Growth of Salmonella enteritidis and Salmonella typhimurium in the presence of quorum sensing signalling compounds produced by spoilage and pathogenic bacteria

Food Microbiology

Volumn 28, Issue 5, 2011, Pages 1011-1018

  Dourou, Dimitra ^a,b   Ammor, Mohammed Salim ^a,c   Skandamis, Panagiotis N ^a   Nychas, George John E ^a  

^a AGRICULTURAL UNIVERSITY OF ATHENS   (Greece)

^b CRANFIELD UNIVERSITY   (United Kingdom)

^c TOTAL   (France)

Author keywords

Acylated homoserine lactones; Autoinducer 2; Conductance; Quorum sensing; Salmonella enterica; Spoilage

Indexed keywords

DRUG DERIVATIVE; GAMMA BUTYROLACTONE; HOMOSERINE; HOMOSERINE LACTONE; LACTONE; N OCTANOYLHOMOSERINE LACTONE; N-OCTANOYLHOMOSERINE LACTONE;

ARTICLE; BACTERIUM; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; QUORUM SENSING; SALMONELLA ENTERITIDIS; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION;

4-BUTYROLACTONE; BACTERIA; HOMOSERINE; LACTONES; QUORUM SENSING; SALMONELLA ENTERITIDIS; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS; SALMONELLA TYPHIMURIUM; SERRATIA; SERRATIA PROTEAMACULANS; YERSINIA ENTEROCOLITICA;

EID: 79955875994     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2011.02.004     Document Type: Article

References (59)

