Chapter 8 : Molecular Mechanisms of Microbial Survival in Foods

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This chapter describes the most important global regulator systems in representative food-borne pathogens and reviews the individual molecular mechanisms of survival against specific food-related stresses. It talks about representative gram-positive bacteria ( and ) and gram-negative (, , and ) food-borne pathogens which have been thoroughly studied. Weber et al. have classified all the RpoS-regulated genes into six major categories based on their functions: metabolism, regulation, transport, adaptation to stress, protein processing, and unknown. Gram-negative and gram-positive bacteria use global strategies in their response to osmotic stress as well as some unique species-specific responses. The chapter reviews the current knowledge on the molecular response to osmotic stress as manifested by a few food-borne pathogens. In most bacteria, glycine betaine is the most effective osmoprotectant, as it increases the volume of available water in the cytoplasm. Low-temperature storage of foods is an extremely successful preservation technology. Advancement of one's knowledge about the molecular basis for bacterial survival under stressful conditions is critical to the assurance of safe and palatable foods, whether using traditional or novel preservation technologies. The advent of genomics-, proteomics-, and metabolomics-based techniques has accelerated one's knowledge of the components involved in novel stress responses. In addition, the availability of an increasing number of fully sequenced bacterial genomes should facilitate further advances in the field of bacterial stress responses.

Citation: Diez-Gonzalez F, Kuruc J. 2009. Molecular Mechanisms of Microbial Survival in Foods, p 135-159. In Jaykus L, Wang H, Schlesinger L (ed), Food-Borne Microbes. ASM Press, Washington, DC. doi: 10.1128/9781555815479.ch8
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Diagram of σ regulation and some of the main factors involved in its activation (+) or inhibition (−). cAmP, cyclic AMP; CRP, catabolite repression protein.

Citation: Diez-Gonzalez F, Kuruc J. 2009. Molecular Mechanisms of Microbial Survival in Foods, p 135-159. In Jaykus L, Wang H, Schlesinger L (ed), Food-Borne Microbes. ASM Press, Washington, DC. doi: 10.1128/9781555815479.ch8
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1. Aertsen, A.,, R. Van Houdt,, K. Vanoirbeck, and, C. W. Michiels. 2004. An SOS response induced by high pressure in Escherichia coli. J. Bacteriol. 186: 61336141.
2. Alpas, H.,, N. Kalchayanand,, F. Bozoglu,, A. Sikes,, C. P. Dunne, and, B. Ray. 1999. Variation in resistance to hydrostatic pressure among strains of food-borne pathogens. Appl. Environ. Microbiol. 65: 42484251.
3. 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.
4. Arnold, K. W., and, C. W. Kaspar. 1995. Starvation- and stationary-phase-induced acid tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 61: 20372039.
5. 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.
6. Barak, J. D.,, L. Gorski,, P. Naraghi-Arani, and, A. O. Charkowski. 2005. Salmonella enterica virulence genes are required for bacterial attachment to plant tissue. Appl. Environ. Microbiol. 71: 56855691.
7. Barth, M.,, C. Marschall,, A. Muffler,, D. Fischer, and, R. Hengge-Aronis. 1995. Role for the histone-like protein H-NS in growth phase-dependent and osmotic regulation of σ S and many σ S-dependent genes in Escherichia coli. J. Bacteriol. 177: 34553464.
8. Becker, L. A.,, M. S. Çetin,, R. W. Hutkins, and, A. K. Benson. 1998. Identification of the gene encoding the alternative sigma factor σ B from Listeria monocytogenes and its role in osmo-tolerance. J. Bacteriol. 180: 45474554.
9. Benito, A.,, G. Ventoura,, M. Casadei,, T. Robinson, and, B. Mackey. 1999. Variation in resistance of natural isolates of Escherichia coli O157 to high hydrostatic pressure, mild heat, and other stresses. Appl. Environ. Microbiol. 65: 15641569.
10. Blount, P.,, M. J. Schroeder, and, C. Kung. 1997. Mutations in a bacterial mechanosensitive channel change the cellular response to osmotic stress. J. Biol. Chem. 272: 3215032157.
