Mechanisms of pressure-mediated cell death and injury in Escherichia coli: From fundamentals to food applications

Frontiers in Microbiology

Volumn 6, Issue JUN, 2015, Pages

  Gänzle, Michael ^a   Liu, Yang ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

EHEC; Escherichia coli; Food preservation; High hydrostatic pressure; STEC

Indexed keywords

BACTERIOCIN; BILE ACID; CYCLOPROPANE; LACTOFERRIN; LACTOPEROXIDASE; LYSOZYME; PORIN; REACTIVE OXYGEN METABOLITE; TREHALOSE;

ANTIBIOTIC RESISTANCE; BACTERIAL SURVIVAL; CELL DEATH; CELL DISRUPTION; CELL MEMBRANE; ENZYME DENATURATION; ESCHERICHIA COLI; GENE MUTATION; GENETIC VARIABILITY; HOMEOSTASIS; HYDROSTATIC PRESSURE; LACTOBACILLUS PLANTARUM; LACTOCOCCUS LACTIS; NONHUMAN; OSMOREGULATION; OXIDATIVE STRESS; PRESSURE; PROTEIN EXPRESSION; PROTEIN FOLDING; REVIEW; RIBOSOME; STAPHYLOCOCCUS AUREUS; STATIC ELECTRICITY;

ESCHERICHIA COLI; STAPHYLOCOCCUS AUREUS;

EID: 84937001681     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00599     Document Type: Review

References (106)

1. Aertsen, A., Vanoirbeek, K., De Spiegeleer, P., 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
2. 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.71.5.2226-2231.2005
3. Alpas, H., and Bozoglu, F. (2000). The combined effect of high hydrostatic pressure, heat and bacteriocins on inactivation of foodborne pathogens in milk and orange juice. World J. Microbiol. Biotechnol. 16, 387-392. doi: 10.1023/A:1008936607413
4. Alpas, H., Kalchayanand, N., Bozoglu, F., and Ray, B. (2000). Interactions of high hydrostatic pressure, pressurization temperature and pH on death and injury of pressure-resistant and pressure-sensitive strains of foodborne pathogens. Intl. J. Food Microbiol. 60, 33-42. doi: 10.1016/S0168-1605(00)00324-X
5. Alpas, H., Kalchayanand, N., Bozoglu, F., Sikes, A., Dunne, C. P., and Ray, B. (1999). Variation in resistance to hydrostatic pressure among strains of food-borne pathogens. Appl. Environ. Microbiol. 65, 4248-4251.
6. Baccus-Taylor, G. S., Falloon, O. C., and Henry, N. (2015). Pressure resistance of cold-shocked Escherichia coli O157:H7 in ground beef, beef gravy and peptone water. J. Appl. Microbiol. 118, 1521-1529. doi: 10.1111/jam.12794
7. Balasubramaniam, V. M., Martinez-Monteagudo, S. I., and Gupta, R. (2015). Principles and application of high pressure-based technologies in the food industry. Ann. Rev. Food Sci. Technol. 6, 435-462. doi: 10.1146/annurev-food-022814-015539
8. Bartlett, D. H. (2002). Pressure effects on in vivo microbial processes. Biochim. Biophys. Acta 1595, 367-381. doi: 10.1016/S0167-4838(01)00357-0
9. Benito, A., Venoura, G., Casadei, M., Robinson, T., and Mackey, B. (1999). Variation in resistance of natural isolates of Escherichia coli O157 to high hydrostatic pressure, mild heat, and other stresses. Appl. Environ. Microbiol. 65, 1564-1569.
