Cold stress tolerance of Listeria monocytogenes: A review of molecular adaptive mechanisms and food safety implications

Journal of Food Protection

Volumn 69, Issue 6, 2006, Pages 1473-1484

  Tasara, T ^a   Stephan, R ^a,b  

^a VETSUISSE FACULTY UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

LISTERIA MONOCYTOGENES;

EID: 33745110969     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X-69.6.1473     Document Type: Review

References (109)

1. Aguilar, P. S., J. E. Cronan, and D. de Mendoza. 1998. A Bacillus subtilis gene induced by cold shock encodes a membrane phospholipid desaturase. J. Bacteriol. 180:2194-2200.
2. Angelidis, A. S., and G. M. Smith. 2003. Role of the glycine betaine and carnitine transporters in adaptation of Listeria monocytogenes to chill stress in defined medium. Appl. Environ. Microbiol. 69:7492-7498.
3. Angelidis, A. S., L. T. Smith, L. M. Hoffman, and G. M. Smith. 2002. Identification of opuC as a chill-activated and osmotically activated carnitine transporter in Listeria monocytogenes. Appl. Environ. Microbiol. 68:2644-2650.
4. Angelidis, A. S., L. T. Smith, and G. M. Smith. 2002. Elevated carnitine accumulation by Listeria monocytogenes impaired in glycine betaine transport is insufficient to restore wild-type cryotolerance in milk whey. Int. J. Food Microbiol. 75:1-9.
5. Annous, B. A., L. A. Becker, D. O. Bayles, D. P. Labeda, and B. J. Wilkinson. 1997. Critical role of anteiso-C15:0 fatty acid in the growth of Listeria monocytogenes at low temperatures. Appl. Environ. Microbiol. 63:3887-3894.
6. 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. 62:1116-1119.
7. Bayles, D. O., M. H. Tunick, T. A. Foglia, and A. J. Miller. 2000. Cold shock and its effect on ribosomes and thermal tolerance in Listeria monocytogenes. Appl. Environ. Microbiol. 66:4351-4355.
8. Bayles, D. O., and B. J. Wilkinson. 2000. Osmoprotectants and cryoprotectants for Listeria monocytogenes. Lett. Appl. Microbiol. 30:23-27.
9. Becker, L. A., M. S. Cetin, R. W. Hutkins, and A. K. Benson. 1998. Identification of the gene encoding the alternative sigma factor sigmaB from Listeria monocytogenes and its role in osmotolerance. J. Bacteriol. 180:4547-4554.
10. Becker, L. A., S. N. Evans, R. W. Hutkins, and A. K. Benson. 2000. Role of sigma(B) in adaptation of Listeria monocytogenes to growth at low temperature. J. Bacteriol. 182:7083-7087.
11. Beumer, R. R., M. C. Te Giffel, L. J. Cox, F. M. Rombouts, and T. Abee. 1994. Effect of exogenous proline, betaine, and carnitine on growth of Listeria monocytogenes in a minimal medium. Appl. Environ. Microbiol. 60:1359-1363.
12. Borezee, E., E. Pellegrini, and P. Berche. 2000. OppA of Listeria monocytogenes, an oligopeptide-binding protein required for bacterial growth at low temperature and involved in intracellular survival. Infect. Immun. 68:7069-7077.
13. Bozzi, M., G. Mignogna, S. Stefanini, D. Barra, C. Longhi, P. Valenti, and E. Chiancone. 1997. A novel non-heme iron-binding ferritin related to the DNA-binding proteins of the Dps family in Listeria innocua. J. Biol. Chem. 272:3259-3265.
14. Brondsted, L., B. H. Kallipolitis, H. 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. 219:233-239.
15. Cetin, M. S., C. Zhang, R. W. Hutkins, and A. K. Benson. 2004. Regulation of transcription of compatible solute transporters by the general stress sigma factor, sigmaB, in Listeria monocytogenes. J. Bacteriol. 186:794-802.
