Chapter 1 : Growth, Survival, and Death of Microbes in Foods

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Food microbiologists must understand microbiology and food systems and be able to integrate them to solve problems in complex food ecosystems. This chapter addresses this in three parts by (i) examining foods as ecosystems and discussing intrinsic and extrinsic environmental factors that control bacterial growth, (ii) explaining first-order or pseudo-first-order kinetics which govern the log phase of microbial growth and many types of lethality, and (iii) focusing on physiology and metabolism of foodborne microbes. Growth of in foods such as potatoes and sauteed onions exposed to air has caused botulism outbreaks. Bacteria are classified as psychrophiles, psychrotrophs, mesophiles, and thermophiles according to the way in which temperature influences their growth. Additional barriers to microbial growth should be incorporated into refrigerated foods containing no other inhibitors. Food microbiology is concerned with all four phases of microbial growth. Growth curves showing the lag, exponential logarithmic or log, stationary, and death phases of a culture are normally plotted as the number of cells on a logarithmic scale or log cell number versus time. These plots represent the states of microbial populations rather than individual microbes. Thus, both the lag phase and stationary phase of growth represent periods when the growth rate equals the death rate to produce no net change in cell numbers. Food microbiologists frequently use doubling times (t) to describe growth rates of foodborne microbes. Developments in molecular biology and microbial ecology will change or deepen the perspective about the growth of microbes in foods.

Citation: Montville T, Matthews K. 2007. Growth, Survival, and Death of Microbes in Foods, p 3-22. In Doyle M, Beuchat L (ed), Food Microbiology: Fundamentals and Frontiers, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815912.ch1
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Figure 1.1

Relative growth rates of bacteria at different temperatures.

Citation: Montville T, Matthews K. 2007. Growth, Survival, and Death of Microbes in Foods, p 3-22. In Doyle M, Beuchat L (ed), Food Microbiology: Fundamentals and Frontiers, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815912.ch1
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Figure 1.2

Major catabolic pathways used by foodborne bacteria.

Citation: Montville T, Matthews K. 2007. Growth, Survival, and Death of Microbes in Foods, p 3-22. In Doyle M, Beuchat L (ed), Food Microbiology: Fundamentals and Frontiers, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815912.ch1
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Figure 1.3

Proton motive force can be generated by respiration, ATP hydrolysis, end-product efflux, or anion exchange mechanisms. Modified from reference .

Citation: Montville T, Matthews K. 2007. Growth, Survival, and Death of Microbes in Foods, p 3-22. In Doyle M, Beuchat L (ed), Food Microbiology: Fundamentals and Frontiers, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815912.ch1
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Figure 1.4

Transport can be at the direct expense of high-energy phosphate bonds or can be linked to the proton gradient of the proton motive force.

Citation: Montville T, Matthews K. 2007. Growth, Survival, and Death of Microbes in Foods, p 3-22. In Doyle M, Beuchat L (ed), Food Microbiology: Fundamentals and Frontiers, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815912.ch1
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Figure 1.5

Data indicative of injury and repair. (a) When bacteria are plated on selective (○) or nonselective (●) media during exposure to some stressor (e.g., heat), the decrease in CFU on a nonselective medium represents the true lethality, while the difference between the values obtained on each medium is defined as “injury.” (b) During “repair,” resistance to selective agents is regained, and the value obtained on the selective medium approaches that of the nonselective medium. Unstressed controls are shown at the top of panel b. Modified and redrawn from reference .

Citation: Montville T, Matthews K. 2007. Growth, Survival, and Death of Microbes in Foods, p 3-22. In Doyle M, Beuchat L (ed), Food Microbiology: Fundamentals and Frontiers, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815912.ch1
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Figure 1.6

Data showing changes of plate count and cell morphology during development of the VNC state induced by temperature downshifts (at time 0 and ↓) and resuscitation by temperature upshifts (↑). Reprinted from reference with permission.

