin, S. & Givskov, M. ( 1998; ). N-Acyl-l-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1. J Bacteriol 180, 6384–6388.
    [Google Scholar]
  48. McClean, K. H., Winson, M. K., Fish, L. & 9 other authors ( 1997; ). Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection <1?show=[to]>of N-acylhomoserine lactones. Microbiology 143, 3703–3711.[CrossRef]
    [Google Scholar]
  49. Miller, M. B. & Bassler, B. L. ( 2001; ). Quorum sensing in bacteria. Annu Rev Microbiol 55, 165–199.[CrossRef]
    [Google Scholar]
  50. Minogue, T. D., Trebra, M. W., Bernhard, F. & Bodman, S. B. ( 2002; ). The autoregulatory role of EsaR, a quorum-sensing regulator in Pantoea stewartii ssp. stewartii: evidence for a repressor function. Mol Microbiol 44, 1625–1635.[CrossRef]
    [Google Scholar]
  51. Nakahama, K., Yoshimura, K., Marumoto, R., Kikuchi, M., Lee, I. S., Hase, T. & Matsubara, H. ( 1986; ). Cloning and sequencing of Serratia protease gene. Nucleic Acids Res 14, 5843–5855.[CrossRef]
    [Google Scholar]
  52. Paludan-Muller, C., Dalgaard, P., Huss, H. H. & Gram, L. ( 1998; ). Evaluation of the role of Carnobacterium piscicola in spoilage of vacuum- and modified-atmosphere-packed cold-smoked salmon stored at 5 °C. Int J Food Microbiol 39, 155–166.[CrossRef]
    [Google Scholar]
  53. Payens, T. A. ( 1982; ). Stable and unstable casein micelles. J Dairy Sci 65, 1863–1873.[CrossRef]
    [Google Scholar]
  54. Pearson, J. P., Gray, K. M., Passador, L., Tucker, K. D., Eberhard, A., Iglewski, B. H. & Greenberg, E. P. ( 1994; ). Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc Natl Acad Sci U S A 91, 197–201.[CrossRef]
    [Google Scholar]
  55. Piper, K. R., Beck von Bodman, S. & Farrand, S. K. ( 1993; ). Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 362, 448–450.[CrossRef]
    [Google Scholar]
  56. Pirhonen, M., Flego, D., Heikinheimo, R. & 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.
    [Google Scholar]
  57. Ravn, L., Christensen, A. B., Molin, S., Givskov, M. & Gram, L. ( 2001; ). Methods for detecting acylated homoserine lactones produced by Gram-negative bacteria and their application in studies of AHL-production kinetics. J Microbiol Methods 44, 239–251.[CrossRef]
    [Google Scholar]
  58. Riedel, K., Ohnesorg, T., Krogfelt, K. A., Hansen, T. S., Omori, K., Givskov, M. & Eberl, L. ( 2001; ). N-Acyl-l-homoserine lactone-mediated regulation of the Lip secretion system in Serratia liquefaciens MG1. J Bacteriol 183, 1805–1809.[CrossRef]
    [Google Scholar]
  59. Salmond, G. P., Bycroft, B. W., Stewart, G. S. & Williams, P. ( 1995; ). The bacterial ‘enigma’: cracking the code of cell–cell communication. Mol Microbiol 16, 615–624.[CrossRef]
    [Google Scholar]
  60. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  61. Sitnikov, D. M., Schineller, J. B. & Baldwin, T. O. ( 1995; ). Transcriptional regulation of bioluminescence genes from Vibrio fischeri. Mol Microbiol 17, 801–812.[CrossRef]
    [Google Scholar]
  62. Snaidr, J., Amann, R., Huber, I., Ludwig, W. & Schleifer, K. H. ( 1997; ). Phylogenetic analysis and in situ identification of bacteria in activated sludge. Appl Environ Microbiol 63, 2884–2896.
