Relationship between membrane fatty acid composition and heat resistance of acid and cold stressed Salmonella senftenberg CECT 4384

Food Microbiology

Volumn 26, Issue 3, 2009, Pages 347-353

  Álvarez Ordóñez, Avelino ^a   Fernández, Ana ^a   López, Mercedes ^a   Bernardo, Ana ^a  

^a UNIVERSITY OF LEÓN   (Spain)

Author keywords

Acid adaptation; Cold stress; Food safety; Heat resistance; Membrane fatty acids; Membrane fluidity; Salmonella senftenberg

Indexed keywords

FATTY ACID; MEMBRANE LIPID;

ADAPTATION; ARTICLE; BACTERIAL COUNT; CHEMISTRY; CULTURE MEDIUM; FOOD CONTROL; FREEZING; GROWTH, DEVELOPMENT AND AGING; HEAT; MEMBRANE FLUIDITY; PH; PHYSIOLOGY; SAFETY; SALMONELLA; SALMONELLA FOOD POISONING; SENSITIVITY AND SPECIFICITY;

ADAPTATION, PHYSIOLOGICAL; COLONY COUNT, MICROBIAL; CONSUMER PRODUCT SAFETY; CULTURE MEDIA; FATTY ACIDS; FOOD MICROBIOLOGY; HOT TEMPERATURE; HYDROGEN-ION CONCENTRATION; MEMBRANE FLUIDITY; MEMBRANE LIPIDS; REFRIGERATION; SALMONELLA; SALMONELLA FOOD POISONING; SENSITIVITY AND SPECIFICITY;

BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR SENFTENBERG;

EID: 61449200379     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2008.11.002     Document Type: Article

References (62)