11. Botsford, J. L.,, M. Alvarez,, R. Hernandez, and, R. Nichols. 1994. Accumulation of glutamate by Salmonella typhimurium in response to osmotic stress. Appl. Environ. Microbiol. 60: 25682574.
12. Braeken, K.,, M. Moris,, R. Daniels,, J. Vanderleyden, and, J. Michiels. 2006. New horizons for (p)ppGpp in bacterial and plant physiology. Trends Microbiol. 14: 4554.
13. Brown, M. R., and, A. Kornberg. 2004. Inorganic polyphosphate in the origin and survival of species. Proc. Natl. Acad. Sci. USA 101: 1608516087.
14. Brul, S., and, J. Wells. 2005. Understanding pathogen survival and resistance in the food chain, p. 391420. In M. Griffiths (ed.), Understanding Pathogen Behaviour. Woodhead Publishing Ltd., Cambridge, England.
15. Castanie-Cornet, M.-P.,, T. A. Penfound,, D. Smith,, J. F. Elliott, and, J. W. Foster. 1999. Control of acid resistance in Escherichia coli. J. Bacteriol. 181: 35253535.
16. Cheville, A. M.,, K. W. Arnold,, C. Buchrieser,, C.-M. Cheng, and, C. W. Kaspar. 1996. rpoS regulation of acid, heat, and salt tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 62: 18221824.
17. Chuang, S., and, F. R. Blattner. 1993. Characterization of twenty-six new heat shock genes of Escherichia coli. J. Bacteriol. 175: 52425252.
18. Chuang, S.,, D. L. Daniels, and, F. R. Blattner. 1993. Global regulation of gene expression in Escherichia coli. J. Bacteriol. 175: 20262036.
19. Cotter, P. D.,, K. O’Reilly, and, C. Hill. 2001. Role of the glutamate decarboxylase acid resistance system in the survival of Listeria monocytogenes LO28 in low pH foods. J. Food Prot. 64: 13621368.
20. Cotter, P. D.,, S. Ryan,, C. G. Gahan, and, C. Hill. 2005. Presence of GadD1 glutamate decarboxylase in selected Listeria monocytogenes strains is associated with an ability to grow at low pH. Appl. Environ. Microbiol. 71: 28322839.
21. Csonka, L. N. 1989. Physiological and genetic responses of bacteria to osmotic stress. Microbiol. Rev. 53: 121147.
22. Cui, S.,, J. Meng, and, A. A. Bhagwat. 2001. Availability of glutamate and arginine during acid challenge determines cell density-dependent survival phenotype of Escherichia coli strains. Appl. Environ. Microbiol. 67: 49144918.
23. Culham, D. E.,, A. Lu,, M. Jishage,, K. A. Krogfelt,, A. Ishihama, and, J. M. Wood. 2001. The osmotic stress response and virulence in pyelonephritis isolates of Escherichia coli: contributions of RpoS, ProP, ProU and other systems. Microbiology 147: 16571670.
24. Dartigalongue, C.,, D. Missiakas, and, S. Raina. 2001. Characterization of the Escherichia coli σ E regulon. J. Biol. Chem. 276: 2086620875.
25. Derré, I.,, G. Rapoport, and, T. Msadek. 1999. CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in Gram-positive bacteria. Mol. Microbiol. 31: 117131.
26. Diez-Gonzalez, F., and, Y. Karaibrahimoglu. 2004. Comparison of the glutamate-, arginine- and lysine-dependent acid resistance systems in Escherichia coli O157:H7. J. Appl. Microbiol. 96: 12371244.
27. Dobrindt, U., and, J. Hacker. 2001. Whole genome plasticity in pathogenic bacteria. Curr. Opin. Microbiol. 4: 550557.
28. Dodd, C. 2005. Factors affecting stress response, p. 115127. In M. Griffiths (ed.), Understanding Pathogen Behaviour. Woodhead Publishing Ltd., Cambridge, England.
29. Ellermeier, J. R., and, J. M. Slauch. 2008. Fur regulates expression of the Salmonella pathogenicity island 1 type III secretion system through HilD. J. Bacteriol. 190: 476486.
