Development of stress resistance in Staphylococcus aureus after exposure to sublethal environmental conditions

International Journal of Food Microbiology

Volumn 140, Issue 1, 2010, Pages 26-33

  Cebrián, G ^a   Sagarzazu, N ^a   Pagán, R ^a   Condón, S ^a   Mañas, P ^a  

^a UNIVERSIDAD DE ZARAGOZA   (Spain)

Author keywords

Cross protection; Extreme pHs; Heat resistance; Hydrogen peroxide; Staphylococcus aureus; Stress response

Indexed keywords

CHLORAMPHENICOL; HYDROGEN PEROXIDE; RIFAMPICIN;

ADAPTATION; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; CONTROLLED STUDY; CROSS PROTECTION; CROSS RESISTANCE; ENVIRONMENTAL STRESS; FOOD CONTROL; FOOD PROCESSING; HEAT TOLERANCE; INDUCED RESISTANCE; NONHUMAN; PH; STAPHYLOCOCCUS AUREUS;

ACIDS; ADAPTATION, PHYSIOLOGICAL; ANTI-BACTERIAL AGENTS; CHLORAMPHENICOL; FOOD HANDLING; HOT TEMPERATURE; HYDROGEN PEROXIDE; HYDROGEN-ION CONCENTRATION; RIFAMPIN; STAPHYLOCOCCUS AUREUS; STRESS, PHYSIOLOGICAL; TIME FACTORS;

STAPHYLOCOCCUS AUREUS;

EID: 77952259009     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2010.02.017     Document Type: Article

References (71)

