Chapter 4 : Stress Responses in Foodborne Bacteria

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Preservation technologies subject bacterial cells to different levels of stress, which in the most effective cases lead to their inactivation and death. The term “stress” can refer to any extracellular influence that threatens the ability of microorganisms to perform their living functions. The food preservation technologies designed to rapidly inactivate microbial cells include thermal processes, irradiation, high-pressure processing, and the use of strong oxidant compounds. Other technologies accomplish the preservation of foods by inhibiting growth; the most extensively used are low-temperature storage (refrigeration and freezing), reduction of moisture content (concentration and drying), control of ox-redox potential (use of controlled atmospheres and vacuum packaging), and acidification (fermentation and addition of organic acids). In nature, microorganisms are constantly exposed to similar changes in temperature, oxygen, moisture, light, pH, and chemical composition. Bacteria are able to survive thanks to a wide array of molecular responses that provide cellular protection against stresses. Bacteria are protected from changes in pH, temperature, oxidative conditions, solute concentrations, and pressure by a network of sophisticated global genetic regulatory systems and molecular stress responses specific to individual chemical or physical threats. The most important general regulators and specific genetic systems reported in representative foodborne pathogenic bacteria are highlighted in this chapter.

Citation: Diez-Gonzalez F. 2019. Stress Responses in Foodborne Bacteria, p 79-99. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch4
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Image of Figure 4.1
Figure 4.1

Diagram of σ regulation and some of the main factors involved in its activation (+) or inhibition (−). cAMP, cyclic AMP; CRP, cyclic AMP receptor protein.

Citation: Diez-Gonzalez F. 2019. Stress Responses in Foodborne Bacteria, p 79-99. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch4
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Image of Figure 4.2
Figure 4.2

Hypothetical depiction of a bacterial cell with some of the most important specific stress response mechanisms reported in foodborne pathogenic bacteria. Illustration ideas were taken partially from reference .

Citation: Diez-Gonzalez F. 2019. Stress Responses in Foodborne Bacteria, p 79-99. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch4
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1. Madigan MT, Martinko JM, Dunlap PV, Clark DP . 2008. Brock Biology of Microorganisms, 12th ed. Pearson Benjamin Cummings, San Francisco, CA.
2. McArthur JV . 2006. Microbial Ecology: An Evolutionary Approach. Elsevier, Boston, MA.
3. Jay JM, Loessner M, , Gold J. 2005. Modern Food Microbiology, 7th ed. Springer, New York, NY.
4. Hartman PA, . 2001. The evolution of food microbiology, p 3 12. In Doyle MP, Beuchat LR, Montville TJ (ed), Food Microbiology: Fundamentals and Frontiers. ASM Press, Washington, DC.
5. Montville TJ, Matthews KR, Kniel KE . 2013. Food Microbiology: an Introduction, 3rd ed. ASM Press, Washington, DC.
6. Brul S, Wells J, Ueckert J, . 2005. Understanding pathogen survival and resistance in the food chain, p 391 421. In Griffiths M (ed), Understanding Pathogen Behaviour. Woodhead Publishing, Cambridge, England.[CrossRef]
7. Dobrindt U, Hacker J . 2001. Whole genome plasticity in pathogenic bacteria. Curr Opin Microbiol 4 : 550 557[CrossRef].[PubMed]
8. Pál C, Papp B, Lercher MJ . 2005. Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat Genet 37 : 1372 1375[CrossRef].[PubMed]
9. Rodriguez-Romo L, , Yousef A, . 2005. Cross-protective effects of bacterial stress, p 128 151. In Griffiths M (ed), Understanding Pathogen Behaviour . Woodhead Publishing, Cambridge, England.
10. Diez-Gonzalez F, Karaibrahimoglu Y . 2004. Comparison of the glutamate-, arginine- and lysine-dependent acid resistance systems in Escherichia coli O157:H7. J Appl Microbiol 96 : 1237 1244[CrossRef].[PubMed]
11. Wang G, Doyle MP . 1998. Heat shock response enhances acid tolerance of Escherichia coli O157:H7. Lett Appl Microbiol 26 : 31 34[CrossRef].[PubMed]
12. Begley M, Hill C . 2015. Stress adaptation in foodborne pathogens. Annu Rev Food Sci Technol 6 : 191 210[CrossRef].[PubMed]
13. Yousef AE, Balasubramaniam VM, . 2013. Physical methods of food preservation, p 737 763. In Doyle MP, Buchanan RL (ed), Food Microbiology: Fundamentals and Frontiers, 4th ed. ASM Press, Washington, DC.