Citation: Montville T, Matthews K. 2007. Growth, Survival, and Death of Microbes in Foods, p 3-22. In Doyle M, Beuchat L (ed), Food Microbiology: Fundamentals and Frontiers, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815912.ch1
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1. Arnold, C. N.,, J. McElhanon,, A. Lee,, R. Leonhart, and, D. A. Siegele. 2001. Global analysis of Escherichia coli gene expression during the acetate-induced acid tolerance response. J. Bacteriol. 183: 21782186.
2. Bang, I. S.,, B. H. Kim,, J. W. Foster, and, Y. K. Park. 2000. ompR regulates the stationary-phase acid tolerance response of Salmonella enterica serovar Typhimurium. J. Bacteriol. 182: 22452252.
3. Bang, I. S.,, J. P. Audia,, Y. K. Park, and, J. W. Foster. 2002. Autoinduction of the ompR response regulator by acid shock and control of the Salmonella enterica acid tolerance response. Mol. Microbiol. 44: 12351250.
4. Barer, M. R.,, L. T. Gribbon,, C. R. Harwood, and, C. E. Nwaguh. 1993. The viable but non-culturable hypothesis and medical bacteriology. Rev. Med. Microbiol. 4: 183191.
5. Barer, M. R., and, C. R. Harwood. 1999. Bacterial viability and culturability. Adv. Microb. Physiol. 41: 93137.
6. Bassler, B. L. 2002. Small talk: cell-to-cell communication in bacteria. Cell 109: 421424.
7. Bauer, W. D.,, U. Mathesius, and, M. Teplitski. 2005. Eukaryotes deal with quorum sensing. ASM News 71: 129135.
8. Bayles, D. O.,, B. A. Annous, and, B. J. Wilkinson. 1996. Cold stress proteins induced in Listeria monocytogenes in response to temperature downshock and growth at low temperatures. Appl. Environ. Microbiol. 62: 11161119.
9. Bearson, B. L.,, L. Wilson, and, J. W. Foster. 1998. A low pH-inducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J. Bacteriol. 180: 24092417.
10. Bearson, S.,, B. Bearson, and, J. W. Foster. 1997. Acid stress responses in enterobacteria. FEMS Microbiol. Lett. 147: 173180.
11. Beltrametti, F.,, A. U. Kresse, and, C. A. Guzman. 1999. Transcriptional regulation of esp genes of enterohemorrhagic Escherichia coli. J. Bacteriol. 181: 34093418.
12. Besnard, V.,, M. Federighi, and, J. M. Cappelier. 2000. Development of a direct viable count procedure for the investigation of VBNC state in Listeria monocytogenes. Lett. Appl. Microbiol. 31: 7781.
13. Beuchat, L. R. 1978. Injury and repair of gram-negative bacteria with special consideration of the involvement of the cytoplasmic membrane. Adv. Appl. Microbiol. 23: 219243.
14. Board, R. G.,, D. Jones,, R. G. Kroll, and, G. L. Pettipher (ed). 1992. Ecosystems: microbes: food. J. Appl. Bacteriol. 73: 1S178S.
15. Boddy, L., and, J. W. T. Wimpenny. 1992. Ecological concepts in food microbiology. J. Appl. Bacteriol. 73: 23S38S.
16. Bogosian, G.,, N. D. Aardema,, E. V. Bourneauf,, P. J. Morris, and, J. P. O’Neil. 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: 50705075.
17. Bogosian, G.,, P. J. L. Morris, and, J. P. O’Neil. 1998. A mixed culture recovery method indicates that enteric bacteria do not enter the viable but nonculturable state. Appl. Environ. Microbiol. 64: 17361742.
18. Bonnet, M. 2005. Acid tolerance response of Listeria monocytogenes: bioenergetics and mechanisms of resistance to the antimicrobial nisin. Ph.D. dissertation. The Graduate School, Rutgers, the State University of New Jersey, New Brunswick.
19. Bonnet, M., and, T. J. Montville. 2005. Acid-tolerant Listeria monocytogenes persist in a model food system fermented with nisin-producing bacteria. Lett. Appl. Microbiol. 40: 237242.
20. Boyd, A., and, A. M. Chakrabarty. 1995. Pseudomonas aeruginosa biofilms: role of the alginate exopolysaccha-ride. J. Ind. Microbiol. 15: 162168.
21. Bouwer, P., and, T. Abee. 2000. Assessment of viability of microorganisms employing fluorescence techniques. Int. J. Food Microbiol. 55: 193200.
22. Brandl, M. T.,, W. G. Miller,, A. H. Bates, and, R. E. Mandrell. 2005. Production of autoinducer-2 in Salmonella enterica serovar Thompson contributes to its fitness in chickens, but not in cilantro leaf surfaces. Appl. Environ. Microbiol. 71: 26532662.
23. Brock, T. D., and, M.T. Madigan. 1988. Biology of Microorganisms, p. 793795. Prentice Hall, Englewood Cliffs, N.J.
24. Brondsted, L.,, B. H. Kallipolitis,, H. J. Ingmer, and, S. Knochel. 2003. KdpE and a putative RsbQ homologue contribute to growth of Listeria monocytogenes at high osmolarity and low temperature. FEMS Microbiol. Lett. 219: 233239.
