Some like it hot: Heat resistance of Escherichia coli in food

Frontiers in Microbiology

Volumn 7, Issue NOV, 2016, Pages

  Li, Hui ^a   Gänzle, Michael ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b HUBEI UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

Escherichia coli; Food processing; Heat resistance; Locus of heat resistance; Protein; VTEC

Indexed keywords

CYCLOPROPANE DERIVATIVE; HEAT SHOCK PROTEIN; PORIN; SIGMA FACTOR; SODIUM CHLORIDE; SUGAR; WATER;

BACTERIAL MEMBRANE; BACTERIUM ISOLATION; COOKING; ESCHERICHIA COLI; GENE CONTROL; GENE DISRUPTION; GENE OVEREXPRESSION; GENETIC REGULATION; GENETIC VARIABILITY; HEAT STRESS; HEAT TOLERANCE; LETHALITY; MEAT INDUSTRY; MEMBRANE FLUIDITY; MEMBRANE STABILIZATION; NONHUMAN; OSMOTIC STRESS; PATHOGEN CLEARANCE; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN MISFOLDING; REVIEW; TEMPERATURE; WASTE MANAGEMENT;

EID: 85006821318     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01763     Document Type: Review

References (145)

1. Aertsen, A., De Spiegeleer, P., Vanoirbeek, K., Lavilla, M., and Michiels, C. W. (2005). Induction of oxidative stress by high hydrostatic pressure in Escherichia coli. Appl. Environ. Microbiol. 71, 2226-2231. doi: 10.1128/AEM.71.3.1155-1162.2005.
2. Aertsen, A., Vanoirbeek, K., Spiegeleer, P. D., Sermon, J., Hauben, K., Farewell, A., et al. (2004). Heat shock protein-mediated resistance to high hydrostatic pressure in Escherichia coli. Appl. Environ. Microbiol. 70, 2660-2666. doi: 10.1128/AEM.70.5.2660-2666.2004.
3. Ahmed, N. M., Conner, D. E., and Huffman, D. L. (1995). Heat resistance of Escherichia coli O157:H7 in meat and poultry as affected by product composition. J. Food Sci. 60, 606-610. doi: 10.1111/j.1365-2621.1995.tb09838.x.
4. Alba, B. M., and Gross, C. A. (2004). Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol. Micribiol. 52, 613-619. doi: 10.1111/j.1365-2958.2003.03982.x.
5. Aldsworth, T. G., Sharman, R. L., and Dodd, C. E. (1999). Bacterial suicide through stress. Cell. Mol. Life Sci. 56, 378-383. doi: 10.1007/s000180050439.
6. Allen, K. J., Lepp, D., McKellar, R. C., and Griffiths, M. W. (2008). Examination of stress and virulence gene expression in Escherichia coli O157:H7 using targeted microarray analysis. Foodborne Pathog. Dis. 5, 437-447. doi: 10.1089/fpd.2008.0100.
7. Archer, J., Jervis, E. T., Bird, J., and Gaze, J. E. (1998). Heat resistance of Salmonella weltevreden in low-moisture environments. J. Food Prot. 61, 969-973.
8. Arneborg, N., Salskov-Iversen, A. S., and Mathiasen, T. E. (1993). The effect of growth rate and other growth conditions on the lipid composition of Escherichia coli. Appl. Microbiol. Biotechnol. 39, 353-357. doi: 10.1007/BF00192091.
9. Arsène, F., Tomoyasu, T., and Bukau, B. (2000). The heat shock response of Escherichia coli. Int. J. Food Microbiol. 55, 3-9. doi: 10.1016/S0168-1605(00)00206-3.
10. Bae, Y., and Lee, S. (2010). Effect of pre-exposure to sodium chloride on the resistance of pathogens to thermal and acid stresses. J. Food Saf. 30, 1016-1025. doi: 10.1111/j.1745-4565.2010.00259.x.
11. Baird-Parker, A. C., Boothroyd, M., and Jones, E. (1970). The effect of water activity on the heat resistance of heat sensitive and heat resistant strains of Salmonellae. J. Appl. Microbiol. 33, 515-522.
12. Beney, L., and Gervais, P. (2001). Influence of the fluidity of the membrane on the response of microorganisms to environmental stresses. Appl. Microbiol. Biotechnol. 57, 34-42. doi: 10.1007/s002530100754.
13. Benov, L., and Fridovich, I. (1995). Superoxide dismutase protects against aerobic heat shock in Escherichia coli. J. Bacteriol. 177, 3344-3346.
14. Beuchat, L. R., Komitopoulou, E., Beckers, H., Betts, R. P., Bourdichon, F., Fanning, S., et al. (2013). Low-water activity foods: increased concern as vehicles of foodborne pathogens. J. Food Prot. 76, 150-172. doi: 10.4315/0362-028X.JFP-12-211.
15. Beuchat, L. R., and Scouten, A. J. (2002). Combined effects of water activity, temperature and chemical treatments on the survival of Salmonella and Escherichia coli O157:H7 on alfalfa seeds. J. Appl. Microbiol. 92, 382-395. doi: 10.1046/j.1365-2672.2002.01532.x.