10. Bièche, D., Ritz, M., Tresse, O., Federighi, M., and de Lamballerie, M. (2009). Impacts of treatment parameters on the inactivation of Campylobacter jejuni by high pressure: a statistical study of main effects and interactions. Lett. Appl. Microbiol. 48, 198-202. doi: 10.1111/j.1472-765X.2008.02511.x
11. Black, E. P., Hirneisen, K. A., Hoover, D. G., and Kniel, K. E. (2010). Fate of Escherichia coli O157:H7 in ground beef following high-pressure processing and freezing. J. Appl. Microbiol. 108, 1352-1360. doi: 10.1111/j.1365-2672.2009.04532.x
12. Black, E. P., Setlow, P., Hocking, A. D., Stewart, C. M., Kelly, A. L., and Hoover, D. G. (2007). Response of spores to high-pressure processing. Comp. Rev. Food Sci. Food Safety. 6, 103-119. doi: 10.1111/j.1541-4337.2007.00021.x
13. Brown, J. L., Ross, T., McMeekin, T., 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
14. Buckow, R., Sikes, A., and Tume, R. (2013). Effect of high pressure on physicochemical properties of meat. Crit. Rev. Food Sci. Nutr. 53, 770-786. doi: 10.1080/10408398.2011.560296
15. Butz, P., Funtenberger, S., Haberditzl, T., and Tauscher, B. (1996). High pressure inactivation of Byssochlamys nivea ascospores and other heat resistant molds. Lebensm. Wiss. Technol. 29, 404-410. doi: 10.1006/fstl.1996.0062
16. Buzrul, S., Alpas, H., Largeteau, A., and Demazeau, G. (2008). Inactivation of Escherichia coli and Listeria innocua in kiwifruit and pineapple juices by high hydrostatic pressure. Int. J. Food Microbiol. 124, 275-278. doi: 10.1016/j.ijfoodmicro.2008.03.015
17. Casadei, M. A., Mañas, P., Niven, G. W., Needs, E., and Mackey, B. M. (2002). Role of membrane fluidity in pressure resistance of Escherichia coli NCTC 8164. Appl. Environ. Microbiol. 68, 5965-5972. doi: 10.1128/AEM.68.12.5965-5972.2002
18. 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
19. Chen, H. (2007). Use of linear, Weibull, and log-logistic functions to model pressure inactivation of seven foodborne pathogens in milk. Food Microbiol. 24, 197-204. doi: 10.1016/j.fm.2006.06.004
20. 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
21. Croxen, M. A., Law, R. J., Scholz, R., Keeney, K. M., Wlodarska, M., and Finlay, B. B. (2013). Recent advances in understanding enteric pathogenic Escherichia coli. Clin. Microbiol. Rev. 26, 822-880. doi: 10.1128/CMR.00022-13
22. De Lamo-Castellví, S., Capellas, M., Roig-Sagués, A. X., López-Pedemonte, T., Hernández-Herrero, M. M., and Guamis, B. (2006). Fate of Escherichia coli strains inoculated in model cheese elaborated with or without starter and treated by high hydrostatic pressure. J. Food Prot. 69, 2856-2864.
23. Drake, M. A., Harrison, S. L., Asplund, M., Barbosa-Canovas, G., and Swanson, B. G. (1997). High pressure treatment of milk and effects on microbiological and sensory quality of Cheddar cheese. J. Food Sci. 62, 843-845. doi: 10.1111/j.1365-2621.1997.tb15468.x
24. Espina, L., García-Gonzalo, D., Laglaoui, A., Mackey, B. M., and Pagán, R. (2012). Synergistic combinations of high hydrostatic pressure and essential oils or their constituents and their use in preservation of fruit juices. Int. J. Food Microbiol. 161, 23-30. doi: 10.1016/j.ijfoodmicro.2012.11.015
25. Farber, J. M., Kozaka, G. K., and Duquette, S. (2011). Changing regulation: canada's new thinking on Listeria. Food Control. 22, 1506-1509. doi: 10.1016/j.foodcont.2010.07.019
26. Feyaerts, J., Rogiers, G., Corthouts, J., and Michiels, C. W. (2014). Thiol-reactive natural antimicrobials and high pressure treatment synergistically enhance bacterial inactivation. Innov. Food Sci. Emerg. Technol. 27, 26-34. doi: 10.1016/j.ifset.2014.12.005
27. Gänzle, M. G., Hertel, C., and Hammes, W. P. (1999). Resistance of Escherichia coli and Salmonella against nisin and curvacin A. Int. J. Food Microbiol. 48, 37-50. doi: 10.1016/S0168-1605(99)00026-4
28. Gänzle, M. G., and Vogel, R. F. (2001). On-line fluorescence determination of pressure-mediated outer membrane damage in Escherichia coli. Syst. Appl. Microbiol. 24, 477-485. doi: 10.1078/0723-2020-00069
29. Garcia-Graells, C., Hauben, K. J., and Michiels, C. W. (1998). High-pressure inactivation and sublethal injury of pressure-resistant Escherichia coli mutants in fruit juices. Appl. Environ. Microbiol. 64, 1566-1568.