14. Ahn DU, Lee EJ, . 2007. Mechanisms and prevention of quality changes in meat by irradiation, p 127 142. In Sommers CH, Fan X (ed), Food Irradiation Research and Technology. Taylor & Francis, Ames, IA.
15. Foster PL . 2005. Stress responses and genetic variation in bacteria. Mutat Res 569 : 3 11[CrossRef].[PubMed]
16. Baharoglu Z, Mazel D . 2014. SOS, the formidable strategy of bacteria against aggressions. FEMS Microbiol Rev 38 : 1126 1145[CrossRef].[PubMed]
17. Kreuzer KN . 2013. DNA damage responses in prokaryotes: regulating gene expression, modulating growth patterns, and manipulating replication forks. Cold Spring Harb Perspect Biol 5 : a012674[CrossRef].[PubMed]
18. Foster PL . 2007. Stress-induced mutagenesis in bacteria. Crit Rev Biochem Mol Biol 42 : 373 397[CrossRef].[PubMed]
19. White D . 2007. The Physiology and Biochemistry of Prokaryotes, 3rd ed. Oxford University Press, New York, NY.
20. Rychlik I, Barrow PA . 2005. Salmonella stress management and its relevance to behaviour during intestinal colonisation and infection. FEMS Microbiol Rev 29 : 1021 1040[CrossRef].[PubMed]
21. Mika F, Hengge R . 2014. Small RNAs in the control of RpoS, CsgD, and biofilm architecture of Escherichia coli. RNA Biol 11 : 494 507[CrossRef].[PubMed]
22. Gottesman S . 2004. The small RNA regulators of Escherichia coli: roles and mechanisms. Annu Rev Microbiol 58 : 303 328[CrossRef].[PubMed]
23. Cook H, Ussery DW . 2013. Sigma factors in a thousand E. coli genomes. Environ Microbiol 15 : 3121 3129[CrossRef].[PubMed]
24. Gruber TM, Gross CA . 2003. Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57 : 441 466[CrossRef].[PubMed]
25. Typas A, Becker G, Hengge R . 2007. The molecular basis of selective promoter activation by the σ S subunit of RNA polymerase. Mol Microbiol 63 : 1296 1306[CrossRef].[PubMed]
26. 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 : 373 395[CrossRef].[PubMed]
27. Rees CE, Dodd CE, Gibson PT, Booth IR, Stewart GS . 1995. The significance of bacteria in stationary phase to food microbiology. Int J Food Microbiol 28 : 263 275[CrossRef].[PubMed]
28. Hengge-Aronis R . 1993. Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in E. coli. Cell 72 : 165 168[CrossRef].[PubMed]
29. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R . 2005. Genome-wide analysis of the general stress response network in Escherichia coli: σ S-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187 : 1591 1603[CrossRef].[PubMed]
30. Dong T, Schellhorn HE . 2010. Role of RpoS in virulence of pathogens. Infect Immun 78 : 887 897[CrossRef].[PubMed]
31. Dodd C, . 2005. Factors affecting stress response, p 115 127. In Griffiths M (ed), Understanding Pathogen Behaviour. Woodhead Publishing, Cambridge, England.[CrossRef]
32. Layton JC, Foster PL . 2003. Error-prone DNA polymerase IV is controlled by the stress-response sigma factor, RpoS, in Escherichia coli. Mol Microbiol 50 : 549 561[CrossRef].[PubMed]
33. Schellhorn HE, Stones VL . 1992. Regulation of katF and katE in Escherichia coli K-12 by weak acids. J Bacteriol 174 : 4769 4776[CrossRef].[PubMed]
34. Strøm AR, Kaasen I . 1993. Trehalose metabolism in Escherichia coli: stress protection and stress regulation of gene expression. Mol Microbiol 8 : 205 210[CrossRef].[PubMed]
35. Lange R, Hengge-Aronis R . 1991. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol 5 : 49 59[CrossRef].[PubMed]
36. Lange R, Hengge-Aronis R . 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 : 1600 1612[CrossRef].[PubMed]
37. Hengge R . 2009. Proteolysis of σ S (RpoS) and the general stress response in Escherichia coli. Res Microbiol 160 : 667 676[CrossRef].[PubMed]
38. Hecker M, Pané-Farré J, Völker U . 2007. SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu Rev Microbiol 61 : 215 236[CrossRef].[PubMed]
39. van Schaik W, Abee T . 2005. The role of σ B in the stress response of Gram-positive bacteria—targets for food preservation and safety. Curr Opin Biotechnol 16 : 218 224[CrossRef].[PubMed]
40. Arnold KW, Kaspar CW . 1995. Starvation- and stationary-phase-induced acid tolerance in Escherichia coli O157:H7. Appl Environ Microbiol 61 : 2037 2039.[PubMed]