16. Bogosian, G., Aardema, N. D., Bourneuf, E. V., Morris, P. J. L., and O'Neil, J. P. (2000). Recovery of hydrogen peroxide-sensitive culturable cells of Vibrio vulnificus gives the appearance of resuscitation from a viable but nonculturable state. J. Bacteriol. 182, 5070-5075. doi: 10.1128/JB.182.18.5070-5075.2000.
17. Brandl, M. T., Pan, Z., Huynh, S., Zhu, Y., and McHugh, T. H. (2008). Reduction of Salmonella enteritidis population sizes on almond kernels with infrared heat. J. Food Prot. 71, 897-902.
18. Brown, J. L., Ross, T., McMeekin, T. A., and Nichols, P. D. (1997). Acid habituation of Escherichia coli and the potential role of cyclopropane fatty acids in low pH tolerance. Int. J. Food Microbiol. 37, 163-173. doi: 10.1016/S0168-1605(97)00068-8.
19. Buchanan, R. L., and Edelson, S. G. (1999). Effect of pH-dependent, stationary phase acid resistance on the thermal tolerance of Escherichia coli O157:H7. Food Microbiol. 16, 447-458. doi: 10.1006/fmic.1998.0260.
20. Bukau, B. (1993). Regulation of the Escherichia coli heat-shock response. Mol. Microbiol. 9, 671-680. doi: 10.1111/j.1365-2958.1993.tb01727.x.
21. Cabiscol, E., Tamarit, J., and Ros, J. (2000). Oxidative stress in bacteria and protein damage by reactive oxygen species. Int. Microbiol. 3, 3-8.
22. Charoenwong, D., Andrews, S., and Mackey, B. (2011). Role of rpoS in the development of cell envelope resilience and pressure resistance in stationary-phase Escherichia coli. Appl. Environ. Microbiol. 77, 5220-5229. doi: 10.1128/AEM.00648-11.
23. Chen, Y. Y., and Gänzle, M. G. (2016). Influence of cyclopropane fatty acids on heat, high pressure, acid and oxidative resistance in Escherichia coli. Int. J. Food Microbiol. 222, 16-22. doi: 10.1016/j.ijfoodmicro.2016.01.017.
24. Cheville, A. M., Arnold, W., Buchrieser, C., Cheng, M. M., and Kaspar, C. W. (1996). rpoS regulation of acid, heat, and salt tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 62, 1822-1824.
25. Choi, S. H., Baumler, D. J., and Kaspar, C. W. (2000). Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 66, 3911-3916. doi: 10.1128/AEM.66.9.3911-3916.2000.
26. Christ, D., and Chin, J. W. (2008). Engineering Escherichia coli heat-resistance by synthetic gene amplification. Protein Eng. Des. Sel. 21, 121-125. doi: 10.1093/protein/gzm085.
27. Chung, H. J., Wang, S., and Tang, J. (2007). Influence of heat transfer with tube methods on measured thermal inactivation parameters for Escherichia coli. J. Food Prot. 70, 851-859.
28. Czechowicz, S. M., Santos, O., and Zottola, E. A. (1996). Recovery of thermally-stressed Escherichia coli O157:H7 by media supplemented with pyruvate. Int. J. Food Microbiol. 33, 275-284. doi: 10.1016/0168-1605(96)01116-6.
29. Dartigalongue, C., and Raina, S. (1998). A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli. EMBO J. 17, 3968-3980. doi: 10.1093/emboj/17.14.3968.
30. De Mendoza, D., and Cronan, J. E. Jr. (1983). Thermal regulation of membrane lipid fluidity in bacteria. Trends Biochem. Sci. 8, 49-52. doi: 10.1016/0968-0004(83)90388-2.
31. Denich, T. J., Beaudette, L. A., Lee, H., and Trevors, J. T. (2003). Effect of selected environmental and physico-chemical factors on bacterial cytoplasmic membranes. J. Microbiol. Methods 52, 149-182. doi: 10.1016/S0167-7012(02)00155-0.
32. Dlusskaya, E. A., McMullen, L. M., and Gänzle, M. G. (2011). Characterization of an extremely heat-resistant Escherichia coli obtained from a beef processing facility. J. Appl. Microbiol. 110, 840-849. doi: 10.1111/j.1365-2672.2011.04943.x.
33. Doyle, M. P., and Beuchat, L. R. (2013). Food Microbiology: Fundamentals and Frontiers. New York, NY: American Society for Microbiology Press.
34. Du, W., Abd, S. J., McCarthy, K. L., and Harris, L. J. (2010). Reduction of Salmonella on inoculated almonds exposed to hot oil. J. Food Prot. 73, 1238-1246.
35. Earnshaw, R. G., Appleyard, J., and Hurst, R. M. (1995). Understanding physical inactivation processes: combined preservation opportunities using heat, ultrasound and pressure. Int. J. Food Microbiol. 28, 197-219. doi: 10.1016/0168-1605(95)00057-7.