    [Google Scholar]
  63. Swift, S., Winson, M. K., Chan, P. F. & 11 other authors ( 1993; ). A novel strategy for the isolation of luxI homologues: evidence for the widespread distribution of a LuxR : LuxI superfamily in enteric bacteria. Mol Microbiol 10, 511–520.[CrossRef]
    [Google Scholar]
  64. Swift, S., Williams, P. & Stewart, G. S. A. B. ( 1999; ). N-Acylhomoserine lactones and quorum sensing in Proteobacteria. In Cell–Cell Signaling in Bacteria, pp. 291–314. Edited by G. M. Dunny & S. C. Winans. Washington, DC: American Society for Microbiology.
  65. Tan, Y. & Miller, K. J. ( 1992; ). Cloning, expression, and nucleotide sequence of a lipase gene from Pseudomonas fluorescens B52. Appl Environ Microbiol 58, 1402–1407.
    [Google Scholar]
  66. Thompson, S. A., Shedd, O. L., Ray, K. C., Beins, M. H., Jorgensen, J. P. & Blaser, M. J. ( 1998; ). Campylobacter fetus surface layer proteins are transported by a type I secretion system. J Bacteriol 180, 6450–6458.
    [Google Scholar]
  67. Thomson, N. R., Crow, M. A., McGowan, S. J., Cox, A. & Salmond, G. P. ( 2000; ). Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol Microbiol 36, 539–556.
    [Google Scholar]
  68. Throup, J. P., Camara, M., Briggs, G. S., Winson, M. K., Chhabra, S. R., Bycroft, B. W., Williams, P. & Stewart, G. S. ( 1995; ). Characterization of the yenI/yenR locus from Yersinia enterocolitica mediating the synthesis of two N-acylhomoserine lactone signal molecules. Mol Microbiol 17, 345–356.[CrossRef]
    [Google Scholar]
  69. Watanabe, T., Kimura, K., Sumiya, T., Nikaidou, N., Suzuki, K., Suzuki, M., Taiyoji, M., Ferrer, S. & Regue, M. ( 1997; ). Genetic analysis of the chitinase system of Serratia marcescens 2170. J Bacteriol 179, 7111–7117.
    [Google Scholar]
  70. Watson, B., Currier, T. C., Gordon, M. P., Chilton, M. D. & Nester, E. W. ( 1975; ). Plasmid required for virulence of Agrobacterium tumefaciens. J Bacteriol 123, 255–264.
    [Google Scholar]
  71. Welch, M., Todd, D. E., Whitehead, N. A., McGowan, S. J., Bycroft, B. W. & Salmond, G. P. ( 2000; ). N-Acyl homoserine lactone binding to the CarR receptor determines quorum-sensing specificity in Erwinia. EMBO J 19, 631–641.[CrossRef]
    [Google Scholar]
  72. Whitehead, N. A., Barnard, A. M., Slater, H., Simpson, N. J. & Salmond, G. P. ( 2001; ). Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25, 365–404.[CrossRef]
    [Google Scholar]
  73. Whiteley, M., Lee, K. M. & Greenberg, E. P. ( 1999; ). Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 96, 13904–13909.[CrossRef]
    [Google Scholar]
  74. Winson, M. K., Bainton, N. J., Chhabra, S. R., Bycroft, B. W., Salmond, G. P., Williams, P. & Stewart, G. S. A. B. ( 1994; ). Control of N-acyl homoserine lactone-regulated expression of multiple phenotypes in Chromobacterium violaceum. In Abstracts of the 94th General Meeting of the American Society for Microbiology 1994, abstract H-71, p. 212. Washington, DC: American Society for Microbiology.
  75. Winson, M. K., Camara, M., Latifi, A. & 7 other authors ( 1995; ). Multiple N-acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 92, 9427–9431.[CrossRef]
    [Google Scholar]
  76. Winson, M. K., Swift, S., Fish, L., Throup, J. P., Jorgensen, F., Chhabra, S. R., Bycroft, B. W., Williams, P. & Stewart, G. S. ( 1998; ). Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol Lett 163, 185–192.[CrossRef]
    [Google Scholar]
  77. Zhang, L., Murphy, P. J., Kerr, A. & Tate, M. E. ( 1993; ). Agrobacterium conjugation and gene regulation by N-acyl-l-homoserine lactones. Nature 362, 446–448.[CrossRef]
    [Google Scholar]
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