41. Waterman SR, Small PLC . 1996. Characterization of the acid resistance phenotype and rpoS alleles of Shiga-like toxin-producing Escherichia coli. Infect Immun 64 : 2808 2811.[PubMed]
42. Cheville AM, Arnold KW, Buchrieser C, Cheng C-M, Kaspar CW . 1996. rpoS regulation of acid, heat, and salt tolerance in Escherichia coli O157:H7. Appl Environ Microbiol 62 : 1822 1824.[PubMed]
43. Price SB, Cheng C-M, Kaspar CW, Wright JC, DeGraves FJ, Penfound TA, Castanie-Cornet M-P, Foster JW . 2000. Role of rpoS in acid resistance and fecal shedding of Escherichia coli O157:H7. Appl Environ Microbiol 66 : 632 637[CrossRef].[PubMed]
44. de Oliveira Elias S, Noronha TB, Tondo EC . 2018. Assessment of Salmonella spp. and Escherichia coli O157:H7 growth on lettuce exposed to isothermal and non-isothermal conditions. Food Microbiol 72 : 206 213[CrossRef].[PubMed]
45. Hauryliuk V, Atkinson GC, Murakami KS, Tenson T, Gerdes K . 2015. Recent functional insights into the role of (p)ppGpp in bacterial physiology. Nat Rev Microbiol 13 : 298 309[CrossRef].[PubMed]
46. Harms A, Maisonneuve E, Gerdes K . 2016. Mechanisms of bacterial persistence during stress and antibiotic exposure. Science 354 : aaf4268[CrossRef].[PubMed]
47. Atkinson GC, Tenson T, Hauryliuk V . 2011. The RelA/SpoT homolog (RSH) superfamily: distribution and functional evolution of ppGpp synthetases and hydrolases across the tree of life. PLoS One 6 : e23479[CrossRef].[PubMed]
48. Brown MR, Kornberg A . 2004. Inorganic polyphosphate in the origin and survival of species. Proc Natl Acad Sci USA 101 : 16085 16087[CrossRef].[PubMed]
49. Kornberg A . 2008. Abundant microbial inorganic polyphosphate, poly P kinase are underappreciated. Microbe 3 : 119 123.
50. Rao NN, Kornberg A . 1999. Inorganic polyphosphate regulates responses of Escherichia coli to nutritional stringencies, environmental stresses and survival in the stationary phase. Prog Mol Subcell Biol 23 : 183 195[CrossRef].[PubMed]
51. Price-Carter M, Fazzio TG, Vallbona EI, Roth JR . 2005. Polyphosphate kinase protects Salmonella enterica from weak organic acid stress. J Bacteriol 187 : 3088 3099[CrossRef].[PubMed]
52. Kim KS, Rao NN, Fraley CD, Kornberg A . 2002. Inorganic polyphosphate is essential for long-term survival and virulence factors in Shigella and Salmonella spp. Proc Natl Acad Sci USA 99 : 7675 7680[CrossRef].[PubMed]
53. Jahid IK, Silva AJ, Benitez JA . 2006. Polyphosphate stores enhance the ability of Vibrio cholerae to overcome environmental stresses in a low-phosphate environment. Appl Environ Microbiol 72 : 7043 7049[CrossRef].[PubMed]
54. Foster JW, . 2000. Microbial responses to acid stress, p 99 115. In Storz G, Hengge-Aronis R (ed), Bacterial Stress Responses. ASM Press, Washington, DC.
55. Foster JW . 1995. Low pH adaptation and the acid tolerance response of Salmonella typhimurium. Crit Rev Microbiol 21 : 215 237[CrossRef].[PubMed]
56. Samelis J, Ikeda JS, Sofos JN . 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 : 563 575[CrossRef].[PubMed]
57. Lin J, Smith MP, Chapin KC, Baik HS, Bennett GN, Foster JW . 1996. Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl Environ Microbiol 62 : 3094 3100.[PubMed]
58. Ferreira A, Sue D, O'Byrne CP, Boor KJ . 2003. Role of Listeria monocytogenes σ B in survival of lethal acidic conditions and in the acquired acid tolerance response. Appl Environ Microbiol 69 : 2692 2698[CrossRef].[PubMed]
59. Greenacre EJ, Brocklehurst TF, Waspe CR, Wilson DR, Wilson PDG . 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 : 3945 3951[CrossRef].[PubMed]
60. Lin J, Lee IS, Frey J, Slonczewski JL, Foster JW . 1995. Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J Bacteriol 177 : 4097 4104[CrossRef].[PubMed]
61. Castanie-Cornet M-P, Penfound TA, Smith D, Elliott JF, Foster JW . 1999. Control of acid resistance in Escherichia coli. J Bacteriol 181 : 3525 3535.[PubMed]
62. Koutsoumanis KP, Sofos JN . 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 : 321 326[CrossRef].[PubMed]
63. Lou Y, Yousef AE . 1997. Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Appl Environ Microbiol 63 : 1252 1255.[PubMed]
64. Large TM, Walk ST, Whittam TS . 2005. Variation in acid resistance among Shiga toxin-producing clones of pathogenic Escherichia coli. Appl Environ Microbiol 71 : 2493 2500[CrossRef].[PubMed]