1. Álvarez-Ordóñez A., Fernández A., López M., Arenas R., and Bernardo A. Modifications in membrane fatty acid composition of Salmonella typhimurium in response to growth conditions and their effect on heat resistance. Int. J. Food Microbiol. 123 (2008) 212-219
2. Álvarez-Ordóñez A., Fernández A., Bernardo A., and López M. Comparison of acids on the induction of an acid tolerance response in Salmonella typhimurium, consequences for food safety. Meat Sci. 81 (2009) 65-70
3. Annous B.A., and Kozempel M.F. Influence of growth medium on thermal resistance of Pediococcus sp. strain NRRL B-2354 (formerly Micrococcus freudenreichii) in liquid foods. J. Food Prot. 61 (1998) 578-581
4. Annous B.A., Kozempel M.F., and Kurantz M.J. Changes in membrane fatty acid composition of Pediococcus sp. strain NRRL B-2354 in response to growth conditions and its effect on thermal resistance. Appl. Environ. Microbiol. 65 (1999) 2857-2862
5. Bacon R.T., Ransom J.R., Sofos J.N., Kendall P.A., Belk K.E., and Smith G.C. Thermal inactivation of susceptible and multiantimicrobial-resistant Salmonella strains grown in the absence or presence of glucose. Appl. Environ. Microbiol. 69 (2003) 4123-4128
6. Bastianini A., Granchi S., Guerini S., and Vincenzini M. Fatty acid composition of malolactic Oenococcus oeni strains exposed to pH and ethanol stress. Ital. J. Food Sci. 12 (2000) 333-342
7. Bayles D.O., Tunick M.H., Foglia T.A., and Miller A.J. Cold shock and its effect on ribosomes and thermal tolerance in Listeria monocytogenes. Appl. Environ. Microbiol. 66 (2000) 4351-4355
8. Béal C., Fonseca F., and Corrieu G. Resistance to freezing and frozen storage of Streptococcus thermophilus is related to membrane fatty acid composition. J. Dairy Res. 84 (2001) 2347-2356
9. Bligh E.G., and Dyer W.J. A rapid method for total lipid extraction and purification. Can. J. Biochem. Physiol. 37 (1959) 911-917
10. Brown J.L., Ross T., McMeekin T.A., and Nichols P.D. Acid habituation of Escherichia coli and the potential role of cyclopropane fatty acids in low pH tolerance. Int. J. Food Microbiol. 37 (1997) 163-173
11. Buchanan R.L., Whiting R.C., and Damert W.C. When is simple good enough: a comparison of the Gompertz, Baranyi, and three-phase linear models for fitting bacterial growth curves. Food Microbiol. 14 (1997) 313-326
12. Buchanan R.L., and Edelson S.G. Effect of pH-dependent, stationary phase acid resistance on the thermal tolerance of E. coli O157:H7. Food Microbiol. 16 (1999) 447-458
13. Casadei M.A., Mañas P., Niven G., Needs E., and Mackey B.M. Role of membrane fluidity in pressure resistance of Escherichia coli NCTC 8164. Appl. Environ. Microbiol. 68 (2002) 5965-5972
14. Chang Y.Y., and Cronan J.E. Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol. Microbiol. 33 (1999) 249-259
15. Condón S., García M.L., Otero A., and Sala F.J. Effect of culture age, preincubation at low temperature and pH on the thermal resistance of Aeromonas hydrophila. J. Appl. Bacteriol. 72 (1992) 322-366
16. Condón S., Arrizubieta M.J., and Sala F.J. Microbial heat resistance determinations by the multipoint system with the thermoresistometer TR-SC. Improvement of this methodology. J. Microbiol. Methods 18 (1993) 357-366
17. D'Aoust J.Y. Salmonella. In: Lund B.M., Baird-Parker T.C., and Gould G.W. (Eds). The Microbiological Safety and Quality of Foods (2000), Aspen, Gaithersburg, Maryland, USA 1233-1299
18. Dodd C.E.R., and Aldsworth T.G. The importance of RpoS in the survival of bacteria through food processing. Int. J. Food Microbiol. 74 (2002) 189-194
19. Duffy G., Riordan D.C.R., Sheridan J.J., Call J.E., Whiting R.C., Blair I.S., and McDowell D.A. Effect of pH on survival, thermotolerance and verotoxin production of E. coli O157:H7 during simulated fermentation and storage. J. Food Prot. 63 (2000) 12-18
20. European Food Safety Authority (EFSA). Opinion of the scientific panel on biological hazards on the request from the commission related to "Risk assessment and mitigation options of Salmonella in pig production". The EFSA J. 341 (2006) 1-131