25. Bruhn, J. B.,, A. B. Christensen,, L. R. Flodgaard,, K. F. Nielsen,, T. O. Larson,, M. Givskov, and, L. Gram. 2004. Presence of acylated homoserine lactones (AHLs) of AHL-producing bacteria in meat and potential role of AHL in spoilage of meat. Appl. Environ. Microbiol. 70: 42934302.
26. Bull, M. K.,, M. M. Hayman,, C. M. Stewart,, E. A. Szabo, and, S. J. Knabel. 2005. Effect of prior growth temperature, type of enrichment medium, and temperature and time of storage on recovery of Listeria monocytogenes following high pressure processing of milk. Int. J. Food Microbiol. 101: 5361.
27. Busta, F. F. 1978. Introduction to injury and repair of microbial cells. Adv. Appl. Microbiol. 23: 195201.
28. Byrd, J. J.,, H.-S. Xu, and, R. R. Colwell. 1991. Viable but nonculturable bacteria in drinking water. Appl. Env. Microbiol. 57: 875878.
29. Carpentier, B., and, O. Cerf. 1993. Biofilms and their consequences, with particular reference to hygiene in the food industry. J. Appl. Bacteriol. 75: 499511.
30. Castanie-Cornet, M.,, T. A. Penfound,, D. Smith,, J. F. Elliot, and, J. W. Foster. 1999. Control of acid resistance in Escherichia coli. J. Bacteriol. 181: 35253535.
31. Chmielewski, R., and, J. F. Frank. 1995. Formation of viable but nonculturable Salmonella during starvation in chemically defined solutions. Lett. Appl. Microbiol. 20: 380384.
32. Cho, J. C., and, S. J. Kim. 1999. Green fluorescent protein-based direct viable count to verify a viable but non-culturable state of Salmonella typhi in environmental samples. J. Microbiol. Methods 36: 227235.
33. Choi, S. H.,, D. J. Baumler, and, C. W. Kasper. 2000. Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 66: 39113916.
34. Cloak, O. M.,, B. T. Solow,, C. Briggs,, C. Y. Chen, and, P. M. Fratamico. 2002. Quorum sensing and production of antoinducer-2 in Campylobacter spp., E. coli O157:H7, and Salmonella enterica serovar Typhimurium in foods. Appl. Environ. Microbiol. 68: 46664671.
35. Conte, M. P.,, C. Longhi,, G. Petrone,, M. Polidoro,, P. Valenti, and, L. Seganti. 1994. Listeria monocytogenes infection of Caco-2 cells: role of growth temperature. Res. Microbiol. 145: 677682.
36. Cossins, A. R., and, M. Sinensky. 1984. Adaptation of membranes to temperature, pressure and exogenous lipids, p. 120. In M. Shinitzky (ed.), Physiology of Membrane Fluidity. CRC Press, Boca Raton, Fla.
37. Costerton, J. W. 1995. Overview of microbial biofilms. J. Ind. Microbiol. 15: 137140.
38. Crawford, R. W.,, C. M. Belizeau,, T. J. Poeler,, C. W. Donnelly, and, U. K. Bunning. 1989. Comparative recovery of uninjured and heat-injured Listeria monocytogenes cells from bovine milk. Appl. Environ. Microbiol. 55: 14901494.
39. Davies, D. G.,, M. R. Parsek,, J. P. Pearson,, B. H. Iglewski,, J. W. Costeron, and, E. P. Greenberg. 1997. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science. 280: 295298.
40. Day, A. P., and, J. D. Oliver. 2004. Changes in membrane fatty acid composition during entry of Vibrio vulnificus into a viable but nonculturable state. J. Microbiol. 42: 6973.
41. Duffy, G.,, D. C. Riordan,, J. J. Sheridan,, J. E. Call,, R. C. Whiting,, I. S. Blair, and, D. A. McDowell. 2000. Effect of pH on survival, thermotolerance, and verotoxin production of Escherichia coli O157:H7 during simulated fermentation and storage. J. Food Prot. 63: 1218.
42. Duncan, S.,, L. A. Glover,, K. Killham, and, J. I. Prosser. 1994. Luminescence-based detection of activity of starved and viable but nonculturable bacteria. Appl. Environ. Microbiol. 60: 13081316.
43. Dussurget, O.,, E. Dumas,, C. Archambaud,, I. Chafsey,, C. Chambon,, M. Hebraud, and, P. Cossart. 2005. Listeria monocytogenes ferritin protects against multiple stresses and is required for virulence. FEMS Microbiol. Lett. 250: 253261.
44. Elhanafi, D.,, B. Leenanon,, W. Bang, and, M. A. Drake. 2004. Impact of cold and cold-acid stress on poststress tolerance and virulence factor expression of Escherichia coli O157:H7. J. Food Prot. 67: 1926.
45. El-Kest, S. E., and, E. H. Marth. 1991. Injury and death of frozen Listeria monocytogenes as affected by glycerol and milk components. J. Dairy Sci. 74: 12011208.
46. El-Kest, S. E., and, E. H. Marth. 1991. Strains and suspending menstrua as factors affecting death and injury of Listeria monocytogenes during freezing and frozen storage. J. Dairy Sci. 74: 12091213.
47. Elstner, E. F., and, A. Heupel. 1973. On the decarboxylation of α-keto acid by isolated chloroplasts. Biochim. Biophys. Acta 352: 182188.
48. Farber, J. M., and, B. E. Brown. 1990. Effect of prior heat shock on heat resistance of Listeria monocytogenes in meat. Appl. Environ. Microbiol. 56: 15841587.