1. Abee T., Wouters J.A. Microbial stress response in minimal processing. International Journal of Food Microbiology 1999, 50:65-91.
2. Baranyi J., Roberts T.A. A dynamic approach to predicting bacterial-growth in food. International Journal of Food Microbiology 1994, 23:277-294.
3. Baranyi J., Jones A., Walker C., Kaloti A., Robinson T.P., Mackey B.M. A combined model for growth and subsequent thermal inactivation of Brochothrix thermosphacta. Applied and Environmental Microbiology 1996, 62:1029-1035.
4. Booth I.R. Stress and the single cell: intrapopulation diversity is a mechanism to ensure survival upon exposure to stress. International Journal of Food Microbiology 2002, 78:19-30.
5. Bore E., Langsrud S., Langsrud O., Rode T.M., Holck A. Acid-shock responses in Staphylococcus aureus investigated by global gene expression analysis. Microbiology 2007, 153:2289-2303.
6. Bremer E., Krämer R. Coping with osmotic challenges: osmoregulation through accumulation and release of compatible solutes in bacteria. Bacterial Stress Responses 2000, 79-97. ASM Press, Washington, D.C. G. Storz, R. Hengge-Aronis (Eds.).
7. B on Staphylococcus aureus resistance to stresses of relevance to food preservation. Journal of Applied Microbiology 2009, 107:187-196.
8. Condón S., Arrizubieta M.J., Sala F.J. Microbial heat resistance determinations by the multipoint system with the thermoresistometer TR-SC. Journal of Microbiological Methods 1993, 18:357-366.
9. Condón S., Palop A., Raso J., Sala F.J. Influence of the incubation temperature after heat treatment upon the estimated heat resistance values of spores of Bacillus subtilis. Letters in Applied Microbiology 1996, 22:149-152.
10. Craig E.A. The heat shock response. CRC Critical Reviews in Biochemistry 1985, 18:239-280.
11. Davis M.J., Coote P.J., O'Byrne C.P. Acid tolerance in Listeria monocytogenes: the adaptive acid tolerance response (ATR) and growth phase-dependent acid resistance. Microbiology 1996, 142:2975-2982.
12. De Angelis M., Gobbetti M. Environmental stress responses in Lactobacillus: a review. Proteomics 2004, 4:106-122.
13. De Angelis M., Di Cagno R., Huet C., Crecchio C., Fox P.F., Gobbetti M. Heat shock response in Lactobacillus plantarum. Applied and Environmental Microbiology 2004, 70:1336-1346.
14. Demple B., Halbrook J. Inducible repair of oxidative DNA damage in Escherichia coli. Nature 1983, 304:466-468.
15. Duffy G., Riordan D.C., Sheridan J.J., Call J.E., Whiting R.C., Blair I.S., McDowell D.A. Effect of pH on survival, thermotolerance, and verotoxin production of Escherichia coli O157:H7 during simulated fermentation and storage. Journal of Food Protection 2000, 63:12-18.
16. Faleiro M.L., Andrew P.W., Power D. Stress response of Listeria monocytogenes isolated from cheese and other foods. International Journal of Food Microbiology 2003, 84:207-216.
17. Farber J.M., Pagotto F. The effect of acid shock on the resistance of Listeria monocytogenes. Letters in Applied Microbiology 1992, 15:197-201.
18. Flahaut S., Hartke A., Giard J.C., Benachour A., Boutibonnes P., Auffray Y. Relationship between stress response toward bile salts, acid and heat treatment in Enterococcus faecalis. FEMS Microbiology Letters 1996, 138:49-54.
19. Flahaut S., Hartke A., Giard J.C., Auffray Y. Alkaline stress response in Enterococcus faecalis: adaptation, cross-protection, and changes in protein synthesis. Applied and Environmental Microbiology 1997, 63:812-814.
20. 2 stress proteins. Letters in Applied Microbiology 1998, 26:259-264.
21. Foster J.W. Salmonella acid shock proteins are required for the adaptive acid tolerance response. Journal of Bacteriology 1991, 173:6896-6902.
22. Foster J.W. The acid tolerance response of Salmonella typhimurium involves transient synthesis of key acid shock proteins. Journal of Bacteriology 1993, 175:1981-1987.
23. Foster J.W., Hall H.K. Adaptative acidification tolerance responses of Salmonella typhimurium. Journal of Bacteriology 1990, 172:771-778.
24. Foster J.W., Hall H.K. Inducible pH homeostasis and the acid tolerance response of Salmonella thyphimurium. Journal of Bacteriology 1991, 173:5129-5135.