21. Evrendilek G.A., and Zhang Q.H. Effects of pH, temperature, and pre-pulsed electric field treatment on pulsed electric field and heat inactivation of Escherichia coli O157:H7. J. Food Prot. 66 (2003) 755-759
22. Farber J.M., and Pagotto F. The effect of acid shock on the heat resistance of Listeria monocytogenes. Lett. Appl. Microbiol. 15 (1992) 197-201
23. Fernández Murga M.L., Cabrera G., Font de Valdez A., Disalvo A., and Seldes A.M. Influence of growth temperature on cryotolerance and lipid composition of Lactobacillus acidophilus. J. Appl. Microbiol. 88 (2000) 342-348
24. Foster J.W., and Spector M.P. How Salmonella survive against the odds. Annu. Rev. Microbiol. 49 (1995) 145-174
25. Foster J.W. Microbial responses to acid stress. In: Storz G., and Hengge-Aronis R. (Eds). Bacterial Stress Responses (2000), ASM Press, Washington, DC 99-115
26. Gay M., and Cerf O. Significance of temperature and preincubation temperature on survival of Listeria monocytogenes at pH 4.8. Lett. Appl. Microbiol. 25 (1997) 257-260
27. Guillot A., Obis D., and Mistou M.Y. Fatty acid membrane composition and activation of glycine-betaine transport in Lactococcus lactis subjected to osmotic stress. Int. J. Food Microbiol. 55 (2000) 47-51
28. Humphrey T.J. Heat resistance in Salmonella enteritidis phage type PT4: the influence of storage temperatures before heating. J. Appl. Bacteriol. 69 (1990) 493-497
29. Ibarz, P., Palop, A., Condón, S., Sala, F.J., 1991. Adaptador de un contador automático de U.F.C. al recuento de placas densamente pobladas. In: Proceedings of the XIII Congreso Nacional de Microbiología, Salamanca, Spain, p. 159.
30. Ingham S.C., and Uljas H.E. Prior storage conditions influence the destruction of E. coli O157:H7 during heating of apple cider and juice. J. Food Prot. 61 (1998) 390-394
31. Jackson T.C., Hardin M.D., and Acuff G.R. Heat resistance of Escherichia coli O157:H7 in a nutrient medium and in ground beef patties as influenced by storage and holding temperature. J. Food Prot. 59 (1996) 230-237
32. Juneja V.K., Foglia T.A., and Marmer B.S. Heat resistance and fatty acid composition of Listeria monocytogenes: effect of pH, acidulant, and growth temperature. J. Food Prot. 61 (1998) 683-687
33. Kadner R.J. Cytoplasmic membrane. In: Neidhasdt F.C., Curtiss III R., Ingraham J.L., Lin E.C.C., Low K.B., Magasanik B., Reznikoff W.S., Riley M., Schaechter M., and Umbarger H.E. (Eds). Escherichia coli and Salmonella: Cellular and Molecular Biology (1996), ASM Press, Washington, DC 58-87
34. Katsui N., Tsuchido T., Takano M., and Shibasaki I. Effect of preincubation temperature on the heat resistance of Escherichia coli having different fatty acid compositions. J. Gen. Microbiol. 122 (1981) 357-361
35. Katsui N., Tsuchido T., Takano M., and Shibasaki I. Viability of heat-stressed cells of microorganisms as influenced by pre-incubation and post-incubation temperatures. J. Appl. Bacteriol. 53 (1982) 103-108
36. Kennedy J., Blair I.S., McDowell D.A., and Bolton D.J. An investigation of the thermal inactivation of Staphylococcus aureus and the potential for increased thermotolerance as a result of chilled storage. J. Appl. Microbiol. 99 (2005) 1229-1235
37. Kornacki J.L., and Marth E.H. Thermal inactivation of Staphylococcus aureus in retentates from ultrafiltered milk. J. Food Prot. 52 (1989) 631-637
38. Kumar A., and Kumar S. Survival kinetics of Salmonella enterica serotype senftenberg (S. senftenberg) after heat and acid stress. World J. Microbiol. Biotechnol. 19 (2003) 985-987
39. L'Ecuyer P.B., Diego J., Murphy D., Trovillion E., Jones M., Sahm D.F., and Fraser V.J. Nosocomial outbreak of gastroenteritis due to Salmonella senftenberg. Clin. Infect. Dis. 23 (1996) 734-742
40. Leyer G.J., and Johnson E.A. Acid adaptation induces cross-protection against environmental stresses in Salmonella typhimurium. Appl. Environ. Microbiol. 59 (1993) 1842-1847