65. Gale EF . 1946. The bacterial amino acid decarboxylases. Adv Enzym VI : 1 31.
66. Gale EF, Epps HMR . 1942. The effect of the pH of the medium during growth on the enzymic activities of bacteria ( Escherichia coli and Micrococcus lysodeikticus) and the biological significance of the changes produced. Biochem J 36 : 600 618[CrossRef].[PubMed]
67. Hersh BM, Farooq FT, Barstad DN, Blankenhorn DL, Slonczewski JL . 1996. A glutamate-dependent acid resistance gene in Escherichia coli. J Bacteriol 178 : 3978 3981[CrossRef].[PubMed]
68. Richard H, Foster JW . 2004. Escherichia coli glutamate- and arginine-dependent acid resistance systems increase internal pH and reverse transmembrane potential. J Bacteriol 186 : 6032 6041[CrossRef].[PubMed]
69. Meng SY, Bennett GN . 1992. Nucleotide sequence of the Escherichia coli cad operon: a system for neutralization of low extracellular pH. J Bacteriol 174 : 2659 2669[CrossRef].[PubMed]
70. Gong S, Richard H, Foster JW . 2003. YjdE (AdiC) is the arginine:agmatine antiporter essential for arginine-dependent acid resistance in Escherichia coli. J Bacteriol 185 : 4402 4409[CrossRef].[PubMed]
71. Stim-Herndon KP, Flores TM, Bennett GN . 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 : 1311 1320[CrossRef].[PubMed]
72. Richard HT, Foster JW . 2003. Acid resistance in Escherichia coli. Adv Appl Microbiol 52 : 167 186[CrossRef].[PubMed]
73. Neely MN, Dell CL, Olson ER . 1994. Roles of LysP and CadC in mediating the lysine requirement for acid induction of the Escherichia coli cad operon. J Bacteriol 176 : 3278 3285[CrossRef].[PubMed]
74. Tetsch L, Koller C, Haneburger I, Jung K . 2008. The membrane-integrated transcriptional activator CadC of Escherichia coli senses lysine indirectly via the interaction with the lysine permease LysP. Mol Microbiol 67 : 570 583[CrossRef].[PubMed]
75. Smith DK, Kassam T, Singh B, Elliott JF . 1992. Escherichia coli has two homologous glutamate decarboxylase genes that map to distinct loci. J Bacteriol 174 : 5820 5826[CrossRef].[PubMed]
76. Arnold CN, McElhanon J, Lee A, Leonhart R, Siegele DA . 2001. Global analysis of Escherichia coli gene expression during the acetate-induced acid tolerance response. J Bacteriol 183 : 2178 2186[CrossRef].[PubMed]
77. Tucker DL, Tucker N, Ma Z, Foster JW, Miranda RL, Cohen PS, Conway T . 2003. Genes of the GadX-GadW regulon in Escherichia coli. J Bacteriol 185 : 3190 3201[CrossRef].[PubMed]
78. Opdyke JA, Kang JG, Storz G . 2004. GadY, a small-RNA regulator of acid response genes in Escherichia coli. J Bacteriol 186 : 6698 6705[CrossRef].[PubMed]
79. Feehily C, Karatzas KAG . 2013. Role of glutamate metabolism in bacterial responses towards acid and other stresses. J Appl Microbiol 114 : 11 24[CrossRef].[PubMed]
80. Smith JL, Liu Y, Paoli GC . 2013. How does Listeria monocytogenes combat acid conditions? Can J Microbiol 59 : 141 152[CrossRef].[PubMed]
81. NicAogáin K, O'Byrne CP . 2016. The role of stress and stress adaptations in determining the fate of the bacterial pathogen Listeria monocytogenes in the food chain. Front Microbiol 7 : 1865[CrossRef].[PubMed]
82. O'Driscoll B, Gahan CGM, Hill C . 1996. Adaptive acid tolerance response in Listeria monocytogenes: isolation of an acid-tolerant mutant which demonstrates increased virulence. Appl Environ Microbiol 62 : 1693 1698.[PubMed]