36. Enache, E., Mathusa, E. C., Elliott, P. H., Black, D. G., Chen, Y., Scott, V. N., et al. (2011). Thermal resistance parameters for shiga toxin-producing Escherichia coli in apple juice. J. Food Prot. 74, 1231-1237. doi: 10.4315/0362-028X.JFP-10-488.
37. Finn, S., Condell, O., McClure, P., Amézquita, A., and Fanning, S. (2013). Mechanisms of survival, responses and sources of Salmonella in low-moisture environments. Front. Microbiol. 4:331. doi: 10.3389/fmicb.2013.00331.
38. Frenzen, P. D., Drake, A., Angulo, F. J., and the Emerging Infections Program Foodnet Working Group (2005). Ecomomic cost of illness due to Escherichia coli O157 infections in the United States. J. Food Prot. 68, 2623-2630.
39. Gänzle, M. G., and Liu, Y. (2015). Mechanisms of pressure-mediated cell death and injury in Escherichia coli: from fundamentals to food applications. Front. Microbiol. 6:599. doi: 10.3389/fmicb.2015.00599.
40. Garcia-Hernandez, R., McMullen, L., and Gänzle, M. G. (2015). Development and validation of a surrogate strain cocktail to evaluate bactericidal effects of pressure on verotoxigenic Escherichia coli. Int. J. Food Microbiol. 205, 16-22. doi: 10.1016/j.ijfoodmicro.2015.03.028.
41. Govers, S. K., Dutre, P., and Aertsen, A. (2014). In vivo disassembly and reassembly of protein aggregates in Escherichia coli. J. Bacteriol. 196, 2325-2332. doi: 10.1128/JB.01549-14.
42. Greig, J. D., and Ravel, A. (2009). Analysis of foodborne outbreak data reported internationally for source attribution. Int. J. Food Microbiol. 31, 77-87. doi: 10.1016/j.ijfoodmicro.2008.12.031.
43. Grogan, D. W., and Cronan, J. E. Jr. (1997). Cyclopropane ring formation in membrane lipids of bacteria. Microbiol. Mol. Biol. Rev. 61, 429-441.
44. Gupte, A. R., De Rezende, C. L. E., and Joseph, S. W. (2003). Induction and resuscitation of viable but nonculturable Salmonella enterica serovar Typhimurium DT104. Appl. Environ. Microbiol. 69, 6669-6675. doi: 10.1128/AEM.69.11.6669-6675.2003.
45. Guyot, S., Pottier, L., Ferret, E., Gal, L., and Gervais, P. (2010). Physiological responses of Escherichia coli exposed to different heat-stress kinetics. Arch. Microbiol. 192, 651-661. doi: 10.1007/s00203-010-0597-1.
46. Hauben, K. J. A., Bartlett, D. H., Soontjens, C., Cornelis, K., Wuytack, E. Y., and Michiels, C. W. (1997). Escherichia coli mutants resistant to inactivation by high hydrostatic pressure. Appl. Environ. Microbiol. 63, 945-950.
47. Hauben, K. J. A., Bernaerts, K., and Michiels, C. W. (1998). Protective effect of calcium on inactivation of Escherichia coli by high hydrostatic pressure. J. Appl. Microbiol. 85, 678-684. doi: 10.1111/j.1365-2672.1998.00577.x.
48. Hengge-Aronis, R. (2002). Signal transduction and regulatory mechanisms involved in control of the sS (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 66, 373-395. doi: 10.1128/MMBR.66.3.373-395.2002.
49. Hengge-Aronis, R., Klein, W., Lange, R., Rimmele, M., and Boos, W. (1991). Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli. J. Bacteriol. 173, 7918-7924.
50. Hiramatsu, R., Matsumoto, M., Sakae, K., and Miyazaki, Y. (2005). Ability of shiga toxin-producing Escherichia coli and Salmonella spp. to survive in a desiccation model system and in dry foods. Appl. Environ. Microbiol. 71, 6657-6663. doi: 10.1128/AEM.71.11.6657-6663.2005.
51. Hitchener, B. J., and Egan, A. F. (1977). Outer-membrane damage in sublethally heated Escherichia coli K-12. Can. J. Microbiol. 23, 311-318. doi: 10.1139/m77-046.
52. Huang, I. D., Yousef, A. E., Marth, E. H., and Mathew, M. E. (1992). Thermal inactivation of Listeria monocytogenes in chicken gravy. J. Food Prot. 55, 492-496.
53. Imlay, J. A. (2013). The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat. Rev. Microbiol. 11, 443-454. doi: 10.1038/nrmicro3032.
54. Jakob, U., Gaestel, M., Engel, K., and Buchner, J. (1993). Small heat shock proteins are molecular chaperones. J. Biol. Chem. 268, 1517-1520.
55. Jaquette, C. B., Beuchat, L. R., and Mahon, B. E. (1996). Efficacy of chlorine and heat treatment in killing Salmonella stanley inoculated onto alfalfa seeds and growth and survival of the pathogen during sprouting and storage. Appl. Environ. Microbiol. 62, 2212-2215.