41. Liebana E., Guns D., García-Migura L., Woodward M.J., Clifton-Hadley F.A., and Davies R.H. Molecular typing of Salmonella serotypes prevalent in animals in England: assessment of methodology. J. Clin. Microbiol. 39 (2001) 3609-3616
42. Lou Y., and Yousef A.E. Resistance of Listeria monocytogenes to heat after adaptation to environmental stresses. J. Food Prot. 59 (1996) 465-471
43. Magnuson K., Jackowski S., Rock C.O., and Cronan J.E. Regulation of fatty acid biosynthesis in Escherichia coli. Microbiol. Rev. 57 (1993) 522-542
44. Mañas P., Pagán R., Raso J., and Condón S. Predicting thermal inactivation in media of different pH of Salmonella grown at different temperatures. Int. J. Food Microbiol. 87 (2003) 45-53
45. Martínez S., López M., and Bernardo A. Thermal inactivation of Enterococcus faecium: effect of growth temperature and physiological state of microbial cells. Lett. Appl. Microbiol. 37 (2003) 475-481
46. Martínez-Urtaza J., Peiteado J., Lozano-León A., and García-Martín O. Detection of Salmonella senftenberg associated with high saline environments in mussel processing facilities. J. Food Prot. 67 (2004) 256-263
47. Mazzota A.S. Thermal inactivation of stationary-phase and acid-adapted E. coli O157:H7, Salmonella and Listeria monocytogenes in fruit juices. J. Food Prot. 64 (2001) 315-320
48. Palmfeldt J., and Hahn Hagerdal B. Influence of culture pH on survival of Lactobacillus reuteri subjected to freeze-drying. Int. J. Food Microbiol. 55 (2000) 235-238
49. Read R.B., Bradshaw J.G., Dickerson R.W., and Peeler J.T. Thermal resistance of salmonellae isolated from dry milk. Appl. Microbiol. 16 (1968) 998-1001
50. Rowan N.J., and Anderson J.G. Effects of above-optimum growth temperature and cell morphology on thermotolerance of Listeria monocytogenes cells suspended in bovine milk. Appl. Environ. Microbiol. 64 (1998) 2065-2071
51. Rowe M.T., and Kirk R.B. An investigation into the phenomenon of cross-protection in Escherichia coli O157:H7. Food Microbiol. 16 (1999) 157-164
52. Russell N.J., Evans R.I., ter Steg P.F., Hellemons J., Verheul A., and Abee T. Membranes as a target for stress adaptation. Int. J. Food Microbiol. 28 (1995) 255-261
53. Ryu J.H., and Beuchat L.R. Influence of acid tolerance responses on survival, growth and thermal cross-protection of E. coli O157:H7 in acidified media and fruit juices. Int. J. Food Microbiol. 45 (1998) 185-193
54. Ryu J.H., and Beuchat L.R. Changes in heat tolerance of Escherichia coli O157:H7 after exposure to acidic environments. Food Microbiol. 16 (1999) 317-324
55. Sampathkumar B., Khachatourians G.G., and Korber D.R. Treatment of Salmonella enterica serovar Enteritidis with a sublethal concentration of trisodium phosphate or alkaline pH induces thermotolerance. Appl. Environ. Microbiol. 70 (2004) 4613-4620
56. Sogaard H., and Nielsen B.B. The occurrence of Salmonella in waste water from Danish slaughterhouses. A quantitative study. Nordisk Vet. 31 (1979) 353-359
57. Steel R.G.D., and Torrie J.H. Comparación entre dos medias muestrales. Bioestadística: Principios y Procedimientos (1986), McGraw Hill, Madrid 83-116
58. Tosun H., and Gonul S.A. Acid adaptation protects Salmonella typhimurium from environmental stress. Turk. J. Biol. 27 (2003) 31-36
59. Uyttendaele M., Vankeirsbilck S., and Debevere J. Recovery of heat-stressed E. coli O157:H7 from ground beef and survival of E. coli O157:H7 in refrigerated and frozen ground beef and in fermented sausage kept at 7 °C and 22 °C. Food Microbiol. 18 (2001) 511-519
60. Wang Y., Corrieu G., and Béal C. Fermentation pH and temperature influence the cryotolerance of Lactobacillus acidophilus RD758. J. Dairy Sci. 88 (2005) 21-29
61. Wilde S., Jorgensen F., Campbell A., Rowbury R., and Humphrey T. Growth of Salmonella enterica serovar Enteritidis PT4 in media containing glucose results in enhanced RpoS-independent heat and acid tolerance but does not affect the ability to survive air-drying on surfaces. Food Microbiol. 17 (2000) 679-686
62. Yatvin M.B., Gipp J.J., Klessig D.R., and Dennis W.H. Hyperthermic sensitivity and growth stage in Escherichia coli. Radiat. Res. 106 (1986) 78-88