25. Goodson M., Rowbury R.J. Habituation to normally lethal acidity by prior growth of Escherichia coli at a sub-lethal acid pH value. Letters in Applied Microbiology 1989, 8:77-79.
26. Hartke A., Bouché S., Giard J.C., Benachour A., Boutibonnes P., Auffray Y. The lactic acid stress response of Lactococcus lactis subsp. lactis. Current Microbiology 1996, 33:194-199.
27. Hassani M., Cebrián G., Mañas P., Condón S., Pagán R. Induced thermotolerance under nonisothermal treatments of a heat sensitive and a resistant strain of Staphylococcus aureus in media of different pH. Letters in Applied Microbiology 2006, 43:619-624.
28. Hassani M., Mañas P., Condón S., Pagán R. Predicting heat inactivation of Staphylococcus aureus under nonisothermal treatments at different pH. Molecular Nutrition and Food Research 2007, 50:572-580.
29. Hecker M., Schumann W., Völker U. Heat-shock and general stress response in Bacillus subtilis. Molecular Microbiology 1996, 3:417-428.
30. Helmann J.D., Wu M.F.W., Gaballa A., Kobel P.A., Morshedi M.M., Fawcett P., Paddon C. The global transcriptional response of Bacillus subtilis to peroxide stress is coordinated by three transcription factors. Journal of Bacteriology 2003, 185:243-253.
31. Hill C., Cotter P.D., Sleator R.D., Gahan C.G.M. Bacterial stress response in Listeria monocytogenes: jumping the hurdles imposed by minimal processing. International Dairy Journal 2002, 12:273-283.
32. Horsburgh M.J., Clements M.O., Crossley H., Ingham E., Foster S.J. PerR controls oxidative stress resistance and iron storage proteins and is required for virulence in Staphylococcus aureus. Infection and Immunity 2001, 3744-3754.
33. Humphrey T.J., Richardson N.P., Statton K.M., Rowbury R.J. Effects of temperature shift on acid and heat tolerance in Salmonella enteritidis phage type 4. Applied and Environmental Microbiology 1993, 59:3120-3122.
34. Isonhood J.H., Gerard P.D., Leenanon B., Drake M.A. Stress responses of Aeromonas hydrophila following environmental challenges. Food Microbiology 2002, 19:285-293.
35. Juneja V.K., Klein P.G., Marmer B.S. Heat Shock and thermotolerance of Escherichia coli O157:H7 in a model beef gravy system and ground beef. Journal of Applied Microbiology 1998, 84:677-684.
36. Katsui N., Tsuchido T., Takano N., Shibasaki I. Viability of heat stressed cells of microorganisms as influenced by pre-incubation and post-incubation temperatures. Journal of Applied Bacteriology 1982, 53:103-108.
37. Koutsoumanis K.P., Sofos J.N. Comparative acid stress response of Listeria monocytogenes, Escherichia coli O157:H7 and Salmonella Typhimurium after habituation at different pH conditions. Letters in Applied Microbiology 2004, 38:321-326.
38. B in Staphylococcus aureus reveals its function as a global regulator of virulence genes. Journal of Bacteriology 1998, 180:4814-4820.
39. S (RpoS) is required for a sustained acid tolerance response in virulent Salmonella typhimurium. Molecular Microbiology 1995, 17:155-167.
40. Leistner L. Basic aspects of food preservation by hurdle technology. International Journal of Food Microbiology 2000, 55:181-186.
41. Leyer G.J., Johnson E.A. Acid adaptation promotes survival of Salmonella sp. in cheese. Applied and Environmental Microbiology 1992, 58:2075-2080.
42. Leyer G.J., Johnson E.A. Acid adaptation induces cross-protection against environmental stresses in Salmonella typhimurium. Applied and Environmental Microbiology 1993, 59:1842-1847.
43. Leyer G.J., Wang L.L., Johnson E.A. Acid adaptation of Escherichia coli O157:H7 increases survival in acidic foods. Applied and Environmental Microbiology 1995, 61:3752-3755.
44. Lindquist S. The heat-shock response. Annual Reviews in Biochemistry 1986, 55:1151-1191.
45. Linton R.H., Pierson M.D., Bishop J.R. Increase in heat resistance of Listeria monocytogenes Scott A by sublethal heat shock. Journal of Food Protection 1990, 53:924-927.
46. Lou Y., Yousef A.E. Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Applied and Environmental Microbiology 1997, 63:1252-1255.
47. Mackey B.M., Derrick C.M. Elevation of the heat resistance of Salmonella typhimurium by sub-lethal heat shock. Journal of Applied Bacteriology 1986, 61:389-393.