56. Jay, J. M., Loessner, M. J., and Golden, D. A. (2005). Modern Food Microbiology. New York, NY: Springer Science and Business Media Press.
57. Jenkins, D. E., Auger, E. A., and Matin, A. (1991). Role of RpoH, a heat shock regulator protein, in Escherichia coli carbon starvation protein synthesis and survival. J. Bacteriol. 173, 1992-1996.
58. Jin, T., Zhang, H., Boyd, G., and Tang, J. (2008). Thermal resistance of Salmonella enteritidis and Escherichia coli K-12 in liquid egg determined by thermal-death-time disks. J. Food Eng. 84, 608-614. doi: 10.1016/j.jfoodeng.2007.06.026.
59. Juneja, V. K., Cadavez, V., Gonzales-Barron, U., and Mukhopadhyay, S. (2015). Modelling the effect of pH, sodium chloride and sodium pyrophosphate on the thermal resistance of Escherichia coli O157:H7 in ground beef. Food Res. Int. 69, 289-304. doi: 10.1016/j.foodres.2014.11.050.
60. Juneja, V. K., and Marmer, B. S. (1999). Lethality of heat to Escherichia coli O157:H7: D-and z-value determinations in turkey, lamb, and pork. Food Res. Int. 32, 23-28. doi: 10.1016/S0963-9969(99)00060-5.
61. Karch, H., Tarr, P. I., and Bielaszewska, M. (2005). Enterohaemorrhagic Escherichia coli in human medicine. Int. J. Med. Microbiol. 295, 405-418. doi: 10.1016/j.ijmm.2005.06.009.
62. Kato, A., Ohnishi, H., Yamamoto, K., Furuta, E., Tanabe, H., and Utsumi, R. (2000). Transcription of emrKY is regulated by the EvgA-EvgS two-component system in Escherichia coli K-12. Biosci. Biotechnol. Biochem. 64, 1203-1209. doi: 10.1271/bbb.64.1203.
63. Katsui, N., Tsuchido, T., Takano, M., and Shibasaki, I. (1981). Effect of preincubation temperature on the heat resistance of Escherichia coli having different fatty acid compositions. J. Gen. Microbiol. 122, 357-361.
64. Kaur, J., Ledward, D. A., Park, R. W. A., and Robson, R. L. (1998). Factors affecting the heat resistance of Escherichia coli O157:H7. Lett. Appl. Microbiol. 26, 325-330. doi: 10.1046/j.1472-765X.1998.00339.x.
65. Kempf, B., and Bremmer, E. (1998). Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch. Microbiol. 170, 319-330. doi: 10.1007/s002030050649.
66. Kennedy, J., Blair, I. S., McDowell, D. A., and Bolton, D. J. (2005). 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, 1229-1235. doi: 10.1111/j.1365-2672.2005.02697.x.
67. Kim, Y. B., Kim, H. W., Song, M. K., and Rhee, M. S. (2015). Decontamination method using heat and relative humidity for radish seeds achieves a 7-log reduction of Escherichia coli O157:H7 without affecting product quality. Int. J. Food Microbiol. 201, 42-46. doi: 10.1016/j.ijfoodmicro.2015.02.015.
68. Kitagawa, M., Matsumura, Y., and Tsuchido, T. (2000). Small heat shock proteins, IbpA and IbpB, are involved in resistances to heat and superoxide stresses in Escherichia coli. FEMS Microbiol. Lett. 184, 165-171. doi: 10.1111/j.1574-6968.2000.tb09009.x.
69. Klaiber, R. G., Baur, S., Wolf, G., Hammes, W. P., and Carle, R. (2005). Quality of minimally processed carrots as affected by warm water washing and chlorination. Innov. Food Sci. Emerg. Technol. 6, 351-362. doi: 10.1016/j.ifset.2005.03.002.
70. Kotrola, J., and Conner, D. E. (1997). Heat inactivation of Escherichia coli O157:H7 in turkey meat as affected by sodium chloride, sodium lactate, polyphosphate, and fat content. J. Food Prot. 60, 898-902.
71. Kuczyñska-Wisnik, D., Kêdzierska, S., Matuszewska, E., Lund, P., Taylor, A., Lipiñska, B., et al. (2002). The Escherichia coli small heat-shock proteins IbpA and IbpB prevent the aggregation of endogenous proteins denatured in vivo during extreme heat shock. Microbiology 148, 1757-1765. doi: 10.1099/00221287-148-6-1757.
72. Lamosa, P., Burke, A., Peist, R., Huber, R., Liu, M. Y., Silva, G., et al. (2000). Thermostabilization of proteins by diglycerol phosphate: a new compatible solute from the hyperthermophile Archaeoglobus fulgidus. Appl. Environ. Microbiol. 66, 1974-1979. doi: 10.1128/AEM.66.5.1974-1979.2000.
73. Landini, P., Egli, T., Wolf, J., and Lacour, S. (2014). SigmaS, a major player in the response to environmental stresses in Escherichia coli: role, regulation and mechanisms of promoter recognition. Environ. Microbiol. Rep. 6, 1-13. doi: 10.1111/1758-2229.12112.