49. Farkas, J. 1994. Tolerance of spores to ionizing radiation: mechanisms of inactivation, injury, and repair. J. Appl. Bacteriol. 76: 81S90S.
50. Fedio, W. M., and, H. Jackson. 1989. Effect of tempering on the heat resistance of Listeria monocytogenes. Lett. Appl. Microbiol. 9: 157160.
51. Feeherry, F. E.,, D. T. Munsey, and, D. B. Rowley. 1987. Thermal inactivation and injury of Bacillus stearothermophilus spores. Appl. Environ. Microbiol. 53: 365370.
52. Foegoding, P. M., and, F. F. Busta. 1981. Bacterial spore injury—an update. J. Food Prot. 44: 776786.
53. Foster, J. W., and, H. K. Hall. 1991. Inducible pH homeostasis and the acid tolerance response of Salmonella typhimurium. J. Bacteriol. 173: 51295135.
54. Foster, J. W.,, Y. K. Park,, L. S. Bang,, K. Karem,, H. Betts,, H. K. Hall, and, E. Shaw. 1994. Regulatory circuits involved with pH-regulated gene expression in Salmonella typhimurium. Microbiology 140: 341352.
55. Frank, J. F., and, R. A. Koffi. 1990. Surface-adherent growth of Listeria monocytogenes is associated with increased resistance to surfactant sanitizers and heat. J. Food Prot. 48: 740742.
56. Fratamico, P. M. 2003. Tolerance to stress and ability of acid-adapted and non-acid-adapted Salmonella enterica serovar Typhimurium DT104 to invade and survive in mammalian cells in vitro. J. Food Prot. 66: 11151125.
57. Fuqua, C., and, E. P. Greenberg. 1998. Cell-to-cell communication in Escherichia coli and Salmonella typhimurium: they may be talking, but who’s listening? Proc. Natl. Acad. Sci. USA 95: 65716572.
58. Gould, G. W. 1995. Homeostatic mechanisms during food preservation by combined methods, p. 397410. In G. V. Barbosa-Canovas and, J. Welti-Chanes (ed.), Food Preservation by Moisture Control. Technomic Publishing Co., Inc., Lancaster, Pa.
59. Gracia, K. S., and, J. L. McKillip. 2004. A review of conventional detection and enumeration methods for pathogenic bacteria in food. Can. J. Microbiol. 50: 883890.
60. Gram, L.,, L. Ravin,, M. Rasch,, J. B. Bruhn,, A. B. Christensen, and, M. Givskov. 2002. Food spoilage—interactions between food spoilage bacteria. Int. J. Food Microbiol. 78: 7997.
61. Gupte, A. R.,, C. L. Rezende, and, S. W. Joseph. 2003. Induction and resuscitation of viable but nonculturable Salmonella enterica serovar Typhimurium DT104. Appl. Environ. Microbiol. 69: 66696675.
62. Hara-Kudo, Y.,, M. Ifedo,, H. Kodaka,, H. Nakagawa,, K. Goto,, T. Masuda,, H. Konuma,, T. Kojima, and, S. Kumagai. 2000. Selective enrichment with resuscitation step for isolation of freeze-injured Escherichia coli O157:H7 from foods. Appl. Environ. Mircobiol. 66: 28662872.
63. Harold, F. M. 1981. The Vital Force: a Study of Bioenergetics. W. H. Freeman & Company, New York, N.Y.
64. Hellingwerf, K. J.,, W. C. Crieland,, M. J. T. de Mattos,, W. D. Hoff,, R. Kort,, D. T. Verhamme, and, C. Avignone-Rosa. 1998. Current topics in signal transduction in bacteria. Antonie Leeuwenhoek 74: 211227.
65. International Commission on Microbiological Specifications for Foods. 1980. Injury and its effect on recovery, p. 205214. In Microbial Ecology of Foods, vol. 1. Factors Affecting Life and Death of Microorganisms. Academic Press, Inc., New York, N.Y.
66. Jay, J. M.,, J. P. Vilai, and, M. E. Huges. 2003. Profile and activity of bacteria biota of ground beef held from freshness to spoilage at 5–7°C. Int. J. Food Microbiol. 81: 105111.
67. Juneja, V. K.,, P. G. Klein, and, B. S. Marmer. 1998. Heat shock and thermotolerance of Escherichia coli O157:H7 in a model beef gravy system and ground beef. J. Appl. Microbiol. 84: 677684.
68. Kashket, E. R. 1987. Bioenergetics of lactic acid bacteria: cytoplasmic pH and osmotolerances. FEMS Microbiol. Rev. 46: 233244.
69. Kell, D. B.,, A. S. Kaprelyants,, D. H. Weichart,, C. R. Harwood, and, M. R. Barer. 1998. Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Antonie Leeuwenhoek 73: 169187.
70. Ko, R.,, L. T. Smith, and, G. M. Smith. 1994. Glycine betaine confers enhanced osmotolerance and cryotolerance in Listeria monocytogenes. J. Bacteriol. 176: 426431.
71. Kobayashi, H.,, T. Miyamoto,, Y. Hashimoto,, M. Kirki,, A. Motomatsu,, K. Honjoh, and, M. Iio. 2005. Identification of factors involved in recovery of heat-injured Salmonella enteritidis. J. Food Prot. 68: 932941.
72. Konings, W. N.,, J. Kok,, O. P. Kuipers, and, B. Poolman. 2000. Lactic acid bacteria: the bugs of the new millennium. Curr. Opin. Microbiol. 3: 276282.
73. Korem, M.,, A. S. Sheoran,, Y. Gov,, S. Tzipori,, I. Borovok, and, N. Balahan. 2003. Characterization of RAP, a quorum sensing activator of Staphylococcus aureus. FEMS Microbiol. Lett. 223: 165175.