30. Ermolenko, D. N., and, G. I. Makhatadze. 2002. Bacterial cold-shock proteins. Cell. Mol. Life Sci. 59: 19021913.
31. Fang, W.,, H. Siegumfeldt,, B. B. Budde, and, M. Jakobsen. 2004. Osmotic stress leads to decreased intracellular pH of Listeria monocytogenes as determined by fluorescence ratio-imaging microscopy. Appl. Environ. Microbiol. 70: 31763179.
32. Farkas, J. 2001. Physical methods of food preservation, p. 567591. In M. P. Doyle,, L. R. Beuchat, and, T. J. Montville (ed.), Food Microbiology: Fundamentals and Frontiers, 2nd ed. ASM Press, Washington, DC.
33. Fedoroff, N. 2006. Redox regulatory mechanisms in cellular stress responses. Ann. Bot. 98: 289300.
34. Ferreira, A.,, D. Sue,, C. P. O’Byrne, and, K. J. Boor. 2003. Role of Listeria monocytogenes σ B in survival of lethal acidic conditions and in the acquired acid tolerance response. Appl. Environ. Microbiol. 69: 26922698.
35. Foster, J. W. 2000. Microbial responses to acid stress, p. 99115. In G. Storz and, R. Hengge-Aronis (ed.), Bacterial Stress Responses. ASM Press, Washington, DC.
36. Foster, J. W. 1991. Salmonella acid shock proteins are required for the adaptive acid tolerance response. J. Bacteriol. 173: 68966902.
37. Foster, J. W., and, H. K. Hall. 1991. Inducible pH homeostasis and the acid tolerance response of Salmonella typhimurium. J. Bacteriol. 173: 51295135.
38. Foster, P. L. 2007. Stress-induced mutagenesis in bacteria. Crit. Rev. Biochem. Mol. Biol. 42: 372397.
39. Foster, P. L. 2005. Stress responses and genetic variation in bacteria. Mutat. Res. 569: 311.
40. Friedberg, E. C.,, G. C. Walker,, W. Siede,, R. D. Wood,, R. A. Schultz, and, T. Ellenberger. 2006. DNA Repair and Mutagenesis, 2nd ed. ASM Press, Washington, DC.
41. Gale, E. F. 1946. The bacterial amino acid decarboxylases. Adv. Enzymol. VI: 131.
42. Garcia-Graells, C.,, K. J. A. Hauben, and, C. W. Michiels. 1998. High-pressure inactivation and sublethal injury of pressure-resistant Escherichia coli mutants in fruit juices. Appl. Environ. Microbiol. 64: 15661568.
43. Gardan, R.,, O. Duché,, S. Leroy-Sétrin,, the European Listeria Genome Consortium, and J. Labadie. 2003. Role of ctc from Listeria monocytogenes in osmotolerance. Appl. Environ. Microbiol. 69: 154161.
44. Gong, S.,, H. Richard, and, J. W. Foster. 2003. YjdE (AdiC) is the arginine:agmatine antiporter essential for arginine-dependent acid resistance in Escherichia coli. J. Bacteriol. 185: 44024409.
45. Gottesman, S. 2004. The small RNA regulators of Escherichia coli: roles and mechanisms. Annu. Rev. Microbiol. 58: 303328.
46. Gould, G. 2005. Pathogen resistance and adaptation to emerging technologies, p. 442459. In M. Griffith (ed.), Understanding Pathogen Behaviour. Woodhead Publishing Ltd., Cambridge, England.
47. Gragerov, A.,, E. Nudler,, N. Komissarova,, G. A. Gaitanaris,, M. E. Gottesman, and, V. Nikiforov. 1992. Cooperation of GroEL/GroES and DnaK/DnaJ heat shock proteins in preventing protein misfolding in Escherichia coli. Proc. Natl. Acad. Sci. USA 89: 1034110344.
48. Greenacre, E. J.,, T. F. Brocklehurst,, C. R. Waspe,, D. R. Wilson, and, P. D. G. Wilson. 2003. Salmonella enterica serovar Typhimurium and Listeria monocytogenes acid tolerance response induced by organic acids at 20°C: optimization and modeling. Appl. Environ. Microbiol. 69: 39453951.