16. Chastanet, A., I. Derre, S. Nair, and T. Msadek. 2004. clpB, a novel member of the Listeria monocytogenes CtsR regulon, is involved in virulence but not in general stress tolerance. J. Bacteriol. 186:1165-1174.
17. Chaturongakul, S., and K. J. Boor. 2004. RsbT and RsbV contribute to sigmaB-dependent survival under environmental, energy, and intracellular stress conditions in Listeria monocytogenes. Appl. Environ. Microbiol 70:5349-5356.
18. Christiansen, J. K., M. H. Larsen, H. Ingmer, L. Sogaard-Andersen, and B. H. Kallipolitis. 2004. The RNA-binding protein Hfq of Listeria monocytogenes: role in stress tolerance and virulence. J. Bacteriol. 186:3355-3362.
19. Condon, C., D. Liveris, C. Squires, I. Schwartz, and C. L. Squires. 1995. rRNA operon multiplicity in Escherichia coli and the physiological implications of rrn inactivation. J. Bacteriol. 177:4152-4156.
20. de Mendoza, D., R. Grau, and J. E. Cronan, Jr. 1993. Biosynthesis and function of membrane lipids, p. 411-421. In Sonenshine, A. L., J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and other gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, D.C.
21. Dons, L., O. F. Rasmussen, and J. E. Olsen. 1992. Cloning and characterization of a gene encoding flagellin of Listeria monocytogenes. Mol. Microbiol. 6:2919-2929.
22. Dutta, R., L. Qin, and M. Inouye. 1999. Histidine kinases: diversity of domain organization. Mol. Microbiol. 34:633-640.
23. Ermolenko, D. N., and G. I. Makhatadze. 2002. Bacterial cold-shock proteins. Cell Mol. Life Sci. 59:1902-1913.
24. Farber, J. M., and P. I. Peterkin. 1991. Listeria monocytogenes, a food-borne pathogen. Microbiol. Rev. 55:476-511.
25. Fraser, K. R., D. Harvie, P. J. Coote, and C. P. O'Byrne. 2000. Identification and characterization of an ATP binding cassette L-carnitine transporter in Listeria monocytogenes. Appl. Environ. Microbiol. 66:4696-4704.
26. Fraser, K. R., D. Sue, M. Wiedmann, K. Boor, and C. P. O'Byrne. 2003. Role of sigmaB in regulating the compatible solute uptake systems of Listeria monocytogenes: osmotic induction of opuC is sigmaB dependent. Appl. Environ. Microbiol. 69:2015-2022.
27. Gaillot, O., E. Pellegrini, S. Bregenholt, S. Nair, and P. Berche. 2000. The ClpP serine protease is essential for the intracellular parasitism and virulence of Listeria monocytogenes. Mol., Microbiol. 35:1286-1294.
28. Gerhardt, P. N., L. Tombras Smith, and G. M. Smith. 2000. Osmotic and chill activation of glycine betaine porter II in Listeria monocytogenes membrane vesicles. J. Bacteriol. 182:2544-2550.
29. Giovannacci, I., C. Ragimbeau, S. Queguiner, G. Salvat, J. L. Vendeuvre, V. Carlier, and G. Ermel. 1999. Listeria monocytogenes in pork slaughtering and cutting plants: use of RAPD, PFGE and PCR-REA for tracing and molecular epidemiology. Int. J. Food. Microbiol. 53:127-140.
30. Glaser, P., L. Frangeul, C. Buchrieser, C. Rusniok, A. Amend, F. Baquero, P. Berche, H. Bloecker, P. Brandt, T. Chakraborty, A. Charbit, F. Chetouani, E. Couve, A. de Daruvar, P. Dehoux, E. Domann, G. Dominguez-Bernal, E. Duchaud, L. Durant, O. Dussurget, K. D. Entian, H. Fsihi, F. Garcia-del Portillo, P. Garrido, L. Gautier, W. Goebel, N. Gomez-Lopez, T. Hain, J. Hauf, D. Jackson, L. M. Jones, U. Kaerst, J. Kreft, M. Kuhn, F. Kunst, G. Kurapkat, E. Madueno, A. Maitournam, J. M. Vicente, E. Ng, H. Nedjari, G. Nordsick, S. Novella, B. de Pablos, J. C. Perez-Diaz, R. Purcell, B. Remmel, M. Rose, T. Schlueter, N. Simoes, A. Tierrez, J. A. Vazquez-Boland, H. Voss, J. Wehland, and P. Cossart. 2001. Comparative genomics of Listeria species. Science 294:849-852.