83. Cotter PD, Emerson N, Gahan CGM, Hill C . 1999. Identification and disruption of lisRK, a genetic locus encoding a two-component signal transduction system involved in stress tolerance and virulence in Listeria monocytogenes. J Bacteriol 181 : 6840 6843.[PubMed]
84. van der Veen S, Abee T . 2011. Contribution of Listeria monocytogenes RecA to acid and bile survival and invasion of human intestinal Caco-2 cells. Int J Med Microbiol 301 : 334 340[CrossRef].[PubMed]
85. Cotter PD, Gahan CGM, Hill C . 2000. Analysis of the role of the Listeria monocytogenes F 0F 1-AtPase operon in the acid tolerance response. Int J Food Microbiol 60 : 137 146[CrossRef].[PubMed]
86. Cotter PD, O'Reilly K, Hill C . 2001. Role of the glutamate decarboxylase acid resistance system in the survival of Listeria monocytogenes LO28 in low pH foods. J Food Prot 64 : 1362 1368[CrossRef].[PubMed]
87. Cotter PD, Ryan S, Gahan CGM, Hill C . 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 : 2832 2839[CrossRef].[PubMed]
88. Karatzas KAG, Suur L, O'Byrne CP . 2012. Characterization of the intracellular glutamate decarboxylase system: analysis of its function, transcription, and role in the acid resistance of various strains of Listeria monocytogenes. Appl Environ Microbiol 78 : 3571 3579[CrossRef].[PubMed]
89. Ryan S, Begley M, Gahan CGM, Hill C . 2009. Molecular characterization of the arginine deiminase system in Listeria monocytogenes: regulation and role in acid tolerance. Environ Microbiol 11 : 432 445[CrossRef].[PubMed]
90. Hall HK, Foster JW . 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 : 5683 5691[CrossRef].[PubMed]
91. Foster JW . 1991. Salmonella acid shock proteins are required for the adaptive acid tolerance response. J Bacteriol 173 : 6896 6902[CrossRef].[PubMed]
92. Lee IS, Lin J, Hall HK, Bearson B, Foster JW . 1995. The stationary-phase sigma factor σ S (RpoS) is required for a sustained acid tolerance response in virulent Salmonella typhimurium. Mol Microbiol 17 : 155 167[CrossRef].[PubMed]
93. Bang IS, Audia JP, Park YK, Foster JW . 2002. Autoinduction of the ompR response regulator by acid shock and control of the Salmonella enterica acid tolerance response. Mol Microbiol 44 : 1235 1250[CrossRef].[PubMed]
94. Foster JW, Hall HK . 1991. Inducible pH homeostasis and the acid tolerance response of Salmonella typhimurium. J Bacteriol 173 : 5129 5135[CrossRef].[PubMed]
95. Lee IS, Slonczewski JL, Foster JW . 1994. A low-pH-inducible, stationary-phase acid tolerance response in Salmonella typhimurium. J Bacteriol 176 : 1422 1426[CrossRef].[PubMed]
96. Kieboom J, Abee T . 2006. Arginine-dependent acid resistance in Salmonella enterica serovar Typhimurium. J Bacteriol 188 : 5650 5653[CrossRef].[PubMed]
97. Liu J, Zhai L, Lu W, Lu Z, Bie X . 2017. Amino acid decarboxylase-dependent acid tolerance, selected phenotypic, and virulence gene expression responses of Salmonella enterica serovar Heidelberg. Food Res Int 92 : 33 39[CrossRef].[PubMed]
98. Viala JPM, Méresse S, Pocachard B, Guilhon AA, Aussel L, Barras F . 2011. Sensing and adaptation to low pH mediated by inducible amino acid decarboxylases in Salmonella. PLoS One 6 : e22397[CrossRef].[PubMed]