74. Koutsoumanis, K. P., and, J. N. Sofos. 2004. Comparative acid stress response of Listeria monocytogenes, Escherichia coli O157:H7 and Salmonella Typhimurium after habituation at different pH conditions. Lett. Appl. Microbiol. 38: 321326.
75. Kuipers, O. P.,, P. G. G. A. de Ruyter,, M. Kleerebezem, and, W. M. de Vos. 1998. Quorum sensing-controlled gene expression in lactic acid bacteria. J. Biotechnol. 64: 1521.
76. Kumar, C. G., and, S. K. Anand. 1998. Significance of microbial biofilms in food industry: a review. Int. J. Food Microbiol. 42: 927.
77. Kwon, Y. M., and, S. C. Ricke. 1998. Induction of acid resistance of Salmonella typhimurium by exposure to short-chain fatty acids. Appl. Environ. Mircrobiol. 64: 34583463.
78. Leenanon, B., and, M. A. Drake. 2001. Acid stress, starvation, and cold stress affect poststress behavior of Escherichia coli O157:H7 and nonpathogenic Escherichia coli. J. Food Prot. 64: 970974.
79. Leimeister-Wachter, M.,, E. Domann, and, T. Chakraborty. 1992. The expression of virulence genes in Listeria monocytogenes is thermoregulated. J. Bacteriol. 174: 947952.
80. Leistner, L. 1994. Principles and applications of hurdle technology, p. 121. In G. W. Gould (ed.), New Methods of Food Preservation. Blackie Academic and Professional, Glasgow, Scotland.
81. Leyer, G.J., and, E. A. Johnson. 1993. Acid adaptation induces cross-protection against environmental stresses in Salmonella typhimurium. Appl. Environ. Microbiol. 59: 18421847.
82. Likimani, T. A., and, J. N. Sofos. 1990. Bacterial spore injury during extrusion cooking of corn/soybean mixtures. Int. J. Food Microbiol. 11: 243249.
83. Linton, R. H.,, J. B. Webster,, M. D. Pierson,, J. R. Bishop, and, C. R. Hackney. 1992. The effect of sublethal heat shock and growth atmosphere on the heat resistance of Listeria monocytogenes Scott A. J. Food Prot. 55: 8487.
84. Liu, L.,, M. E. Hume, and, S. D. Pillai. 2004. Autoinducer-2-like activity associated with foods and its interaction with food additives. J. Food Prot. 67: 14571462.
85. Lund, B. M. 1992. Ecosystems in vegetable foods. J. Appl. Bacteriol. 73: 115S126S.
86. Mafart, P. 2000. Taking injuries of surviving bacteria into account for optimizing heat treatments. Int. J. Food Microbiol. 55: 175179.
87. Mahapatra, A. K.,, K. Muthukumarappan, and, J. L. Julson. 2005. Application of ozone, bacteriocins and irradiation in food processing: a review. Cit. Rev. Food Sci. Nutr. 45: 447461.
88. Maloney, P. C. 1990. Microbes and membrane biology. FEMS Microbiol. Rev. 87: 91102.
89. McDougald, D.,, S. A. Rice,, D. Weichart, and, S. Kjelleberg. 1998. Nonculturability: adaptation or debilitation? FEMS Microbiol. Ecol. 25: 19.
90. McEntire, J. C.,, G. M. Carman, and, T. J. Montville. 2004. Increased ATPase activity is responsible for acid sensitivity of nisin-resistant Listeria monocytogenes ATCC 700302. Appl. Environ. Microbiol. 70: 27172721.
91. McKay, A. M. 1992. Viable but non-culturable forms of potentially pathogenic bacteria in water. Lett. Appl. Microbiol. 14: 129135.
92. Meyer, D. H., and, C. W. Donnelly. 1992. Effect of incubation temperature on repair of heat-injured Listeria in milk. J. Food Prot. 55: 579582.
93. Michels, P. A. M.,, J. P. J. Michels,, J. Boonstra, and, W. L. Konings. 1979. Generation of an electrochemical proton gradient in bacteria by the excretion of metabolic end products. FEMS Microbiol. Lett. 5: 357364.
94. Mikulskis, A. V.,, I. Delor,, V. H. Thi, and, G. R. Cornelis. 1994. Regulation of Yersinia enterocolitica enterotoxin yst gene. Influence of growth phase, temperature, osmolarity, pH and bacterial host factors. Mol. Microbiol. 14: 905915.
95. Miller, M. B., and, B. L. Bassler. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55: 165169.
96. Miller, M. B.,, K. Skorupski,, D. H. Lenz,, R. K. Taylor, and, B. L. Bassler. 2002. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110: 303314.
97. Mizunoe, Y.,, S.N. Wai,, A. Takade, and, S. Yoshida. 1999. Restoration of culturability of starvation-stressed and low temperature-stressed Escherichia coli O157 cells by using H 2O 2-degrading compounds. Arch. Microbiol. 172: 6367.
98. Mizunoe, Y.,, S. N. Wai,, T. Ishikawa,, A. Takade, and, S. Yoshida. 2000. Resuscitation of viable but non-culturable cells of Vibrio parahaemolyticus induced at low temperature under starvation. FEMS Microbiol. Lett. 186: 115120.
99. Mossel, D. A. A., and, C. B. Struijk. 1992. The contribution of microbial ecology to management and monitoring of the safety, quality and acceptability (SQA) of foods. J. Appl. Bacteriol. 73: 1S22S.