1. Ammor M.S., Michaelidis C., Nychas G.-J.E. Insights into the role of quorum sensing in food spoilage. J. Food Prot. 2008, 71:1510-1525.
2. Atkinson S., Sockett R.E., Camara M., Williams P. Quorum sensing and the lifestyle of Yersinia. Curr. Issues Mol. Biol. 2006, 8:1-10.
3. Baranyi J., Roberts T.A. A dynamic approach to predicting bacterial growth in food. Int. J. Food Microbiol. 1994, 23:277-294.
4. Bertani G. Studies on lysogenesis. The mode of phage liberation by lysogenic Escherichia coli. J. Bacteriol. 1951, 62:293-300.
5. Bruhn J.B., Christensen A.B., Flodgaard L.R., Nielsen K.F., Larsen T.O., Givskov M., Gram L. Presence of acylated homoserine lactones (AHLs) and AHL-producing bacteria in meat and potential role of AHL in spoilage of meat. Appl. Environ. Microbiol. 2004, 70:4293-4302.
6. Chorianopoulos N., Giaouris E., Kourkoutas I., Nychas G.-J.E. Early stages of biofilm development by Salmonella Enteritidis on stainless steel are inhibited by the cell-free culture supernatant of Hafnia alvei. Appl. Environ. Microbiol. 2010, 76:2018-2022.
7. Chorianopoulos N., Giaouris E., Skandamis P., Xaroutounian S., Nychas G.-J.E. Disinfectant test against monoculture and mixed-culture biofilms composed of technological, spoilage and pathogenic bacteria: bactericidal effect of essential oil and hydrosol of Satureja thymbra and comparison with standard acid-base sanitizers. J. Appl. Microbiol. 2008, 104:1586-1596.
8. Chorianopoulos N.G., Lambert R.J.W., Skandamis P.N., Evergetis E.T., Haroutounian S.A., Nychas G.-J.E. A newly developed assay to study the minimum inhibitory concentration of Satureja spinosa essential oil. J. Appl. Microbiol. 2006, 100:778-786.
9. Christensen A.B., Riedel K., Eberl L., Flodgaard L.R., Molin S., Gram L., Givskov M. Quorum-sensing-directed protein expression in Serratia proteamaculans B5a. Microbiology 2003, 149:471-483.
10. Dunstall G., Rowe M.T., Wisdom G.B., Kilpatrick D. Effect of quorum sensing agents on the growth kinetics of Pseudomonas spp. of raw milk origin. J. Dairy Res. 2005, 72:276-280.
11. The Community summary report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and foodborne outbreaks in the European Union in 2006. EFSA J. 2007, 130:2-352. EFSA-ECDC.
12. Federle M.J., Bassler B.L. Interspecies communication in bacteria. J. Clin. Invest. 2003, 112:1291-1299.
13. Firstenberg-Eden R., Eden G. Impedance Microbiology 1984, Research Studies Press Ltd, Letchworth, England.
14. Fuqua C., Winans S.C. Conserved cis-acting promoter elements are required for density-dependent transcription of Agrobacterium tumefaciens conjugal transfer genes. J. Bacteriol. 1996, 178:435-440.
15. Giaouris E., Chorianopoulos N., Nychas G.-J.E. Effect of temperature, pH, and water activity on biofilm formation by Salmonella enterica Enteritidis PT4 on stainless steel surfaces as indicated by the bead vortexing method and conductance measurements. J. Food Prot. 2005, 68:2149-2154.
16. 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. 1999, 65:3458-3463.
17. Greenberg E.P., Hastings J.W., Ulitzur S. Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch. Microbiol. 1979, 120:87-91.
18. Hense B.A., Kuttler C., Müller J., Rothballer M., Hartmann A., Kreft J.-U. Does efficiency sensing unify diffusion and quorum sensing?. Nat. Rev. Microbiol. 2007, 5:230-239.
19. Hughes D.T., Sperandio V. Inter-kingdom signalling: communication between bacteria and their hosts. Nat. Rev. Microbiol. 2008, 6:111-120.
20. Keller L., Surette M. Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol. 2006, 4:249-258.
21. Kendall M.M., Sperandio V. Quorum sensing by enteric pathogens. Curr. Opin. Gastroenterol. 2007, 23:10-15.
22. Kolling G.L., Matthews K.R. Influence of enteric bacteria conditioned media on recovery of Escherichia coli O157:H7 exposed to starvation and sodium hypochlorite. J. Appl. Microbiol. 2007, 103:1435-1441.
23. Koutsoumanis K., Giannakourou M., Taoukis P.S., Nychas G.-J.E. Application of SLDs (Shelf life Decision System) to marine cultured fish quality. Int. J. Food Microbiol. 2002, 73:375-382.
24. Koutsoumanis K., Nychas G.-J.E. Application of a systematic experimental procedure to develop a microbial model for rapid fish shelf life predictions. Int. J. Food Microbiol. 2000, 60:171-184.
25. Koutsoumanis K., Tassou C.C., Taoukis P., Nychas G.-J.E. Modelling the effectiveness of a natural antimicrobial on Salmonella enteritidis as a function of concentration, temperature and pH, using conductance measurements. J. Appl. Microbiol. 1998, 84:911-918.
26. Lambert R.J.W., Pearson J. Susceptibility testing: accurate and reproducible minimum inhibitory concentration (MIC) and non-inhibitory concentration (NIC) values. J. Appl. Microbiol. 2000, 88:784-790.
27. Lu L., Hume M.E., Pillai S.D. Autoinducer-2-like activity associated with foods and its interaction with food additives. J. Food Prot. 2004, 67:1457-1462.