99. Cooper GM . 2000. The Cell: A Molecular Approach, 2nd ed. Sinauer Associates, Sunderland, MA.
100. Krämer R . 2010. Bacterial stimulus perception and signal transduction: response to osmotic stress. Chem Rec 10 : 217 229[CrossRef].[PubMed]
101. Vijaranakul U, Nadakavukaren MJ, Bayles DO, Wilkinson BJ, Jayaswal RK . 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 : 1889 1897.[PubMed]
102. Botsford JL, Alvarez M, Hernandez R, Nichols R . 1994. Accumulation of glutamate by Salmonella typhimurium in response to osmotic stress. Appl Environ Microbiol 60 : 2568 2574.[PubMed]
103. Stewart CM, Cole MB, Legan JD, Slade L, Schaffner DW . 2005. Solute-specific effects of osmotic stress on Staphylococcus aureus. J Appl Microbiol 98 : 193 202[CrossRef].[PubMed]
104. Kültz D, Csonka L . 1999. What sets the TonE during osmotic stress? Proc Natl Acad Sci USA 96 : 1814 1816.
105. Bi S, Jin F, Sourjik V . 2018. Inverted signaling by bacterial chemotaxis receptors. Nat Commun 9 : 2927[CrossRef].[PubMed]
106. Vaknin A, Berg HC . 2006. Osmotic stress mechanically perturbs chemoreceptors in Escherichia coli. Proc Natl Acad Sci USA 103 : 592 596[CrossRef].[PubMed]
107. Blount P, Schroeder MJ, Kung C . 1997. Mutations in a bacterial mechanosensitive channel change the cellular response to osmotic stress. J Biol Chem 272 : 32150 32157[CrossRef].[PubMed]
108. Sleator RD, Gahan CGM, Hill C . 2003. A postgenomic appraisal of osmotolerance in Listeria monocytogenes. Appl Environ Microbiol 69 : 1 9[CrossRef].[PubMed]
109. Booth IR, Blount P . 2012. The MscS and MscL families of mechanosensitive channels act as microbial emergency release valves. J Bacteriol 194 : 4802 4809[CrossRef].[PubMed]
110. Ko R, Smith LT, Smith GM . 1994. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J Bacteriol 176 : 426 431[CrossRef].[PubMed]
111. Grothe S, Krogsrud RL, McClellan DJ, Milner JL, Wood JM . 1986. Proline transport and osmotic stress response in Escherichia coli K-12. J Bacteriol 166 : 253 259[CrossRef].[PubMed]
112. Csonka LN . 1989. Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev 53 : 121 147.[PubMed]
113. Barth M, Marschall C, Muffler A, Fischer D, Hengge-Aronis R . 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 : 3455 3464[CrossRef].[PubMed]
114. Culham DE, Lu A, Jishage M, Krogfelt KA, Ishihama A, Wood JM . 2001. The osmotic stress response and virulence in pyelonephritis isolates of Escherichia coli: contributions of RpoS, ProP, ProU and other systems. Microbiology 147 : 1657 1670[CrossRef].[PubMed]
115. Chuang SE, Daniels DL, Blattner FR . 1993. Global regulation of gene expression in Escherichia coli. J Bacteriol 175 : 2026 2036[CrossRef].[PubMed]
116. Shin S, Park C . 1995. Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J Bacteriol 177 : 4696 4702[CrossRef].[PubMed]
117. Brzostek K, Skorek K, Raczkowska A, . 2012. OmpR, a central integrator of several cellular responses in Yersinia enterocolitica, p 325 334. In de Almeida AMP, Leal NC (ed), Advances in Yersinia Research. Springer, New York, NY.
118. Liao MK, Maloy S . 2001. Substrate recognition by proline permease in Salmonella. Amino Acids 21 : 161 174[CrossRef].[PubMed]
119. Liu LK, Becker DF, Tanner JJ . 2017. Structure, function, and mechanism of proline utilization A (PutA). Arch Biochem Biophys 632 : 142 157[CrossRef].[PubMed]
120. Gardan R, Duché O, Leroy-Sétrin S, Labadie J European Listeria Genome Consortium . 2003. Role of ctc from Listeria monocytogenes in osmotolerance. Appl Environ Microbiol 69 : 154 161[CrossRef].[PubMed]
121. Hain T, Hossain H, Chatterjee SS, Machata S, Volk U, Wagner S, Brors B, Haas S, Kuenne CT, Billion A, Otten S, Pane-Farre J, Engelmann S, Chakraborty T . 2008. Temporal transcriptomic analysis of the Listeria monocytogenes EGD-e σ B regulon. BMC Microbiol 8 : 20[CrossRef].[PubMed]
122. Sleator RD, Gahan CGM, Hill C . 2001. Identification and disruption of the proBA locus in Listeria monocytogenes: role of proline biosynthesis in salt tolerance and murine infection. Appl Environ Microbiol 67 : 2571 2577[CrossRef].[PubMed]
123. Cebrián G, Arroyo C, Condón S, Mañas P . 2015. Osmotolerance provided by the alternative sigma factors σ B and rpoS to Staphylococcus aureus and Escherichia coli is solute dependent and does not result in an increased growth fitness in NaCl containing media. Int J Food Microbiol 214 : 83 90[CrossRef].[PubMed]
124. Vilhelmsson O, Miller KJ . 2002. Synthesis of pyruvate dehydrogenase in Staphylococcus aureus is stimulated by osmotic stress. Appl Environ Microbiol 68 : 2353 2358[CrossRef].[PubMed]
125. Stimeling KW, Graham JE, Kaenjak A, Wilkinson BJ . 1994. Evidence for feedback (trans)regulation of, and two systems for, glycine betaine transport by Staphylococcus aureus. Microbiology 140 : 3139 3144[CrossRef].[PubMed]
126. Schumann W . 2016. Regulation of bacterial heat shock stimulons. Cell Stress Chaperones 21 : 959 968[CrossRef].[PubMed]
127. Mongkolsuk S, Helmann JD . 2002. Regulation of inducible peroxide stress responses. Mol Microbiol 45 : 9 15[CrossRef].[PubMed]
128. Storz G, Zheng M, . 2000. Oxidative stress, p 47 59. In Storz G, Hengge-Aronis R (ed), Bacterial Stress Responses. ASM Press, Washington, DC.
129. Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA, Storz G . 2001. DNA-microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183 : 4562 4570.
130. Helmann JD, Wu MFW, Kobel PA, Gamo F-J, Wilson M, Morshedi MM, Navre M, Paddon C . 2001. Global transcriptional response of Bacillus subtilis to heat shock. J Bacteriol 183 : 7318 7328[CrossRef].[PubMed]
131. Rea RB, Gahan CGM, Hill C . 2004. Disruption of putative regulatory loci in Listeria monocytogenes demonstrates a significant role for Fur and PerR in virulence. Infect Immun 72 : 717 727[CrossRef].[PubMed]
132. Rea R, Hill C, Gahan CGM . 2005. Listeria monocytogenes PerR mutants display a small-colony phenotype, increased sensitivity to hydrogen peroxide, and significantly reduced murine virulence. Appl Environ Microbiol 71 : 8314 8322[CrossRef].[PubMed]
133. Derré I, Rapoport G, Msadek T . 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 : 117 131[CrossRef].[PubMed]
134. Schlesinger MJ . 1990. Heat shock proteins. J Biol Chem 265 : 12111 12114.[PubMed]
135. Noor R . 2015. Mechanism to control the cell lysis and the cell survival strategy in stationary phase under heat stress. Springerplus 4 : 599[CrossRef].[PubMed]
136. Van Derlinden E, Bernaerts K, Van Impe JF . 2008. Dynamics of Escherichia coli at elevated temperatures: effect of temperature history and medium. J Appl Microbiol 104 : 438 453.[PubMed]
137. Gunasekera TS, Csonka LN, Paliy O . 2008. Genome-wide transcriptional responses of Escherichia coli K-12 to continuous osmotic and heat stresses. J Bacteriol 190 : 3712 3720[CrossRef].[PubMed]
138. Missiakas D, Raina S . 1997. Protein misfolding in the cell envelope of Escherichia coli: new signaling pathways. Trends Biochem Sci 22 : 59 63[CrossRef].[PubMed]
139. Dartigalongue C, Missiakas D, Raina S . 2001. Characterization of the Escherichia coli σ E regulon. J Biol Chem 276 : 20866 20875[CrossRef].[PubMed]
140. Liberek K, Galitski TP, Zylicz M, Georgopoulos C . 1992. The DnaK chaperone modulates the heat shock response of Escherichia coli by binding to the σ 32 transcription factor. Proc Natl Acad Sci USA 89 : 3516 3520[CrossRef].[PubMed]
141. Chuang SE, Blattner FR . 1993. Characterization of twenty-six new heat shock genes of Escherichia coli. J Bacteriol 175 : 5242 5252[CrossRef].[PubMed]
142. Gragerov A, Nudler E, Komissarova N, Gaitanaris GA, Gottesman ME, Nikiforov V . 1992. Cooperation of GroEL/GroES and DnaK/DnaJ heat shock proteins in preventing protein misfolding in Escherichia coli. Proc Natl Acad Sci USA 89 : 10341 10344[CrossRef].[PubMed]
143. Hecker M, Völker U . 2001. General stress response of Bacillus subtilis and other bacteria. Adv Microb Physiol 44 : 35 91[CrossRef].[PubMed]
144. Hecker M, Schumann W, Völker U . 1996. Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol 19 : 417 428[CrossRef].[PubMed]
145. Narberhaus F . 1999. Negative regulation of bacterial heat shock genes. Mol Microbiol 31 : 1 8[CrossRef].[PubMed]
146. Horn G, Hofweber R, Kremer W, Kalbitzer HR . 2007. Structure and function of bacterial cold shock proteins. Cell Mol Life Sci 64 : 1457 1470[CrossRef].[PubMed]
147. Ermolenko DN, Makhatadze GI . 2002. Bacterial cold-shock proteins. Cell Mol Life Sci 59 : 1902 1913[CrossRef].[PubMed]
148. Wemekamp-Kamphuis HH, Karatzas AK, Wouters JA, Abee T . 2002. Enhanced levels of cold shock proteins in Listeria monocytogenes LO28 upon exposure to low temperature and high hydrostatic pressure. Appl Environ Microbiol 68 : 456 463[CrossRef].[PubMed]