49. Gross, M.,, K. Lehle,, R. Jaenicke, and, K. H. Nierhaus. 1993. Pressure-induced dissociation of ribosomes and elongation cycle intermediates. Stabilizing conditions and identification of the most sensitive functional state. Eur. J. Biochem. 218: 463468.
50. Grothe, S.,, R. L. Krogsrud,, D. J. McClellan,, J. L. Milner, and, J. M. Wood. 1986. Proline transport and osmotic stress response in Escherichia coli K-12. J. Bacteriol. 166: 253259.
51. Hain, T.,, H. Hossain,, S. S. Chatterjee,, S. Machata,, U. Volk,, S. Wagner,, B. Brors,, S. Haas,, C. T. Kuenne,, A. Billion,, S. Otten,, J. Pane-Farre,, S. Engelmann, and, T. Chakraborty. 2008. Temporal transcriptomic analysis of the Listeria monocytogenes EGD-e σ B regulon. BMC Microbiol. 8: 20.
52. Hall, H. K., and, J. W. Foster. 1996. The role of Fur in the acid tolerance response of Salmonella typhimurium is physiologically and genetically separable from its role in iron acquisition. J. Bacteriol. 178: 56835691.
53. Hartman, P. A. 2001. The evolution of food microbiology, p. 312. In M. P. Doyle,, L. R. Beuchat, and, T. J. Montville (ed.), Food Microbiology: Fundamentals and Frontiers, 2nd ed. ASM Press, Washington, DC.
54. Hauben, K. J. A.,, D. H. Bartlett,, C. C. F. Soontjens,, K. Cornelis,, E. Y. Wuytack, and, C. W. Michiels. 1997. Escherichia coli mutants resistant to inactivation by high hydrostatic pressure. Appl. Environ. Microbiol. 63: 945950.
55. Hecker, M.,, J. Pané-Farré, and, U. Völker. 2007. SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu. Rev. Genet. 61: 215236.
56. Hecker, M.,, W. Schumann, and, U. Völker. 1996. Heat-shock and general stress response in Bacillus subtilis. Mol. Microbiol. 19: 417428.
57. Hecker, M., and, U. Völker. 2001. General stress response of Bacillus subtilis and other bacteria. Adv. Microb. Physiol. 44: 3591.
58. Helmann, J. D.,, M. F. W. Wu,, P. A. Kobel,, F. Gamo,, M. Wilson,, M. M. Morshedi,, M. Navre, and, C. Paddon. 2001. Global transcriptional response of Bacillus subtilis to heat shock. J. Bacteriol. 183: 73187328.
59. Hengge-Aronis, R. 2002. Signal transduction and regulatory mechanisms involved in control of the σ S (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 66: 373395.
60. Hengge-Aronis, R. 1993. Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in E. coli. Cell 72: 165168.
61. Hersh, B. M.,, F. T. Farooq,, D. N. Barstad,, D. L. Blankenhorn, and, J. L. Slonczewski. 1996. A glutamate-dependent acid resistance gene in Escherichia coli. J. Bacteriol. 178: 39783981.
62. Horn, G.,, R. Hofweber,, W. Kremer, and, H. R. Kalbitzer. 2007. Structure and function of bacterial cold shock proteins. Cell. Mol. Life Sci. 64: 14571470.
63. Jahid, I. K.,, A. J. Silva, and, J. A. Benitez. 2006. Polyphosphate stores enhance the ability of Vibrio cholerae to overcome environmental stresses in a low-phosphate environment. Appl. Environ. Microbiol. 72: 70437049.
64. Jay, J. M.,, M. J. Loessner, and, D. A. Golden. 2005. Modern Food Microbiology, 7th ed. Springer, New York, NY.
65. Karatzas, K. A. G., and, M. H. J. Bennik. 2002. Characterization of a Listeria monocytogenes Scott A isolate with high tolerance towards high hydrostatic pressure. Appl. Environ. Microbiol. 68: 31833189.
66. Kieboom, J., and, T. Abee. 2006. Arginine-dependent acid resistance in Salmonella enterica serovar Typhimurium. J. Bacteriol. 188: 56505653.