74. Lange, R., and Hengge-Aronis, R. (1991). Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol. Microbiol. 5, 49-59. doi: 10.1111/j.1365-2958.1991.tb01825.x.
75. Laskowska, E., Wawrzynów, A., and Taylor, A. (1996). IbpA and IbpB, the new heat-shock proteins, bind to endogenous Escherichia coli proteins aggregated intracellularly by heat shock. Biochimie 78, 117-122. doi: 10.1016/0300-9084(96)82643-5.
76. Lee, C., Wigren, E., Lünsdorf, H., and Römling, U. (2016). Protein homeostasis-more than resisting a hot bath. Curr. Opin. Microbiol. 30, 147-154. doi: 10.1016/j.mib.2016.02.006.
77. Lee, C., Wigren, E., Trcek, J., Peters, V., Kim, J., Hasni, M. S., et al. (2015). A novel protein quality control mechanism contributes to heat shock resistance of worldwide-distributed Pseudomonas aeruginosa clone C strains. Environ. Microbiol. 17, 4511-4526. doi: 10.1111/1462-2920.12915.
78. Lee, G. J., Roseman, A. M., Saibil, H. R., and Vierling, E. (1997). A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J. 16, 659-671. doi: 10.1093/emboj/16.3.659.
79. Lee, J., and Kaletunc, G. (2002). Evaluation of the heat inactivation of Escherichia coli and Lactobacillus plantarum by differential scanning calorimetry. Appl. Environ. Microbiol. 68, 5379-5386. doi: 10.1128/AEM.68.11.5379-5386.2002.
80. Li, H., Garcia-Hernandez, R., Driedger, D., McMullen, L. M., and Gänzle, M. (2016). Effect of the food matrix on pressure resistance of Shiga-toxin producing Escherichia coli. Food Microbiol. 57, 96-102. doi: 10.1016/j.fm.2016.02.002.
81. Lindner, A. B., Madden, R., Demarez, A., Stewart, E. J., and Taddei, F. (2008). Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc. Natl. Acad. Sci. U.S.A. 105, 3076-3081. doi: 10.1073/pnas.0708931105.
82. Line, J. E., Fain, A. R. Jr., Moran, A. B., Martin, L. M., Lechowich, R. V., Carosella, J. M., et al. (1991). Lethality of heat to Escherichia coli O157:H7: D-value and Z-value determinations in ground beef. J. Food Prot. 54, 762-766.
83. Liu, Y. (2015). Heat and Pressure Resistance of Escherichia coli and Its Inactivation in the Presence of Antimicrobial Compounds. Doctor's thesis, University of Alberta, Edmonton, AB.
84. Liu, Y., Gill, A., McMullen, L., and Gänzle, M. G. (2015). Variation in heat and pressure resistance of verotoxigenic and non-toxigenic Escherichia coli. J. Food Prot. 78, 111-120. doi: 10.4315/0362-028X.JFP-14-267.
85. Luchansky, J. B., Porto-Fett, A. C. S., Shoyer, B. A., Call, J. E., Schlosser, W., Shaw, W., et al. (2012). Fate of shiga toxin-producing O157:H7 and non-O157:H7 Escherichia coli cells within blade-tenderized beef steaks after cooking on a commercial open-flame gas grill. J. Food Prot. 75, 62-70. doi: 10.4315/0362-028X.JFP-11-267.
86. Mackey, B. M., Miles, C. A., Parsons, S. E., and Seymour, D. A. (1991). Thermal denaturation of whole cells and cell components of Escherichia coli examined by differential scanning calorimetry. J. Gen. Microbiol. 137, 2361-2374. doi: 10.1099/00221287-137-10-2361.
87. Malone, A. S., Chuang, Y. K., and Yousef, A. E. (2006). Genes of Escherichia coli O157:H7 that are involved in high-pressure resistance. Appl. Environ. Microbiol. 72, 2661-2671. doi: 10.1128/AEM.72.4.2661-2671.2006.
88. Mao, Y., Doyle, M. P., and Chen, J. (2001). Insertion mutagenesis of wca reduces acid and heat tolerance of enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 183, 3811-3815. doi: 10.1128/JB.183.12.3811-3815.2001.
89. Masuda, N., and Church, G. M. (2002). Escherichia coli gene expression responsive to levels of the response regulator EvgA. J. Bacteriol. 184, 6225-6234. doi: 10.1128/JB.184.22.6225-6234.2002.
90. Mazzotta, A. S. (2001). Thermal inactivation of stationary-phase and acid-adapted Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes in fruit juices. J. Food Prot. 3, 287-429.
91. Mecsas, J., Rouviere, P. E., Erickson, J. W., Donohue, T. J., and Gross, C. A. (1993). The activity of sE, an Escherichia coli heat-inducible s-factor, is modulated by expression of outer membrane proteins. Genes Dev. 7, 2618-2628. doi: 10.1101/gad.7.12b.2618.