30. Garcia-Graells, C., Valckx, C., and Michiels, C. W. (2000). Inactivation of Escherichia coli and Listeria innocua in milk by combined treatment with high hydrostatic pressure and the lactoperoxidase system. Appl. Environ. Microbiol. 66, 4173-4179. doi: 10.1128/AEM.66.10.4173-4179.2000
31. 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
32. Garriga, G., Aymerich, M. T., Costa, S., Montfort, J. M., and Hugas, M. (2002). Bactericidal synergism through bacteriocins and high pressure in a meat mode3l system during storage. Food Microbiol. 19, 509-518. doi: 10.1006/fmic.2002.0498
33. Garriga, M., Grèbol, N., Aymerich, M. T., Monfort, J. M., and Hugas, M. (2004). Microbial inactivation after high-pressure processing at 600 MPa in commercial meat products over its shelf life. Innov. Food Sci. Emerg. Technol. 5, 451-457. doi: 10.1016/j.ifset.2004.07.001
34. Gayan, E., Condón, S., Alvarez, I., Nabakabaya, M., and Mackey, B. (2013). Effect of pressure-induced changes in the ionization equilibria of buffers on inactivation of Escherichia coli and Staphylococcus aureus. Appl. Environ. Microbiol. 79, 4041-4047. doi: 10.1128/AEM.00469-13
35. Georget, E., Sevenich, R., Reineke, K., Mathys, A., Heinz, V., Callanan, M., et al. (2015). Inactivation of microorganisms by high isostatic pressure processing in complex matrices: a review. Inoov. Food Sci. Emerg. Technol. 27, 1-14. doi: 10.1016/j.ifset.2014.10.015
36. Gill, A. O., and Ramaswamy, H. O. S. (2008). Application of high pressure processing to kill Escherichia coli O157 in ready-to-eat meats. J. Food Prot. 71, 2182-2189.
37. Gottlieb, S. L., Newbern, E. C., Griffin, P. M., Graves, L. M., Hoekstra, R. M., Baker, N. L., et al. (2006). Multistate outbreak of Listeriosis linked to turkey deli meat and subsequent changes in US regulatory policy. Clin. Infect. Dis. 42, 29-36. doi: 10.1086/498113
38. Govers, S. K., Dutré, 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
39. Grogan, D. W., and Cronan, J. E. (1997). Cyclopropane ring formation in membrane lipids of bacteria. Microbiol. Mol. Biol. Rev. 61, 429-441.
40. 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
41. Hauben, K. J. A., Wuytack, E. Y., Soontjens, C. C. F., and Michiels, C. W. (1996). High-pressure transient sensitization of Escherichia coli to lysozyme and nisin by disruption of outer-membrane permeability. J. Food Prot. 59, 350-355.
42. Hauben, K. J., Bartlett, D. H., Soontjens, C. C., Wuytack, E. Y., and Michiels, C. W. (1997). Escherichia coli mutants resistant to inactivation by high hydrostatic pressure. Appl. Environ. Microbiol. 63, 945-950.
43. Hsu, H., Sheen, S., Sites, J., Cassidy, J., Scullen, B., and Sommers, C. (2015). Effect of high pressure processing on the survival of Shiga Toxin-producing Escherichia coli (Big Six vs. O157:H7) in ground beef. Food Microbiol. 48, 1-7. doi: 10.1016/j.fm.2014.12.002
44. Hsu, H., Sheen, S., Sites, J., Huang, L., and Wu, J. S. (2014). Effect of high pressure treatment on the survival of Shiga toxin-producing Escherichia coli in strawberry puree. Food Microbiol. 40, 25-30. doi: 10.1016/j.fm.2013.11.019
45. Huang, Y., Ye, M., and Chen, H. (2013). Inactivation of Escherichia coli O157:H7 and Salmonella spp. in strawberry puree by high hydrostatic pressure with/without subsequent frozen storage. Int. J. Food Microbiol. 160, 337-343. doi: 10.1016/j.ijfoodmicro.2012.11.008
46. Jofré, A., Aymerich, T., Bover-Cid, S., and Garriga, M. (2010). Inactivation and recovery of Listeria monocytogenes, Salmonella enterica, and Staphylococcus aureus after high hydrostatic pressure treatments up to 900 MPa. Int. Microbiol. 13, 105-112.