100. Murano, E. A., and, M. O. Pierson. 1993. Effect of heat shock and incubation atmosphere on injury and recovery of Escherichia coli O157:H7. J. Food Prot. 56: 568572.
101. Murley, Y. M.,, P. A. Carrol,, K. Skorupski,, R. K. Taylor, and, S. B. Calderwood. 1999. Differential transcription of the tcpPH operon confers biotype-specific control of the Vibrio cholerae ToxR virulence regulon. Infect. Immun. 67: 51175123.
102. National Food Processors Association. 1988. Factors to be considered in establishing good manufacturing practices for the production of refrigerated food. Dairy Food Sanit. 8: 288291.
103. Ngutter, C., and, C. Donnelly. 2003. Nitrate-induced injury of Listeria monocytogenes and the effect of selective versus nonselective recovery procedures on its isolation from frankfurters. J. Food Prot. 66: 22522257.
104. Nicholls, D. G., and, S. J. Ferguson. 1992. Bioenergetics 2. Academic Press, San Diego, Calif.
105. Nilsson. L.,, J. D. Oliver, and, S. Kjelleberg. 1991. Resuscitation of Vibrio vulnificus from the viable but nonculturable state. J. Bacteriol. 173: 50545059.
106. Novick, R. P. 1999. Regulation of pathogenicity in Staphylococcus aureus by a peptide-based density-sensing system, p. 129146. In G. M. Dunny and, S. C. Winns (ed.), Cell-Cell Signaling in Bacteria. ASM Press, Washington, D.C.
107. Nystrom, T. 1998. To be or not to be: the ultimate decision of the growth-arrested bacterial cell. FEMS Microbiol. Rev. 21: 283290.
108. Olasupo, N. A.,, D. J. Fitzgerald,, A. Narbad, and, M. J. Gasson. 2004. Inhibition of Bacillus subtilis and Listeria innocua by nisin in combination with some naturally occurring organic compounds. J. Food Prot. 67: 596600.
109. Oliver, J. D. 2005. The viable but nonculturable state in bacteria. J. Microbiol. 43: 93100.
110. Oliver, J. D., and, R. Bocklan. 1995. In vivo resuscitation, and virulence towards mice, of viable but nonculturable cells of Vibrio vulnificus. Appl. Environ. Microbiol. 61: 26202623.
111. Oliver, J. D.,, M. Dagher, and, K. Linden. 2005. Induction of Escherichia coli and Salmonella typhimurium into the viable but nonculturable state following chlorination of wastewater. J. Water Health 3: 249257.
112. Oliver, J. D.,, F. Hite,, D. McDougald,, N. L. Andon, and, L. M. Simpson. 1995. Entry into, and resuscitation from, the viable but nonculturable state by Vibrio vulnificus in an estuarine environment. Appl. Environ. Microbiol. 61: 26242630.
113. Olson, E. R. 1993. Influence of pH on bacterial gene expression. Mol. Microbiol. 8: 514.
114. Otto, M. 2001. Staphylococcus aureus and Staphylococcus epidermidis peptide pheromones produced by accessory gene regulator agr system. Peptides 22: 16031608.
115. Pai, S.,, J. K. Actor,, E. Sepulveda,, R. L. Hunter, and, C. Jegannath. 2000. Identification of viable and non-viable Mycobacterium tuberculosis in mouse organs by directed RT-PCR for antigen 85B mRNA. Microb. Pathog. 28: 335342.
116. Palumbo, S. A. 1986. Is refrigeration enough to restrain foodborne pathogens? J. Food Prot. 49: 10031009.
117. Pepe, J. C.,, J. L. Badger, and, V. L. Miller. 1994. Growth phase and low pH affect the thermal regulation of the Yersinia enterocolitica inv gene. Mol. Microbiol. 11: 123135.
118. Phan-Thanh, L.,, F. Mahouin, and, S. Alige. 2000. Acid responses of Listeria monocytogenes. Int. J. Food Microbiol. 55: 121126.
119. Quadri, L. E. N. 2002. Regulation of antimicrobial peptide production by autoinducer mediated quorum sensing in lactic acid bacteria. Antonie Leeuwenhoek 83: 133145.
120. Rollins, D. M., and, R. R. Colwell. 1986. Viable but nonculturable stage of Campylobacter jejuni and its role in survival in the natural aquatic environment. Appl. Environ. Microbiol. 52: 531538.
121. Sallam, S. S., and, C. W. Donnelly. 1992. Destruction, injury and repair of Listeria species exposed to sanitizing compounds. J. Food Prot. 59: 771776.
122. Sampathkumar, B.,, G. G. Khachatourians, and, D. R. Korber. 2004. Treatment of Salmonella enterica serovar Enteritidis with a sublethal concentration of trisodium phosphate or alkaline pH induces thermotolerance. Appl. Environ. Microbiol. 70: 46134620.
123. Schuhmacker, D. A., and, K. E. Klose. 1999. Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. J. Bacteriol. 181: 15081514.
124. Sinensky, M. 1974. Homeoviscous adaptation—a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc. Natl. Acad. Sci. USA 71: 522525.
125. Sircili, M. P.,, M. Matthews,, L. R. Trabulsi, and, V. Sperandio. 2004. Modulation of enteropathogenic Escherichia coli virulence by quorum sensing. Infect. Immun. 72: 23292337.