67. Kim, K. S.,, N. N. Rao,, C. D. Fraley, and, A. Kornberg. 2002. Inorganic polyphosphate is essential for long-term survival and virulence factors in Shigella and Salmonella spp. Proc. Natl. Acad. Sci. USA 99: 76757680.
68. Ko, R.,, L. Tombras Smith, and, G. M. Smith. 1994. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J. Bacteriol. 176: 426431.
69. Konkel, M. E.,, B. J. Kim,, J. D. Klena,, C. R. Young, and, R. Ziprin. 1998. Characterization of the thermal stress response of Campylobacter jejuni. Infect. Immun. 66: 36663672.
70. Kornberg, A. 2008. Abundant microbial inorganic polyphosphate, poly P kinase are under-appreciated. Microbe 3: 119123.
71. 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.
72. Kultz, D. 2003. Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function. J. Exp. Biol. 206: 31193124.
73. Kültz, D., and, L. Csonka. 1999. What sets the TonE during osmotic stress? Proc. Natl. Acad. Sci. USA 96: 18141816.
74. Lange, R., and, R. Hengge-Aronis. 1994. The cellular concentration of the σ S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev. 8: 16001607.
75. Lange, R., and, R. Hengge-Aronis. 1991. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol. Microbiol. 5: 4959.
76. Large, T. M.,, S. T. Walk, and, T. S. Whittam. 2005. Variation in acid resistance among Shiga toxin-producing clones of pathogenic Escherichia coli. Appl. Environ. Microbiol. 71: 24932500.
77. Layton, J. C., and, P. L. Foster. 2003. Error-prone DNA polymerase IV is controlled by the stress-response sigma factor, RpoS, in Escherichia coli. Mol. Microbiol. 50: 549561.
78. Lee, I. S.,, J. Lin,, H. K. Hall,, B. Bearson, and, J. W. Foster. 1995. The stationary-phase sigma factor σ S (RpoS) is required for a sustained acid tolerance response in virulent Salmonella typhimurium. Mol. Microbiol. 17: 155167.
79. Lee, I. S.,, J. L. Slonczewski, and, J. W. Foster. 1994. A low-pH-inducible, stationary-phase acid tolerance response in Salmonella typhimurium. J. Bacteriol. 176: 14221426.
80. Liao, M. K., and, S. Maloy. 2001. Substrate recognition by proline permease in Salmonella. Amino Acids 21: 161174.
81. Liberek, K.,, T. P. Galitski,, M. Zylicz, and, C. Georgopoulos. 1992. The DnaK chaperone modulates the heat shock response of Escherichia coli by binding to the σ 32 transcription factor. Biochemistry 89: 35163520.
82. Lin, J.,, I. S. Lee,, J. Frey,, J. L. Slonczewski, and, J. W. Foster. 1995. Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J. Bacteriol. 177: 40974104.
83. Lin, J.,, M. P. Smith,, K. C. Chapin,, H. S. Baik,, G. N. Bennett, and, J. W. Foster. 1996. Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl. Environ. Microbiol. 62: 30943100.
84. Lou, Y., and, A. E. Yousef. 1997. Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Appl. Environ. Microbiol. 63: 12521255.
85. Ma, Z.,, R. Hope,, D. L. Tucker,, T. Conway, and, J. W. Foster. 2002. Collaborative regulation of Escherichia coli glutamate-dependent acid resistance by two AraC-like regulators, GadX and GadW (YhiW). J. Bacteriol. 184: 70017012.
86. Madigan, M. T.,, J. M. Martinko,, P. V. Dunlap, and, D. P. Clark. 2008. Brock Biology of Microorganisms, 12th ed., p. 34115. Pearson Education, Inc., Upper Saddle River, NJ.
87. McArthur, J. V. 2006. Microbial Ecology: an Evolutionary Approach. Elsevier, Boston, MA.
88. Meng, S. Y., and, G. N. Bennett. 1992. Nucleotide sequence of the Escherichia coli cad operon: a system for neutralization of low extracellular pH. J. Bacteriol. 174: 26592669.
89. Missiakas, D., and, S. Raina. 1997. Protein misfolding in the cell envelope of Escherichia coli: new signaling pathways. Trends Biochem. Sci. 22: 5963.