47. Jordan, S. L., Pascual, C., Bracey, E., and Mackey, B. M. (2001). Inactivation and injury of pressure-resistant strains of Escherichia coli O157 and Listeria monocytogenes in fruit juices. J. Appl. Microbiol. 91, 463-469. doi: 10.1046/j.1365-2672.2001.01402.x
48. Kalchayanand, M., Hanlin, M. B., and Ray, B. (1992). Sublethal injury makes Gram-negative and resistant Gram-positive bacteria sensitive to the bacteriocins pediocin AcH and nisin. Lett. Appl. Microbiol. 15, 239-243. doi: 10.1111/j.1472-765X.1992.tb00773.x
49. Karatzas, K. A., and Bennik, M. H. (2002). Characterization of a Listeria monocytogenes Scott A isolate with high tolerance towards high hydrostatic pressure. Appl. Environ. Microbiol. 68, 3183-3189. doi: 10.1128/AEM.68.7.3183-3189.2002
50. Kilimann, K. V., Hartmann, C., Vogel, R. F., and Gänzle, M. G. (2005). Differential inactivation of glucose- and glutamate-dependent acid resistance of Escherichia coli TMW 2.497 by high pressure treatments. Syst. Appl. Microbiol. 28, 663-671. doi: 10.1016/j.syapm.2005.05.004
51. Kilimann, K. V., Kitsubun, P., Delgado, A., Gänzle, M. G., Chapleau, N., Le Bail, A., et al. (2006). Experimental and numerical study of heterogeneous pressure-temperature induced lethal and sublethal injury of Lactococcus lactis in a medium scale high pressure autoclave. Biotechnol. Bioeng. 94, 655-666. doi: 10.1002/bit.20852
52. Kingsley, D. H., Hoover, D. G., Papafragkou, E., and Richards, G. P. (2002). Inactivation of hepatitis A virus and a calicivirus by high hydrostatic pressure. J. Food. Prot. 65, 1605-1609.
53. Koseki, S., and Yamamoto, K. (2006). Recovery of Escherichia coli ATCC 25922 in phosphate buffered saline after treatment with high hydrostatic pressure. Int. J. Food Microbiol. 110, 108-111. doi: 10.1016/j.ijfoodmicro.2006.01.039
54. Koseki, S., and Yamamoto, K. (2007). A novel approach to predicting microbial inactivation kinetics during high pressure processing. Int. J. Food Microbiol. 116, 275-282. doi: 10.1016/j.ijfoodmicro.2007.01.008
55. 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
56. Lavinas, F. C., Miguel, M. A. L., Lopes, M. L. M., and Valente-Mesquita, V. L. (2008). Effect of high hydrostatic pressure on cashew apple (Anacardium occidentale L.) juice preservation. J. Food Sci. 73, 273-277. doi: 10.1111/j.1750-3841.2008.00791.x
57. Lee, S. Y., Chung, H. J., and Kang, D. H. (2006). Combined treatment of high pressure and heat on killing spores of Alicyclobacillus acidoterrestris in apple juice concentrate. J. Food Prot. 69, 1056-1060.