31. Goldstein, J., N. S. Pollitt, and M. Inouye. 1990. Major cold shock protein of Escherichia coli. Proc. Natl. Acad. Sci. USA 87:283-287.
32. Graumann, P., and M. A. Marahiel. 1996. Some like it cold: response of microorganisms to cold shock. Arch. Microbiol. 166:293-300.
33. Graumann, P., and M. A. Marahiel. 1997. Effects of heterologous expression of CspB, the major cold shock protein of Bacillus subtilis, on protein synthesis in Escherichia coli. Mol. Gen. Genet. 253:745-752.
34. Graumann, P. L., and M. A. Marahiel. 1998. A superfamily of proteins that contain the cold-shock domain. Trends Biochem. Sci. 23:286-290.
35. Graumann, P. L., and M. A. Marahiel. 1999. Cold shock response in Bacillus subtilis. J. Mol. Microbiol. Biotechnol. 1:203-209.
36. Graumann, P., T. M. Wendrich, M. H. Weber, K. Schroder, and M. A. Marahiel. 1997. A family of cold shock proteins in Bacillus subtilis is essential for cellular growth and for efficient protein synthesis at optimal and low temperatures. Mol. Microbiol. 25:741-756.
37. Gray, M. J., R. N. Zadoks, E. D. Fortes, B. Dogan, S. Cai, Y. Chen, V. N. Scott, D. E. Gombas, K. J. Boor, and M. Wiedmann. 2004. Listeria monocytogenes isolates from foods and humans form distinct but overlapping populations. Appl. Environ. Microbiol. 70:5833-5841.
38. Grundling, A., L. S. Burrack, H. G. Bouwer, and D. E. Higgins. 2004. Listeria monocytogenes regulates flagellar motility gene expression through MogR, a transcriptional repressor required for virulence. Proc. Natl. Acad. Sci. USA 101:12318-12323.
39. Hartke, A., J. Frere, P. Boutibonnes, and Y. Auffray. 1997. Differential induction of the chaperonin GroEL and the Co-chaperonin GroES by heat, acid, and UV-irradiation in Lactococcus lactis subsp. lactis. Curr. Microbiol. 34:23-26.
40. Hebraud, M., and J. Guzzo. 2000. The main cold shock protein of Listeria monocytogenes belongs to the family of ferritin-like proteins. FEMS Microbiol. Lett. 190:29-34.
41. Holmgren, A. 1985. Thioredoxin. Annu. Rev. Biochem. 54:237-271.
42. Jaradat, Z. W., G. E. Schutze, and A. K. Bhunia. 2002. Genetic homogeneity among Listeria monocytogenes strains from infected patients and meat products from two geographic locations determined by phenotyping, ribotyping and PCR analysis of virulence genes. Int. J. Food Microbiol. 76:1-10.
43. Jones, C. E., G. Shama, D. Jones, I. S. Roberts, and P. W. Andrew. 1997. Physiological and biochemical studies on psychrotolerance in Listeria monocytogenes. J. Appl. Microbiol. 83:31-35.
44. Juneja, V. K., T. A. Foglia, and B. S. Marmer. 1998. Heat resistance and fatty acid composition of Listeria monocytogenes: effect of pH, acidulant, and growth temperature. J. Food Prot. 61:683-687.
45. Junttila, J. R., S. I. Niemela, and J. Hirn. 1988. Minimum growth temperatures of Listeria monocytogenes and non-haemolytic Listeria. J. Appl. Bacteriol. 65:321-327.