149. Alpas H, Kalchayanand N, Bozoglu F, Sikes A, Dunne CP, Ray B . 1999. Variation in resistance to hydrostatic pressure among strains of food-borne pathogens. Appl Environ Microbiol 65 : 4248 4251.[PubMed]
150. Benito A, Ventoura G, Casadei M, Robinson T, 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.[PubMed]
151. Rastogi NK, Raghavarao KS, Balasubramaniam VM, Niranjan K, Knorr D . 2007. Opportunities and challenges in high pressure processing of foods. Crit Rev Food Sci Nutr 47 : 69 112[CrossRef].[PubMed]
152. Hauben KJA, Bartlett DH, Soontjens CCF, Cornelis K, Wuytack EY, Michiels CW . 1997. Escherichia coli mutants resistant to inactivation by high hydrostatic pressure. Appl Environ Microbiol 63 : 945 950.[PubMed]
153. Gould G, . 2005. Pathogen resistance and adaptation to emerging technologies, p 442 459. In Griffitths M (ed), Understanding Pathogen Behaviour. Woodhead Publishing, Boca Raton, FL.[CrossRef]
154. Karatzas KAG, Bennik MHJ . 2002. Characterization of a Listeria monocytogenes Scott A isolate with high tolerance towards high hydrostatic pressure. Appl Environ Microbiol 68 : 3183 3189[CrossRef].[PubMed]
155. Aertsen A, Van Houdt R, Vanoirbeek K, Michiels CW . 2004. An SOS response induced by high pressure in Escherichia coli. J Bacteriol 186 : 6133 6141[CrossRef].[PubMed]
156. Niven GW, Miles CA, Mackey BM . 1999. The effects of hydrostatic pressure on ribosome conformation in Escherichia coli: and in vivo study using differential scanning calorimetry. Microbiology 145 : 419 425[CrossRef].[PubMed]
157. Robey M, Benito A, Hutson RH, Pascual C, Park SF, Mackey BM . 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[CrossRef].[PubMed]
158. Welch TJ, Farewell A, Neidhardt FC, Bartlett DH . 1993. Stress response of Escherichia coli to elevated hydrostatic pressure. J Bacteriol 175 : 7170 7177[CrossRef].[PubMed]
159. Wemekamp-Kamphuis HH, Wouters JA, de Leeuw PPLA, Hain T, Chakraborty T, Abee T . 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 : 3457 3466[CrossRef].[PubMed]
160. Horn N, Bhunia AK . 2018. Food-associated stress primes foodborne pathogens for the gastrointestinal phase of infection. Front Microbiol 9 : 1962[CrossRef].[PubMed]
161. Fang FC, Libby SJ, Buchmeier NA, Loewen PC, Switala J, Harwood J, Guiney DG . 1992. The alternative sigma factor katF ( rpoS) regulates Salmonella virulence. Proc Natl Acad Sci USA 89 : 11978 11982[CrossRef].[PubMed]
162. Yildiz FH, Schoolnik GK . 1998. Role of rpoS in stress survival and virulence of Vibrio cholerae. J Bacteriol 180 : 773 784.[PubMed]
163. Maserati A, Fink RC, Lourenco A, Julius ML, Diez-Gonzalez F . 2017. General response of Salmonella enterica serovar Typhimurium to desiccation: a new role for the virulence factors sopD and sseD in survival. PLoS One 12 : e0187692[CrossRef].[PubMed]
164. Chang RL, Andrews K, Kim D, Li Z, Godzik A, Palsson . 2013. Structural systems biology evaluation of metabolic thermotolerance in Escherichia coli. Science 340 : 1220 1223[CrossRef].[PubMed]


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Table 4.1

Classes of heat shock genes in Gram-positive bacteria

Citation: Diez-Gonzalez F. 2019. Stress Responses in Foodborne Bacteria, p 79-99. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch4

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