48. Mackey B.M., Derrick C.M. Changes in the heat resistance of Salmonella typhimurium during heating at rising temperatures. Letters in Applied Microbiology 1987, 4:13-16.
49. Mackey B.M., Derrick C.M. The effect of prior shock on the thermoresistance of Salmonella thompson in foods. Letters in Applied Microbiology 1987, 5:115-118.
50. Mañas P., Pagán R., Sala F.J., Condón S. Low molecular weight milk whey components protect Salmonella senftenberg 775W against heat by mechanism involving divalent cations. Journal of Applied Microbiology 2001, 91:871-877.
51. McMahon C.M., Byrne C.M., Sheridan J.J., McDowell D.A., Blair I.S., Hegarty T. The effect of culture growth phase on induction of the heat shock response in Yersinia enterocolitica and Listeria monocytogenes. Journal of Applied Microbiology 2000, 89:198-206.
52. Mongkolsuk S., Helmann J.D. Regulation of inducible peroxide stress responses. Molecular Microbiology 2002, 45:9-15.
53. Murphy P., Dowd B.C., McConell D.J., Devine K.M. Oxidative stress and growth temperature in Bacillus subtilis. Journal of Bacteriology 1987, 169:5766-5770.
54. O'Driscoll B., Gahan C.G., Hill C. Two-dimensional polyacrylamide gel electrophoresis analysis of the acid tolerance response in Listeria monocytogenes LO28. Applied and Environmental Microbiology 1997, 63:2679-2685.
55. Pagán R., Condón S., Sala F.J. Effects of several factors on the heat-shock-induced thermotolerance of Listeria monocytogenes. Applied and Environmental Microbiology 1997, 63:3225-3232.
56. B regulon in Staphylococcus aureus and its regulation. International Journal of Medical Microbiology 2006, 296:237-258.
57. Rowbury R.J. An assessment of environmental factors influencing acid tolerance and sensitivity in Escherichia coli, Salmonella spp. and other enterobacteria. Letters in Applied Microbiology 1995, 20:333-337.
58. Rowbury R.J., Goodson M., Humphrey T.J. Acid sensitivity induction (ASI) at alkaline pH in Escherichia coli involves two major sensitization components, induction of both being switched on by increased internal pH. Letters in Applied Microbiology 1993, 17:272-275.
59. Rowbury R.J., Lazim Z., Goodson M. Regulatory aspects of alkali tolerance induction in Escherichia coli. Letters in Applied Microbiology 1996, 22:429-432.
60. Ryu J.-H., Beuchat L.R. Influence of acid tolerance responses on survival, growth, and cross-protection of Escherichia coli O157:H7 in acidified media and fruit juices. International Journal of Food Microbiology 1998, 45:185-193.
61. Sanders J.-W., Venema G., Kok J. Environmental stress response in Lactococcus lactis. FEMS Microbiology Reviews 1999, 23:483-501.
62. Shenoy K., Murano E.A. Effect of heat shock on the thermotolerance and protein composition of Yersinia enterocolitica in brain heart infusion broth and ground pork. Journal of Food Protection 1996, 59:360-364.
63. Singh V.K., Utaida S., Jackson L.S., Jayaswal R.K., Wilkinson B.J., Chamberlain N.R. Role for dnaK locus in tolerance of multiple stresses in Staphylococcus aureus. Microbiology 2007, 153:3162-3173.
64. Storz G., Hengge-Aronis R. Bacterial Stress Responses 2000, AMS Press, Washington D.C.
65. Storz G., Zheng M. Oxidative stress. Bacterial Stress Responses 2000, 47-59. AMS Press, Washington D.C. G. Storz, R. Hengge-Aronis (Eds.).
66. Taglicht D., Padan E., Oppenheim A.B., Schuldiner S. An alkaline shift induces the heat shock response in Escherichia coli. Journal of Bacteriology 1987, 169:885-887.
67. VanBogelen R.A., Acton M.A., Neidhardt F.C. Induction of the heat shock regulon does not produce thermotolerance in Escherichia coli. Genes and Development 1987, 1:525-531.
68. Wang G., Doyle M.P. Heat shock enhances acid tolerance in Escherichia coli O157:H7. Letters in Applied Microbiology 1998, 26:31-34.
69. Welin J., Wilkins J.C., Beighton D., Wrzesinski K., Fey S.J., Mose-Larsen P., Hamilton I.R., Svensäter G. Effect of acid shock on protein expression by biofilm cells of Streptococcus mutans. FEMS Microbiology Letters 2003, 227:287-293.
70. 2 by catalase induction in Salmonella typhimurium. Mutation Research 1984, 141:145-147.
71. Yura T., Kanemori M., Morita M.T. The heat shock response: regulation and function. Bacterial Stress Responses 2000, 3-18. ASM Press, Washington D.C. G. Storz, R. Hengge-Aronis (Eds.).