28. Lynch M., Painter J., Woodruff R., Braden C. Surveillance for foodborne-disease outbreaks-United States, 1998-2002. MMWR Surveill. Summ. 2006, 55:1-42.
29. Michael B., Smith J.N., Swift S., Heffron F., Ahmer B.M. SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J. Bacteriol. 2001, 183:5733-5742.
30. Miller M.B., Bassler B.L. Quorum sensing in bacteria. Annu. Rev. Microbiol. 2001, 55:165-199.
31. Nychas G.-J.E., Dourou D., Skandamis P., Koutsoumanis K., Baranyi J., Sofos J. Effect of microbial cell-free meat extract on the growth rate of spoilage bacteria. J. Appl. Bacteriol. 2009, 107:1819-1829.
32. 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. U S A 1994, 91:197-201.
33. Pearson J.P., Passador L., Iglewski B.H., Greenberg E.P. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U S A 1995, 92:1490-1494.
34. Rantsiou K., Drosinos E.H., Gialitaki M., Metaxopoulos I., Comi G., Cocolin L. Use of molecular tools to characterize Lactobacillus spp. isolated from Greek traditional fermented sausages. Int. J. Food Microbiol. 2006, 112:215-222.
35. Ravn L., Christensen A.B., Moli 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. Methods 2001, 44:239-251.
36. Redfield R.J. Is quorum sensing a side effect of diffusion sensing?. Trends Microbiol. 2002, 10:365-370.
37. Richard J.C.S., Jason A.C., Hobbs G., Gibson D.M., Christie R.H. Electronic measurement of bacterial growth. J. Phys. E: Scient. Instr. 1978, 11:560-568.
38. Schauder S., Bassler B.L. The language of bacteria. Genes Dev. 2001, 15:1468-1480.
39. Shaw P.D., Ping G., Daly S.L., Cha C., Cronan J.E., Rinehart K.L., Farrand S.K. Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc. Natl. Acad. Sci. U S A 1997, 94:6036-6041.
40. Silley P., Forsythe S. Impedance microbiology-a rapid change for microbiologists. J. Appl. Bacteriol. 1996, 80:233-243.
41. Smith J.L., Fratamico P.M., Novak J.S. Quorum sensing: a primer for food microbiologists. J. Food Prot. 2004, 67:1053-1070.
42. Smith J.N., Ahmer B.M. Detection of other microbial species by Salmonella: expression of the SdiA regulon. J. Bacteriol. 2003, 185:1357-1366.
43. Skandamis P., Koutsoumanis K., Fasseas K., Nychas G.-J.E. Evaluation of the inhibitory effect of oregano essential oil on Escherichia coli O157:H7, in broth culture with or without EDTA, using viable counts, turbidity and impedance. Ital. J. Food Sc. Technol. 2001, 13:65-75.
44. Soni K.A., Lu L., Jesudhasan P.R., Hume M.E., Pillai S.D. Influence of autoinducer-2 (AI-2) and beef sample extracts on E.coli O157:H7 survival and gene expression of virulence genes yadk and hhA. J. Food Sci. 2008, 73:135-139.
45. Stephens K. Pheromones among the prokaryotes. Crit. Rev. Microbiol. 1986, 13:309-334.
46. Surette M.G., Bassler B.L. Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc. Natl. Acad. Sci. U S A 1998, 95:7046-7050.
47. Surette M.G., Miller M.B., Bassler B.L. Quorum sensing in Escherichia coli, Salmonella typhimurium and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc. Natl. Acad. Sci. U S A 1999, 96:1639-1644.
48. Taga M.E., Miller S.T., Bassler B.L. Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium. Mol. Microbiol. 2003, 50:1411-1427.
49. Taga M.E., Semmelhack J.L., Bassler B.L. The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium. Mol. Microbiol. 2001, 42:777-793.
50. Tassou C.C., Nychas G.-J.E. Inhibition of Staphylococcus aureus by olive phenolics in broth and in food model system. J. Food Prot. 1994, 57:120-124.
51. Tassou C.C., Nychas G.-J.E. Inhibition of Salmonella enteritidis by oleuropein in broth and in a model food system. Lett. Appl. Microbiol. 1995, 20:120-124.
52. Throup J.P., Camara M., Briggs G.S., Winson M.K., Chhabra S.R., Bycroft B.W., Williams P., Stewart G.S. Characterisation of the yenI/yenR locus from Yersinia enterocolitica mediating the synthesis of two N-acylhomoserine lactone signal molecules. Mol. Microbiol. 1995, 17:345-356.
53. Tranter H.S., Tassou C.C., Nychas G.-J.E. The effect of the olive phenolic compound, oleuropein, on growth and enterotoxin B production by Staphylococcus aureus. J. Appl. Bacteriol. 1993, 74:253-259.
54. Van Houdt R., Givskov M., Michiels C.W. Quorum sensing in Serratia. FEMS Microbiol. Rev. 2007, 31:407-424.
55. Walters M., Sircili M.P., Sperandio V. AI-3 synthesis is not dependent on luxS in Escherichia coli. J. Bacteriol. 2006, 188:5668-5681.
56. Walters M., Sperandio V. Quorum sensing in Escherichia coli and Salmonella. Int. J. Food Microbiol. 2006, 296:125-131.
57. Whan L., Dunstall G., Rowe M.T. A study of the growth kinetics of two pseudomonads from pasteurized milk and the possible role of quorum sensing. Milchwissenschaft 2000, 55:371-373.
58. Winzer K., Hardie K.R., Burgess N., Doherty N., Kirke D., Holden M.T., Linforth R., Cornell K.A., Taylor A.J., Hill P.J., Williams P. LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone. Microbiology 2002, 148:909-922.
59. Zhao A.L., Montville T.J., Schaffner D.W. Evidence for quorum sensing in Clostridium botulinum. Lett. Appl. Microbiol. 2006, 42:54-58.