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
2020-06-01
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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 Bacteriol177:6381–6389
    [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 Bacteriol179:4754–4760
    [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 Microbiol67:575–585
    [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 Microbiol33:1267–1277
    [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 Bacteriol180:3062–3069
    [Google Scholar]
  6. Ayora S., Gotz F. 1994; Genetic and biochemical properties of an extracellular neutral metalloprotease from Staphylococcus hyicus subsp. hyicus. Mol Gen Genet242:421–430
    [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 Bacteriol177:5000–5008
    [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 A95:7687–7692
    [Google Scholar]
  9. Bertani G. 1951; Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol62:293–300
    [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. Gene192:7–11
    [Google Scholar]
  11. Blum H, Beier H., Gross H. J. 1987; Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis8:93–99
    [Google Scholar]
  12. Borch E, Kant-Muermans M. L., Blixt Y. 1996; Bacterial spoilage of meat and cured meat products. Int J Food Microbiol33:103–120
    [Google Scholar]
  13. Bucher G. E. 1960; Potential bacterial pathogens of insects and their characteristics. J Insect Pathol2:172–195
    [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. Microbiology146:3149–3155
    [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 Interact11:1119–1129
    [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 Sci29:754–758
    [Google Scholar]
  17. Clark J. D., Maaloe O. 1967; DNA replication and the division cycle in Escherichia coli. J Mol Biol23:99–112
    [Google Scholar]
  18. Costerton J. W, Stewart P. S., Greenberg E. P. 1999; Bacterial biofilms: a common cause of persistent infections. Science284:1318–1322
    [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. Science280:295–298
    [Google Scholar]
  20. De Lorenzo V, Herrero M, Jakubzik U., Timmis K. N. 1990; Mini-Tn 5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in Gram-negative eubacteria. J Bacteriol172:6568–6572
    [Google Scholar]
  21. Dunlap P. V. 1999; Quorum regulation of luminescence in Vibrio fischeri. J Mol Microbiol Biotechnol1:5–12
    [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 Microbiol20:127–136
    [Google Scholar]
  23. Engebrecht J., Silverman M. 1984; Identification of genes and gene products necessary for bacterial bioluminescence. Proc Natl Acad Sci U S A81:4154–4158
    [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 Genet35:439–468
    [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 Lett160:151–158
    [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 Microbiol15:445–454
    [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 Bacteriol178:6618–6622
    [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 Bacteriol180:742–745
    [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. Electrophoresis21:1037–1053
    [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 Microbiol65:3458–3463
    [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. Microbiology146:2495–2508
    [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-Tn 5 delivery system. Gene186:167–173
    [Google Scholar]
  33. Herrera-Estrella A., Chet I. 1999; Chitinases in biological control. EXS87:171–184
    [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 Bacteriol172:6557–6567
    [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 Microbiol45:1655–1671
    [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. Microbiology147:2517–2528
    [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 J12:2477–2482
    [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 Microbiol89:920–934
    [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 Res151:433–439
    [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 Microbiol27:941–952
    [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 Genet233:293–301
    [Google Scholar]
  42. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685
    [Google Scholar]
  43. Lane D. J. 1991; 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics pp115–175 Edited by Stackebrandt E., Goodfellow M.. London: Wiley;
    [Google Scholar]
  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 Microbiol17:333–343
    [Google Scholar]
  45. Liao C. H. 1989; Analysis of pectate lyases produced by soft rot bacteria associated with spoilage of vegetables. Appl Environ Microbiol55:1677–1683
    [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 Microbiol39:11–17
    [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 Bacteriol180:6384–6388
    [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 of N -acylhomoserine lactones. Microbiology143:3703–3711
    [Google Scholar]
  49. Miller M. B., Bassler B. L. 2001; Quorum sensing in bacteria. Annu Rev Microbiol55:165–199
    [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 Microbiol44:1625–1635
    [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 Res14:5843–5855
    [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 Microbiol39:155–166
    [Google Scholar]
  53. Payens T. A. 1982; Stable and unstable casein micelles. J Dairy Sci65:1863–1873
    [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 A91:197–201
    [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. Nature362:448–450
    [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 J12:2467–2476
    [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 Methods44:239–251
    [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 Bacteriol183:1805–1809
    [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 Microbiol16:615–624
    [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;
    [Google Scholar]
  61. Sitnikov D. M, Schineller J. B., Baldwin T. O. 1995; Transcriptional regulation of bioluminescence genes from Vibrio fischeri. Mol Microbiol17:801–812
    [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 Microbiol63:2884–2896
    [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 Microbiol10:511–520
    [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 pp291–314 Edited by Dunny G. M., Winans S. C.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  65. Tan Y., Miller K. J. 1992; Cloning, expression, and nucleotide sequence of a lipase gene from Pseudomonas fluorescens B52. Appl Environ Microbiol58:1402–1407
    [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 Bacteriol180:6450–6458
    [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 Microbiol36:539–556
    [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 Microbiol17:345–356
    [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 Bacteriol179:7111–7117
    [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 Bacteriol123:255–264
    [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 J19:631–641
    [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 Rev25:365–404
    [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 A96:13904–13909
    [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 p212 Washington, DC: American Society for Microbiology;
    [Google Scholar]
  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 A92:9427–9431
    [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 Lett163:185–192
    [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. Nature362:446–448
    [Google Scholar]
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