126. Skurnik, M. 1985. Expression of antigens encoded by the virulence plasmid of Yersinia enterocolitica under different growth conditions. Infect. Immun. 47: 183190.
127. Slonczewski, J. L., and, J. W. Foster. 1999. pH-regulated genes and survival at extreme pH. In F. C. Neidhardt et al. (ed.), Escherichia coli and Salmonella: Cellular and Molecular Biology. ASM Press, Washington, D.C.
128. Smith, J. L.,, P. M. Fratamico, and, J. S. Novak. 2004. Quorum sensing: a primer for food microbiologists. J. Food Prot. 67: 10531070.
129. Smith, J. L.,, B. S. Marmer, and, R. C. Benedict. 1991. Influence of growth temperature on injury and death of Listeria monocytogenes Scott A during a mild heat treatment. J. Food Prot. 54: 166169.
130. Somers, E. B.,, J. L. Schoeni, and, A. C. L. Wong. 1994. Effect of trisodium phosphate on biofilm and planktonic cells of Campylobacter jejuni, Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella typhimurium. Int. J. Food Microbiol. 22: 269276.
131. Sturme, M. H. L.,, M. Kleerebezem,, J. Nakayama,, A. D. L. Akkermans,, E. E. Vaughan, and, W. M. de Vos. 2002. Cell-to-cell communication by autoinducing peptides in gram-positive bacteria. Antonie Leeuwenhoek 81: 233243.
132. Surette, M. G., and, B. L. Bassler. 1998. Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 95: 70467050.
133. Talibart, R.,, M. Denis,, A. Castillo,, J. M. Cappelier, and, G. Ermel. 2000. Survival and recovery of viable but non-cultivable forms of Campylobacter in aqueous microcosm. Int. J. Food Microbiol. 55: 263267.
134. Thieringer, H. A.,, P. G. Jones, and, M. Inouye. 1998. Cold shock and adaptation. Bioessays 20: 4957.
135. Tiwari, R. P.,, N. Sachdeva, and, G. S. Hoondal. 2004. Adaptive acid tolerance response in Salmonella enterica serovar Typhimurium and Salmonella enterica serovar Typhi. J. Basic Microbiol. 2: 137146.
136. Tomoyasu, T.,, A. Takaya,, T. Sasaki,, T. Nagase,, R. Kikuno,, M. Morioka, and, T. Yamamoto. 2003. A new heat shock gene, agsA, which encodes a small chaperone involved in suppressing protein aggregation in Salmonella enterica serovar Typhimurium. J. Bacteriol. 185: 63316339.
137. Tseng, C.-P., and, T. J. Montville. 1993. Metabolic regulation of end product distribution in lactobacilli: causes and consequences. Biotechnol. Prog. 9: 113121.
138. Van Langendonck, N.,, P. Velge, and, E. Bottreau. 1998. Host cell protein tyrosine kinases are activated during the entry of Listeria monocytogenes. FEMS Microbiol. Lett. 162: 169176.
139. Van Schaik, W.,, C. G. Gahan, and, C. Hill. 1999. Acid-adapted Listeria monocytogenes displays enhanced tolerance against the lantibiotics nisin and lactin 3147. J. Food Prot. 62: 536539.
140. Vigh, V.,, B. Maresca, and, J. L. Harwood. 1998. Does the membrane’s physical state control the expression of heat shock and other genes? Trends Biochem. Sci. 23: 369372.
141. Volker, U.,, H. Mach,, R. Schmid, and, M. Hecker. 1992. Stress proteins and cross-protection by heat shock and salt stress in Bacillus subtilis. J. Gen. Microbiol. 138: 21252135.
142. Wang, G., and, M. P. Doyle. 1998. Heat shock response enhances acid tolerance of Escherichia coli O157:H7. Lett. Appl. Microbiol. 26: 3134.
143. Wiedmann, M.,, T. J. Arvik,, R. J. Hurley, and, K. J. Boor. 1998. General stress transcription factor σ B and its role in acid tolerance and virulence of Listeria monocytogenes. J. Bacteriol. 180: 36503656.
144. Winzer, K.,, K. R. Hardic, and, P. Williams. 2002. Bacterial cell-to-cell communication: sorry, can’t talk now—gone to lunch! Curr. Opin. Microbiol. 5: 216222.
145. Wolffs, P.,, B. Norling,, J. Hoorfar,, M. Griffiths, and, P. Radstrom. 2005. Quantification of Campylobacter spp. in chicken rinse samples by using flotation prior to real-time PCR. Appl. Environ. Microbiol. 71: 57595764.
146. Wong, H. C.,, C. T. Shen,, C. N. Chang,, Y. S. Lee, and, J. D. Oliver. 2004. Biochemical and virulence characterization of viable but nonculturable cells of Vibrio parahaemolyticus. J. Food Prot. 67: 24302305.
147. Wouters, J. A.,, F. M. Rombouts,, W. M. deVos,, O. P. Kuipers, and, T. Abee. 1999. Cold shock proteins and low-temperature response of Streptococcus thermophilus CNRZ302. Appl. Environ. Microbiol. 65: 44364442.
148. Yura, T., and, K. Nakahigashi. 1999. Regulation of the heat-shock response. Curr. Opin. Microbiol. 2: 153158.
149. Zottola, E. A., and, K. C. Sasahara. 1994. Microbial biofilms in the food processing industry—should they be a concern? Int. J. Food Microbiol. 23: 125148.