90. Mongkolsuk, S., and, J. D. Helmann. 2002. Regulation of inducible peroxide stress responses. Mol. Microbiol. 45: 915.
91. Montville, T. J., and, K. R. Matthews. 2005. Food Microbiology—an Introduction. ASM Press, Washington, DC.
92. Narberhaus, F. 1999. Negative regulation of bacterial heat shock genes. Mol. Microbiol. 31: 18.
93. Neely, M. N.,, C. L. Dell, and, E. R. Olson. 1994. Roles of LysP and CadC in mediating the lysine requirement for acid induction of the Escherichia coli cad operon. J. Bacteriol. 176: 32783285.
94. Niven, G. W.,, C. A. Miles, and, B. M. Mackey. 1999. The effect of hydrostatic pressure on ribosome conformation in Escherichia coli: an in vivo study using differential scanning calorimetry. Microbiology 145: 419425.
95. Opdyke, J. A.,, J. G. Kang, and, G. Storz. 2004. GadY, a small-RNA regulator of acid response genes in Escherichia coli. J. Bacteriol. 186: 66986705.
96. Pagán, R., and, B. Mackey. 2000. Relationship between membrane damage and cell death in pressure-treated Escherichia coli cells: difference between exponential- and stationary-phase cells and variation among strains. Appl. Environ. Microbiol. 66: 28292834.
97. Pal, C.,, B. Papp, and, M. J. Lercher. 2005. Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat. Genet. 37: 13721375.
98. Park, G., and, F. Diez-Gonzalez. 2004. A novel glutamate-dependent acid resistance among strains belonging to the Proteeae tribe of Enterobacteriaceae. FEMS Microbiol. Lett. 237: 303309.
99. Park, Y.-K.,, B. Bearson,, S. H. Bang,, I. S. Bang, and, J. W. Foster. 1996. Internal pH crisis, lysine decarboxylase and the acid tolerance response of Salmonella typhimurium. Mol. Microbiol. 20: 605611.
100. Porankiewicz, J.,, J. Wang, and, A. K. Clarke. 1999. New insights into the ATP-dependent Clp protease: Escherichia coli and beyond. Mol. Microbiol. 32: 449458.
101. Préstamo, G.,, P. D. Sanz,, M. Fonberg-Broczek, and, G. Arroyo. 1999. High pressure response of fruit jams contaminated with Listeria monocytogenes. Lett. Appl. Microbiol. 28: 313316.
102. Price, S. B.,, C.-M. Cheng,, C. W. Kaspar,, J. C. Wright,, F. J. DeGraves,, T. A. Penfound,, M.-P. Castanie-Cornet, and, J. W. Foster. 2000. Role of rpoS in acid resistance and fecal shedding of Escherichia coli O157:H7. Appl. Environ. Microbiol. 66: 632637.
103. Price-Carter, M.,, T. G. Fazzio,, E. I. Vallbona, and, J. R. Roth. 2005. Polyphosphate kinase protects Salmonella enterica from weak organic acid stress. J. Bacteriol. 187: 30883099.
104. Raina, S.,, D. Missiakas, and, C. Georgopoulos. 1995. The rpoE gene encoding the σ E24) heat shock sigma factor of Escherichia coli. EMBO J. 14: 10431055.
105. Rao, N. N., and, A. Kornberg. 1999. Inorganic polyphosphate regulates responses of Escherichia coli to nutritional stringencies, environmental stresses and survival in the stationary phase. Prog. Mol. Subcell. Biol. 23: 183195.
106. Rastogi, N. K.,, K. S. Raghavarao,, V. M. Balasubramaniam,, K. Niranjan, and, D. Knorr. 2007. Opportunities and challenges in high pressure processing of foods. Crit. Rev. Food Sci. Nutr. 47: 69112.
107. Rees, C. E. D.,, C. E. R. Dodd,, P. T. Gibson,, I. R. Booth, and, G. S. A. B. Stewart. 1995. The significance of bacteria in stationary phase to food microbiology. Int. J. Food Microbiol. 28: 263275.
108. Richard, H., and, J. W. Foster. 2004. Escherichia coli glutamate- and arginine-dependent acid resistance systems increase internal pH and reverse transmembrane potential. J. Bacteriol. 186: 60326041.