92. Mejía, R., Gómez-Eichelmann, M. C., and Fernández, M. S. (1995). Membrane fluidity of Escherichia coli during heat-shock. Biochim. Biophys. Acta 1239, 195-200. doi: 10.1016/0005-2736(95)00152-S.
93. Mercer, R., Zheng, J., Garcia-Hernandez, R., Ruan, L., Gänzle, M., and McMullen, L. (2015). Genetic determinants of heat resistance in Escherichia coli. Front. Microbiol. 6:932. doi: 10.3389/fmicb.2015.00932.
94. Missiakas, D., Betton, J. M., and Raina, S. (1996). New components of protein folding in the extra-cytoplasmic compartments of Escherichia coli: SurA, FkpA and Skp/OmpH. Mol. Microbiol. 21, 871-884. doi: 10.1046/j.1365-2958.1996.561412.x.
95. Mizunoe, Y., Wai, S. N., Ishikawa, T., Takade, A., and Yoshida, S. (2000). Resuscitation of viable but nonculturable cells of Vibrio parahaemolyticus induced at low temperature under starvation. FEMS Microbiol. Lett. 186, 115-120. doi: 10.1111/j.1574-6968.2000.tb09091.x.
96. Mogk, A., Deuerling, E., Vorderwulbecke, S., Vierling, E., and Bukau, B. (2003). Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol. Microbiol. 50, 585-595.
97. Mogk, A., Tomoyasu, T., Goloubinoff, P., Rüdiger, S., Röder, D., Langen, H., et al. (1999). Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J. 18, 6934-6949. doi: 10.1093/emboj/18.24.6934.
98. Mohácsi-Farkas, C. S., Farkas, J., Mészáros, L., Reichart, O., and Andrássy, É (1999). Thermal denaturation of bacterial cells examined by differential scanning calorimetry. J. Therm. Anal. Calorim. 57, 409-414. doi: 10.1023/A:1010139204401.
99. Morishige, Y., Fujimori, K., and Amano, F. (2013). Differential resuscitative effect of pyruvate and its analogues on VBNC (viable but non-culturable) Salmonella. Microbes Environ. 28, 180-186. doi: 10.1264/jsme2.ME12174.
100. Murphy, R. Y., Marks, B. P., Johnson, E. R., and Johnson, M. G. (1999). Inactivation of Salmonella and Listeria in ground chicken breast meat during thermal processing. J. Food Prot. 9, 975-1096.
101. Nair, M. S., Lau, P., Belskie, K., Fancher, S., Chen, C., Karumathil, D. P., et al. (2016). Potentiating the heat inactivation of Escherichia coli O157:H7 in ground beef patties by natural antimicrobials. Front. Microbiol. 7:15.
102. Nakayama, H., Mitsui, T., Nishihara, M., and Kito, M. (1980). Relation between growth temperature of Escherichia coli and phase transition temperatures of its cytoplasmic and outer membranes. Biochim. Biophys. Acta 601, 1-10. doi: 10.1016/0005-2736(80)90508-8.
103. Neetoo, H., and Chen, H. (2011). Individual and combined application of dry heat with high hydrostatic pressure to inactivate Salmonella and Escherichia coli O157:H7 on alfalfa seeds. Food Microbiol. 28, 119-127. doi: 10.1016/j.fm.2011.05.005.
104. Ng, H., Bayne, H. G., and Garibaldi, J. A. (1969). Heat resistance of Salmonella: the uniqueness of Salmonella Senftenberg 775W. Appl. Microbiol. 17, 78-82.
105. Nicholson, W. L., Munakata, N., Horneck, G., Melosh, H. J., and Setlow, P. (2000). Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64, 548-572. doi: 10.1128/MMBR.64.3.548-572.2000.
106. Nishino, K., Inazumi, Y., and Yamaguchi, A. (2003). Global analysis of genes regulated by EvgA of the two-component regulatory system in Escherichia coli. J. Bacteriol. 185, 2667-2672. doi: 10.1128/JB.185.8.2667-2672.2003.
107. Parsell, D. A., and Lindquist, S. (1993). The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genet. 27, 437-496. doi: 10.1146/annurev.ge.27.120193.002253.
108. Pereira, R., Martins, J., Mateus, C., Teixeira, J. A., and Vicente, A. A. (2006). Death kinetics of Escherichia coli in goat milk and Bacillus licheniformis in cloudberry jam treated by ohmic heating. Chem. Pap. 61, 121-126.
109. Pleitner, A., Zhai, Y., Winter, R., Ruan, L., McMullen, L. M., and Gänzle, M. G. (2012). Compatible solutes contribute to heat resistance and ribosome stability in Escherichia coli AW1.7. Biochim. Biophys. Acta 1824, 1351-1357. doi: 10.1016/j.bbapap.2012.07.007.
110. Podolak, R., Enache, E., Stone, W., Black, D. G., and Elliott, P. H. (2010). Sources and risk factors for contamination, survival, persistence, and heat resistance of Salmonella in low-moisture foods. J. Food Prot. 73, 1919-1936.