Generic image for table
Table 1.1

First-order kinetics can be used to describe exponential growth and inactivation

Citation: Montville T, Matthews K. 2007. Growth, Survival, and Death of Microbes in Foods, p 3-22. In Doyle M, Beuchat L (ed), Food Microbiology: Fundamentals and Frontiers, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815912.ch1
Generic image for table
Table 1.2

Representative specific growth rates and doubling times of microorganisms

Citation: Montville T, Matthews K. 2007. Growth, Survival, and Death of Microbes in Foods, p 3-22. In Doyle M, Beuchat L (ed), Food Microbiology: Fundamentals and Frontiers, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815912.ch1
Generic image for table
Table 1.3

Examples of quorum sensing in food microbiology

Citation: Montville T, Matthews K. 2007. Growth, Survival, and Death of Microbes in Foods, p 3-22. In Doyle M, Beuchat L (ed), Food Microbiology: Fundamentals and Frontiers, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815912.ch1
Generic image for table
Table 1.4

Influence of thermal history and enumeration protocols on experimentally determined values at 55°C for ( )

Citation: Montville T, Matthews K. 2007. Growth, Survival, and Death of Microbes in Foods, p 3-22. In Doyle M, Beuchat L (ed), Food Microbiology: Fundamentals and Frontiers, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815912.ch1

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