109. Richard, H. T., and, J. W. Foster. 2003. Acid resistance in Escherichia coli. Adv. Appl. Microbiol. 52: 167186.
110. Robey, M.,, A. Benito,, R. H. Hutson,, C. Pascual,, S. F. Park, and, B. M. Mackey. 2001. Variation in resistance to high hydrostatic pressure and rpoS heterogeneity in natural isolates of Escherichia coli O157:H7. Appl. Environ. Microbiol. 67: 49014907.
111. Rodriguez-Romo, L., and, A. Yousef. 2005. Cross-protective effects of bacterial stress, p. 128151. In M. Griffiths (ed.), Understanding Pathogen Behaviour. Woodhead Publishing Ltd., Cambridge, England.
112. Rosche, T. M.,, D. J. Smith,, E. E. Parker, and, J. D. Oliver. 2005. RpoS involvement and requirement for exogenous nutrient for osmotically induced cross protection in Vibrio vulnificus. FEMS Microbiol. Lett. 53: 455462.
113. Rychlik, I., and, P. A. Barrow. 2005. Salmonella stress management and its relevance to behaviour during intestinal colonisation and infection. FEMS Microbiol. Rev. 29: 10211040.
114. Samelis, J.,, J. S. Ikeda, and, J. N. Sofos. 2003. Evaluation of the pH-dependent, stationary-phase acid tolerance in Listeria monocytogenes and Salmonella Typhimurium DT104 induced by culturing in media with 1% glucose: a comparative study with Escherichia coli O157: H7. J. Appl. Microbiol. 95: 563575.
115. Schellhorn, H. E., and, V. L. Stones. 1992. Regulation of katF and katE in Escherichia coli K-12 by weak acids. J. Bacteriol. 174: 47694776.
116. Schlesinger, M. J. 1990. Heat shock proteins. J. Biol. Chem. 265: 1211112114.
117. Schulz, A., and, W. Schumann. 1996. hrcA, the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes. J. Bacteriol. 178: 10881093.
118. Shin, S., and, C. Park. 1995. Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J. Bacteriol. 177: 46964702.
119. Sleator, R. D.,, C. G. M. Gahan, and, C. Hill. 2003. A postgenomic appraisal of osmo-tolerance in Listeria monocytogenes. Appl. Environ. Microbiol. 69: 19.
120. Smith, D. K.,, T. Kassam,, B. Singh, and, J. F. Elliot. 1992. Escherichia coli has two homologous glutamate decarboxylase genes that map to distinct loci. J. Bacteriol. 174: 58205826.
121. Stewart, C. M.,, M. B. Cole,, J. D. Legan,, L. Slade, and, D. W. Schaffner. 2005. Solute-specific effects of osmotic stress on Staphylococcus aureus. J. Appl. Microbiol. 98: 193202.
122. Stim-Herndon, K. P.,, T. M. Flores, and, G. N. Bennett. 1996. Molecular characterization of adiY, a regulatory gene which affects expression of the biodegradative acid-induced arginine decarboxylase gene (adiA) of Escherichia coli. Microbiology 142: 13111320.
123. Storz, G., and, M. Zheng. 2000. Oxidative stress, p. 4759. In G. Storz and, R. Hengge-Aronis (ed.), Bacterial Stress Responses. ASM Press, Washington, DC.
124. Strøm, A. R., and, I. Kaasen. 1993. Treha-lose metabolism in Escherichia coli: stress protection and stress regulation of gene expression. Mol. Microbiol. 8: 205210.
125. Tetsch, L.,, C. Koller,, I. Haneburger, and, K. Jung. 2008. The membrane-integrated transcriptional activator CadC of Escherichia coli senses lysine indirectly via the interaction with the lysine permease LysP. Mol. Microbiol. 67: 570583.
126. Tucker, D. L.,, N. Tucker,, Z. Ma,, J. W. Foster,, R. L. Miranda,, P. S. Cohen, and, T. Conway. 2003. Genes of the GadX-GadW regulon in Escherichia coli. J. Bacteriol. 185: 31903201.