111. Privalle, C. T., and Fridovich, I. (1987). Induction of superoxide dismutase in Escherichia coli by heat shock. Proc. Natl. Acad. Sci. U.S.A. 84, 2723-2726. doi: 10.1073/pnas.84.9.2723.
112. Quinn, P. J. (1981). The fluidity of cell membranes and its regulation. Prog. Biophys. Mol. Biol. 38, 1-104. doi: 10.1016/0079-6107(81)90011-0.
113. Rajic, A., Waddell, L. A., Sargeant, J. M., Read, S., Farber, J., Firth, M. J., et al. (2007). An overview of microbial food safety programs in beef, pork, and poultry from farm to processing in Canada. J. Food Prot. 70, 1286-1294.
114. Ramos, A., Raven, N. D. H., Sharp, R. J., Bartolucci, S., Rossi, M., Cannio, R., et al. (1997). Stabilization of enzymes against thermal stress and freeze-drying by mannosylglycerate. Appl. Environ. Microbiol. 63, 4020-4025.
115. Riemann, H. (1968). Effect of water activity on the heat resistance of Salmonella in "dry" materials. Appl. Microbiol. 16, 1621-1622.
116. Riordan, D. C. R., Duffy, G., Sheridan, J. J., Whiting, R. C., Blair, I. S., and McDowell, D. A. (2000). Effects of acid adaptation, product pH, and heating on survival of Escherichia coli O157:H7 in pepperoni. Appl. Environ. Microbiol. 66, 1726-1729. doi: 10.1128/AEM.66.4.1726-1729.2000.
117. Robey, M., Benito, A., Hutson, R. H., Pascual, C., Park, S. F., and Mackey, B. M. (2001). Variation in resistance to high hydrostatic pressure and rpoS heterogeneity in natural isolates of Escherichia coli O157:H7. Appl. Environ. Microbiol. 67, 4901-4907. doi: 10.1128/AEM.67.10.4901-4907.2001.
118. Ruan, L., Pleitner, A. M., Gänzle, M. G., and McMullen, L. M. (2011). Solute transport proteins and the outer membrane protein NmpC contribute to heat-resistance of Escherichia coli AW1.7. Appl. Environ. Microbiol. 77, 2961-2967. doi: 10.1128/AEM.01930-10.
119. Ryu, J., and Beuchat, L. R. (1998). Influence of acid tolerance responses on survival, growth, and thermal cross-protection of Escherichia coli O157:H7 in acidified media and fruit juices. Int. J. Food Microbiol. 45, 185-193. doi: 10.1016/S0168-1605(98)00165-2.
120. Ryu, J., and Beuchat, L. R. (1999). Changes in heat tolerance of Escherichia coli O157:H7 after exposure to acidic environments. Food Microbiol. 16, 317-324. doi: 10.1006/fmic.1998.0234.
121. Santillana Farakos, S. M., Schaffner, D. W., and Frank, J. F. (2014). Predicting survival of Salmonella in low-water activity foods: an analysis of literature data. J. Food Prot. 77, 1448-1461. doi: 10.4315/0362-028X.JFP-14-013.
122. Sharma, M., Adler, B. B., Harrison, M. D., and Beuchat, L. R. (2005). Thermal tolerance of acid-adapted and unadapted Salmonella, Escherichia coli O157:H7, and Listeria monocytogenes in cantaloupe juice and watermelon juice. Lett. Appl. Microbiol. 41, 448-453. doi: 10.1111/j.1472-765X.2005.01797.x.
123. Sinensky, M. (1974). Homeoviscous adaptation: a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 71, 522-525. doi: 10.1073/pnas.71.2.522.
124. Smith, S. E., Maurer, J. L., Orta-Ramirez, A., Ryser, E. T., and Smith, D. M. (2001). Thermal inactivation of Salmonella spp., Salmonella typhimurium DT104 and Escherichia coli O157:H7 in ground beef. J. Food Sci. 66, 1164-1168. doi: 10.1111/j.1365-2621.2001.tb16099.x.
125. Studer, P., Heller, W. E., Hummerjohann, J., and Drissner, D. (2013). Evaluation of aerated steam treatment of alfalfa and mung bean seeds to eliminate high levels of Escherichia coli O157:H7 and O178:H12, Salmonella enterica, and Listeria monocytogenes. Appl. Environ. Microbiol. 79, 4613-4619. doi: 10.1128/AEM.00443-13.
126. Suutari, M., and Laakso, S. (1994). Microbial fatty acids and thermal adaptation. Crit. Rev. Microbiol. 20, 285-328. doi: 10.3109/10408419409113560.
127. Swartz, R. S., Luchansky, J. B., Kulas, M., Shoyer, B. A., Shane, L. E., Strasser, H., et al. (2015). Thermal inactivation of shiga toxin-producing Escherichia coli cells within cubed beef steaks following cooking on a griddle. J. Food Prot. 78, 1013-1017. doi: 10.4315/0362-028X.JFP-14-454.
128. Syamaladevi, R. M., Tang, J., Villa-Rojas, R., Sablani, S., Carter, B., and Campbell, G. (2016). Influence of water activity on thermal resistance of microorganisms in low-moisture foods: a review. Compr. Rev. Food Sci. Food Saf. 15, 353-370. doi: 10.1111/1541-4337.12190.