58. Liu, Y., Betti, M., and Gänzle, M. G. (2012). High pressure inactivation of Escherichia coli, Campylobacter jejuni, and spoilage microbiota on poultry meat. J. Food Prot. 75, 497-503. doi: 10.4315/0362-028X.JFP-11-316
59. 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
60. Luscher, C., Balasa, A., Fröhling, A., Ananta, E., and Knorr, D. (2004). Effect of high-pressure-induced ice I-to-ice III phase transitions on inactivation of Listeria innocua in frozen suspension. Appl. Environ. Microbiol. 70, 4021-4029. doi: 10.1128/AEM.70.7.4021-4029.2004
61. 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
62. Mañas, P., and Mackey, B. M. (2004). Morphological and physiological changes induced by high hydrostatic pressure in exponential- and stationary-phase cells of Escherichia coli: relationship with cell death. Appl. Environ. Microbiol. 70, 1545-1554. doi: 10.1128/AEM.70.3.1545-1554.2004
63. Masschalck, B., Van Houdt, R., Van Haver, E. G., and Michiels, C. W. (2001a). Inactivation of gram-negative bacteria by lysozyme, denatured lysozyme, and lysozyme-derived peptides under high hydrostatic pressure. Appl. Environ. Microbiol. 67, 339-344. doi: 10.1128/AEM.67.1.339-344.2001
64. Masschalck, B., Van Houdt, R., and Michiels, C. W. (2001b). High pressure increases bactericidal activity and spectrum of lactoferrin, lactoferricin and nisin. Int. J. Food Microbiol. 64, 325-332. doi: 10.1016/S0168-1605(00)00485-2
65. Mirelman, D., and Siegel, R. C. (1979). Oxidative deamination of aminolysine residues and formation of Schiff base cross linkages in cell envelopes of Escherichia coli. J. Biol. Chem. 254, 571-574
66. Molina-Gutierrez, A., Stippl, V., Delgado, A., Gänzle, M. G., and Vogel, R. F. (2002). Effect of pH on pressure inactivation and intracellular pH of Lactococcus lactis and Lactobacillus plantarum. Appl. Environ. Microbiol., 68, 4399-4406. doi: 10.1128/AEM.68.9.4399-4406.2002
67. Molina-Höppner, A., Doster, W., Vogel, R. F., and Gänzle, M. G. (2004). Protective effect of sucrose and sodium chloride for Lactococcus lactis during sublethal and lethal high-pressure treatments. Appl. Environ. Microbiol. 70, 2013-2020. doi: 10.1128/AEM.70.4.2013-2020.2004
68. Morales, P., Calzada, J., Avila, M., and Nuñez, M. (2008). Inactivation of Escherichia coli O157:H7 in ground beef by single-cycle and multiple-cycle high-pressure treatments. J. Food Prot. 71, 811-815.
69. Nakashima, K., Horikosh, K., and Mizuno, T. (1995). Effect of hydrostatic pressure on the synthesis of outer membrane proteins in Escherichia coli. Biosci. Biotechnol. Biochem. 59, 130-132. doi: 10.1271/bbb.59.130
70. Nakimbugwe, D., Masschalck, B., Anim, G., and Michiels, C. W. (2006). Inactivation of Gram-negative bacteria in milk and banana juice by hen egg white and lambda-lysozyme under high hydrostatic pressure. Int. J. Food Microbiol. 112, 19-25. doi: 10.1016/j.ijfoodmicro.2006.06.010
71. Nikaido, H. (2003). Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67, 593-656. doi: 10.1128/MMBR.67.4.593-656.2003
72. Niven, G. W., Miles, C. A., and Mackey, B. M. (1999). The effects of hydrostatic pressure on ribosome conformation in Escherichia coli: an in vivo study using differential scanning calorimetry. Microbiology 145, 419-425. doi: 10.1099/13500872-145-2-419
73. Omer, M. K., Alvseike, O., Holck, A., Axelsson, L., Prieto, M., Skjerve, E., et al. (2010). Application of high pressure processing to reduce verotoxigenic E. coli in two types of dry-fermented sausage. Meat Sci. 86, 1005-1009. doi: 10.1016/j.meatsci.2010.08.008
74. Pagan, R., and Mackey, B. (2000). Relationship between membrane damage and cell death in pressure-treated Escherichia coli cells: differences between exponential-and stationary-phase cells and variation among strains. Appl. Environ. Microbiol. 66, 2829-2834. doi: 10.1128/AEM.66.7.2829-2834.2000
75. Patterson, M. F., Quinn, M., Simpson, R., and Gilmour, A. (1995). Sensitivity of vegetative pathogens to high hydrostatic pressure treatment in phosphate-buffered saline and foods. J. Food Prot. 58, 524-529.