127. Typas, A.,, G. Becker, and, R. Hengge. 2007. The molecular basis of selective promoter activation by the σ S subunit of RNA polymerase. Mol. Microbiol. 63: 12961306.
128. Ulmer, H. M.,, M. G. Gänzle, and, R. F. Vogel. 2000. Effects of high pressure on survival and metabolic activity of Lactobacillus plantarum TMW1.460. Appl. Environ. Microbiol. 66: 39663973.
129. Vaknin, A., and, H. C. Berg. 2005. Osmotic stress mechanically perturbs chemoreceptors in Escherichia coli. Proc. Natl. Acad. Sci. USA 103: 592596.
130. Vasudevan, P., and, K. Venkitanarayanan. 2006. Role of the rpoS gene in the survival of Vibrio parahaemolyticus in artificial seawater and fish homogenate. J. Food Prot. 69: 14381442.
131. Vijaranakul, U.,, M. J. Nadakavukaren,, D. O. Bayles,, B. J. Wilkinson, and, R. K. Jayaswal. 1997. Characterization of an NaCl-sensitive Staphylococcus aureus mutant and rescue of the NaCl-sensitive phenotype by glycine betaine but not by other compatible solutes. Appl. Environ. Microbiol. 63: 18891897.
132. Vilhelmsson, O., and, K. J. Miller. 2002. Synthesis of pyruvate dehydrogenase in Staphylococcus aureus is stimulated by osmotic stress. Appl. Environ. Microbiol. 68: 23532358.
133. Wang, G., and, M. P. Doyle. 1998. Heat shock response enhances acid tolerance of Escherichia coli O157:H7. Lett. Appl. Microbiol. 26: 3134.
134. Waterman, S. R., and, P. L. C. Small. 1996. Characterization of the acid resistance pheno-type and rpoS alleles of Shiga-like toxin-producing Escherichia coli. Infect. Immun. 64: 28082811.
135. Weber, H.,, T. Polen,, J. Heuveling,, V. F. Wendisch, and, R. Hengge. 2005. Genomewide analysis of the general stress response network in Escherichia coli: σ S-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187: 15911603.
136. Welch, T. J., and, D. H. Bartlett. 1998. Identification of a regulatory protein required for pressure-responsive gene expression in the deep-sea bacterium Photobacterium species strain SS9. Mol. Microbiol. 27: 977985.
137. Welch, T. J.,, A. Farewell,, F. C. Neidhardt, and, D. H. Bartlett. 1993. Stress response of Escherichia coli to elevated hydrostatic pressure. J. Bacteriol. 175: 71707177.
138. Wemekamp-Kamphuis, H. H.,, A. K. Karatzas,, J. A. Wouters, and, T. Abee. 2002. Enhanced levels of cold shock proteins in Listeria monocytogenes LO28 upon exposure to low temperature and high hydrostatic pressure. Appl. Environ. Microbiol. 68: 456463.
139. Wemekamp-Kamphuis, H. H.,, J. A. Wouters,, P. P. L. A. de Leeuw,, T. Hain,, T. Chakraborty, and, T. Abee. 2004. Identification of sigma factor σ B-controlled genes and their impact on acid stress, high hydrostatic pressure, and freeze survival in Listeria monocytogenes EGD-e. Appl. Environ. Microbiol. 70: 34573466.
140. White, D. 2007. The Physiology and Biochemistry of Prokaryotes, 3rd ed. Oxford University Press, New York, NY.
141. 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.
142. Yuk, H.-G., and, D. L. Marshall. 2003. Heat adaptation alters Escherichia coli O157:H7 membrane lipid composition and verotoxin production. Appl. Environ. Microbiol. 69: 51155119.
143. Zheng, M.,, X. Wang,, L. J. Templeton,, D. R. Smulski,, R. A. LaRossa, and, G. Storz. 2001. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 183: 45624570.


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Heat shock genes of gram-positive bacteria as organized by class

Citation: Diez-Gonzalez F, Kuruc J. 2009. Molecular Mechanisms of Microbial Survival in Foods, p 135-159. In Jaykus L, Wang H, Schlesinger L (ed), Food-Borne Microbes. ASM Press, Washington, DC. doi: 10.1128/9781555815479.ch8

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