129. Thomas, J. G., and Baneyx, F. (1998). Roles of the Escherichia coli small heat shock proteins IbpA and IbpB in thermal stress management: comparison with ClpA, ClpB, and HtpG in vivo. J. Bacteriol. 180, 5165-5172.
130. Torok, Z., Horvath, I., Goloubinoff, P., Kovacs, E., Glatz, A., Balogh, G., et al. (1997). Evidence for a lipochaperonin: association of active protein-folding GroESL oligomers with lipids can stabilize membranes under heat shock conditions. Proc. Natl. Acad. Sci. U.S.A. 94, 2192-2197. doi: 10.1073/pnas.94.6.2192.
131. Tsuchido, T., Katsui, N., Takeuchi, A., Takano, M., and Shibasaki, I. (1985). Destruction of the outer membrane permeability barrier of Escherichia coli by heat treatment. Appl. Environ. Microbiol. 50, 298-303.
132. Vaara, M. (1992). Agents that increase the permeability of the outer-membrane. Microbiol. Rev. 56, 395-411.
133. Vasan, A., Geier, R., Ingham, S. C., and Ingham, B. H. (2014). Thermal tolerance of O157 and non-O157 shiga toxigenic strains of Escherichia coli, Salmonella, and potential pathogen surrogates, in frankfurter batter and ground beef of varying fat levels. J. Food Prot. 77, 1501-1511. doi: 10.4315/0362-028X.JFP-14-106.
134. Veinger, L., Diamant, S., Buchner, J., and Goloubinoff, P. (1998). The small heat-shock proteins IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J. Biol. Chem. 273, 11032-11037. doi: 10.1074/jbc.273.18.11032.
135. Weiss, A., and Hammes, W. P. (2005). Efficacy of heat treatment in the reduction of Salmonella and Escherichia coli O157:H-on alfalfa, mung bean, and radish seeds used for sprout production. Eur. Food Res. Technol. 221, 187-191. doi: 10.1007/s00217-004-1125-9.
136. Whitfield, C., and Valvano, M. A. (1993). Biosynthesis and expression of cell-surface polysaccharides in gram-negative bacteria. Adv. Microb. Physiol. 35, 135-246. doi: 10.1016/S0065-2911(08)60099-5.
137. Winkler, J., Seybert, A., Konig, L., Pruggnaller, S., Haselmann, U., Sourjik, V., et al. (2010). Quantitative and spatio-temporal features of protein aggregation in Escherichia coli and consequences on protein quality control and cellular ageing. EMBO J. 29, 910-923. doi: 10.1038/emboj.2009.412.
138. Woodward, D. L., Clark, C. G., Caldeira, R. A., Ahmed, R., and Rodgers, F. G. (2002). Verotoxigenic Escherichia coli (VTEC): a major public health threat in Canada. Can. J. Infect. Dis. 13, 321-330. doi: 10.1155/2002/383840.
139. Yang, J., Bingol, G., Pan, Z., Brandl, M. T., McHugh, T. H., and Wang, H. (2010). Infrared heating for dry-roasting and pasteurization of almonds. J. Food Eng. 101, 273-280. doi: 10.1016/j.jfoodeng.2010.07.007.
140. Yeni, F., Yavasc, S., Alpas, H., and Soyer, Y. (2015). Most common foodborne pathogens and mycotoxins on fresh produce: a review of recent outbreaks. Crit. Rev. Food Sci. Nutr. 56, 1532-1544. doi: 10.1080/10408398.2013.777021.
141. Yoon, Y., Lee, H., Lee, S., Kim, S., and Choi, K. H. (2015). Membrane fluidity-related adaptive response mechanisms of foodborne bacterial pathogens under environmental stresses. Food Res. Int. 72, 25-36. doi: 10.1016/j.foodres.2015.03.016.
142. Yuk, H., and Marshall, D. L. (2003). Heat adaptation alters Escherichia coli O157:H7 membrane lipid composition and verotoxin production. Appl. Environ. Microbiol. 69, 5115-5119. doi: 10.1128/AEM.69.9.5115-5119.2003.
143. Zhang, Y., and Griffiths, M. W. (2003). Induced expression of the heat shock protein genes uspA and grpE during starvation at low temperatures and their influence on thermal resistance of Escherichia coli O157:H7. J. Food Prot. 66, 2045-2050.
144. Zhang, Y., and Rock, C. O. (2008). Membrane lipid homeostasis in bacteria. Nat. Rev. Microbiol. 6, 222-233. doi: 10.1038/nrmicro1839.
145. Zhao, G., Ceci, P., Ilari, A., Giangiacomo, L., Laue, T. M., Chiancone, E., et al. (2002). Iron and hydrogen peroxide detoxification properties of DNA-binding protein from starved cells. A ferritin-like DNA-binding protein of Escherichia coli. J. Biol. Chem. 277, 27689-22796. doi: 10.1074/jbc.M202094200.