76. 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
77. Porto-Fett, A. C. S., Call, J. E., Shoyer, B. E., Hill, D. E., Pshebniski, C., Cocoma, G. J., et al. (2010). Evaluation of fermentation, drying, and/or high pressure processing on viability of Listeria monocytogenes, Escherichia coli O157:H7, Salmonella spp., and Trichinella spiralis in raw pork and Genoa salami. J. Food Microbiol. 140, 61-75. doi: 10.1016/j.ijfoodmicro.2010.02.008
78. Reineke, K., Sevenich, R., Hertwig, C., Janßen, T., Fröhling, A., Knorr, D., et al. (2015). Comparative study on the high pressure inactivation behavior of the Shiga toxin-producing Escherichia coli O104:H4 and O157:H7 outbreak strains and a non-pathogenic surrogate. Food Microbiol. 46, 184-194. doi: 10.1016/j.fm.2014.07.017
79. Ritz, M., Feulet, M., Orange, N., and Federighi, M. (2000). Effects of high hydrostatic pressure on membrane proteins of Salmonella typhimurium. Int. J. Food Microbiol. 55, 115-119. doi: 10.1016/S0168-1605(00)00165-3
80. Robey, M., Benito, A., Hutson, R. H., Pascual, C., Park, S. F., and Mackey, B. M. (2001). Variation in resistance to high pressure and rpoS heterogeneity in natural isolates of Escherichia coli 0157:H7. Appl. Environ. Microbiol. 67, 4901-4907. doi: 10.1128/AEM.67.10.4901-4907.2001
81. Rodriguez, E., Arques, J. L., Nuñez, M., Gaya, P., and Medina, M. (2005). Combined effect of high-pressure treatments and bacteriocin-producing lactic acid bacteria on inactivation of Escherichia coli O157:H7 in raw-milk cheese. Appl. Environ. Microbiol. 71, 3399-3404. doi: 10.1128/AEM.71.7.3399-3404.2005
82. Ruan, L., Pleitner, A., 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
83. San Martín, M. F., Barbosa-Cánovas, G. V., and Swanson, B. G. (2002). Food processing by high hydrostatic pressure. Crit. Rev. Food Sci. Nutr. 42, 627-645. doi: 10.1080/20024091054274
84. Sleator, R. D., and Hill, C. (2002). Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol. Rev. 26, 49-71. doi: 10.1111/j.1574-6976.2002.tb00598.x
85. Smelt, J. P. P. M. (1998). Recent advances in the microbiology of high pressure processing. Trends Food Sci. Technol. 9, 152-158. doi: 10.1016/S0924-2244(98)00030-2
86. Smiddy, M., Sleator, R. D., Patterson, M. F., Hill, C., and Kelly, A. L. (2004). Role for compatible solutes glycine betaine and L-carnitine in listerial barotolerance. Appl. Environ. Mcirobiol. 70, 7555-7557. doi: 10.1128/AEM.70.12.7555-7557.2004
87. Souzu, H. (1986). Fluorescence polarization studies on Escherichia coli membrane stability and its relation to the resistance of the cell to freeze-thawing. I. Membrane stability in cells of different growth phase. Biochim. Biophys. Acta 861, 353-360. doi: 10.1016/0005-2736(86)90438-4
88. Tassou, C. C., Panagou, E. Z., Samaras, F. J., Galiatsatou, P., and Mallidis, C. G. (2008). Temperature-assisted high hydrostatic pressure inactivation of Staphylococcus aureus in a ham model system: evaluation in selective and nonselective medium. J. Appl. Microbiol. 104, 1764-1773. doi: 10.1111/j.1365-2672.2007.03698.x
89. Teo, A. Y., Ravishankar, S., and Sizer, C. E. (2001). Effect of low temperature, high-pressure treatment on the survival of Escherichia coli O157:H7 and Salmonella in unpasteurized fruit juices. J. Food Prot. 64, 1122-1127.
90. Tonello, C. (2011). "Case studies for high pressure processing of foods," in Non-Thermal Processing Technologies for Food, eds H. Q. Zhang, G. V. Barbosa-Canovas, and V. M. Balasubramaniam (WestSussex: Whiley-Blackwell), 36-50.
91. Ukuku, D. O., Yamamoto, K., Bari, L., Mukhopadhaya, S., Juneja, V., and Kawamoto, S. (2013). Membrane damage and viability loss of E. coli O157:H7 and Salmonella spp in apple juice treated with high hydrostatic pressure and thermal death time disks. J. Food Process. Technol. 4, 236. doi: 10.4172/2157-7110.1000236
92. Ulmer, H. M., Herberhold, H., Fahsel, S., Gänzle, M. G., Winter, R., and Vogel, R. F. (2002). Effects of pressure induced membrane phase transitions on HorA inactivation in Lactobacillus plantarum. Appl. Environ. Microbiol. 68, 1088-1095. doi: 10.1128/AEM.68.3.1088-1095.2002
93. Vaara, M. (1992). Agents that increase the permeability of the outer membrane. Microbiol. Rev. 56, 395-411.
94. Vanlint, D., Rutten, N., Michiels, C. S., and Aertsen, A. (2012). Emergence and stability of high pressure resistance in different foodborne pathogens. Appl. Environ. Microbiol. 78, 3234-3241. doi: 10.1128/AEM.00030-12
95. Vanlint, D., Rutten, N., Govers, S. K., Michiels, C. W., and Aertsen, A. (2013a). Exposure to high hydrostatic pressure rapidly selects for increased RpoS activity and general stress-resistance in Escherichia coli O157:H7. Int. J. Food Microbiol. 163, 28-33. doi: 10.1016/j.ijfoodmicro.2013.02.001
96. Vanlint, D., Pype, B. J., Rutten, N., Vanoirbeek, K. G., Michiels, C. W., and Aertsen, A. (2013b). Loss of cAMP/CRP regulation confers extreme high hydrostatic pressure resistance in Escherichia coli O157:H7. Int. J. Food Microbiol. 166, 65-71. doi: 10.1016/j.ijfoodmicro.2013.06.020
97. Van Opstal, I., Vanmuysen, S. C., and Michiels, C. W. (2003). High sucrose concentration protects E. coli against high pressure inactivation but not against high pressure sensitization to the lactoperoxidase system. Int. J. Food Microbiol. 88, 1-9. doi: 10.1016/S0168-1605(03)00070-9
98. Vercammen, A., Vanoirbeek, K. G. A., Lemmens, L., Lurquin, I., Hendrickx, M. E. G., and Michiels, C. W. (2012). High pressure pasteurization of apple pieces in syrup: microbiological shelf-life and quality evolution during refrigerated storage. Innov. Food Sci. Emerg. Technol. 16, 259-266. doi: 10.1016/j.ifset.2012.06.009
99. Welch, T. J., Farewell, A., Neidhardt, F. C., and Bartlett, D. H. (1993). Stress response of Escherichia coli to elevated hydrostatic pressure. J. Bacteriol. 175, 7170-7177.
100. Whitney, B. M., Williams, R. C., Eifert, J., and Marcy, J. (2007). High-pressure resistance variation of Escherichia coli O157:H7 strains and Salmonella serovars in tryptic soy broth, distilled water, and fruit juice. J. Food Prot. 70, 2078-2083.
101. Whitney, B. M., Williams, R. C., Eifert, J., and Marcy, J. (2008). High pressures in combination with antimicrobials to reduce Escherichia coli O157:H7 and Salmonella Agona in apple juice and orange juice. J. Food Prot. 71, 820-824.
102. Winter, R. (2002). Synchrotron X-ray and neutron small-angle scattering of lyotropic lipid mesophases, model biomembranes and proteins in solution at high pressure. Biochim. Biophys. Acta. 1595, 160-184. doi: 10.1016/S0167-4838(01)00342-9
103. Wouters, P. C., Glaasker, E., and Smelt, J. P. P. M. (1998). Effects of high pressure on inactivation kinetics and events related to proton efflux in Lactobacillus plantarum. Appl. Environ. Microbiol. 64, 509-514.
104. Yan, Y., Waite-Cusic, J. G., Kuppusamy, P., and Yousef, A. E. (2013). Intracellular free iron and its potential role in ultrahigh-pressure-induced inactivation of Escherichia coli. Appl. Environ. Microbiol. 79, 722-724. doi: 10.1128/AEM.02202-12
105. 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
106. Zhu, M., Du, M., Cordray, J., and Ahn, D. U. (2005). Control of Listeria monocytogenes contamination in ready-to-eat meat products. Compr. Rev. Food Sci. Food Saf. 4, 34-42. doi: 10.1111/j.1541-4337.2005.tb00071.x