46. Kathariou, S. 2002. Listeria monocytogenes virulence and pathogenicity: a food safety perspective. J. Food Prot. 65:1811-1829.
47. Knudsen, G. M., J. E. Olsen, and L. Dons. 2004. Characterization of DegU, a response regulator in Listeria monocytogenes, involved in regulation of motility and contributes to virulence. FEMS Microbiol. Lett. 240:171-179.
48. Ko, R., and L. T. Smith. 1999. Identification of an ATP-driven, osmoregulated glycine betaine transport system in Listeria monocytogenes. Appl. Environ. Microbiol. 65:4040-4048.
49. Ko, R., L. T. Smith, and G. M. Smith. 1994. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J. Bacteriol. 176:426-431.
50. Ligozzi, M., F. Pittaluga, and R. Fontana. 1993. Identification of a genetic element (psr) which negatively controls expression of Enterococcus hirae penicillin-binding protein 5. J. Bacteriol. 175:2046-2051.
51. Lippert, K., and A. E. Galinski. 1992. Enzyme stabilization by ectoine-type compatible solutes: protection against heating, freezing and drying. Appl. Microbiol. Biotechnol 37:61-65.
52. Liu, S., J. E. Graham, L. Bigelow, P. D. Morse 2nd, and B. J. Wilkinson. 2002. Identification of Listeria monocytogenes genes expressed in response to growth at low temperature. Appl. Environ. Microbiol. 68:1697-1705.
53. Lou, Y., and A. E. Yousef. 1999. Characteristics of Listeria monocytogenes important to food processors, p. 131-224. In E. T. Ryser and E. H. Marth (ed.), Listeria, listeriosis and food safety. Marcel Dekker, New York.
54. Mafu, A. A., D. Roy, J. Goulet, L. Savoie, and R. Roy. 1990. Efficiency of sanitizing agents for destroying Listeria monocytogenes on contaminated surfaces. J. Dairy Sci. 73:3428-3432.
55. Massidda, O., R. Kariyama, L. Daneo-Moore, and G. D. Shockman. 1996. Evidence that the PBP 5 synthesis repressor (psr) of Enterococcus hirae is also involved in the regulation of cell wall composition and other cell wall-related properties. J. Bacteriol. 178:5272-5278.
56. Mead, P. S., L. Slutsker, V. Dietz, L. F. McCaig, J. S. Bresee, C. Shapiro, P. M. Griffin, and R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-625.
57. Mendum, M. L., and L. T. Smith. 2002. Characterization of glycine betaine porter I from Listeria monocytogenes and its roles in salt and chill tolerance. Appl. Environ. Microbiol. 68:813-819.
58. Mikami, K., Y. Kanesaki, I. Suzuki, and N. Murata. 2002. The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp. PCC 6803. Mol. Microbiol. 46:905-915.
59. Moorhead, S. M., and G. A. Dykes. 2003. The role of the sigB gene in the general stress response of Listeria monocytogenes varies between a strain of serotype 1/2a and a strain of serotype 4c. Curr. Microbiol. 46:461-466.
60. Moorhead, S. M., and G. A. Dykes. 2004. Influence of the sigB gene on the cold stress survival and subsequent recovery of two Listeria monocytogenes serotypes. Int. J. Food Microbiol. 91:63-72.
61. Nelson, K. E., D. E. Fouts, E. F. Mongodin, J. Ravel, R. T. DeBoy, J. F. Kolonay, D. A. Rasko, S. V. Angiuoli, S. R. Gill, I. T. Paulsen, J. Peterson, O. White, W. C. Nelson, W. Nierman, M. J. Beanan, L. M. Brinkac, S. C. Daugherty, R. J. Dodson, A. S. Durkin, R. Madupu, D. H. Haft, J. Selengut, S. Van Aken, H. Khouri, N. Fedorova, H. Forberger, B. Tran, S. Kathariou, L. D. Wonderling, G. A. Uhlich, D. O. Bayles, J. B. Luchansky, and C. M. Fraser. 2004. Whole genome comparisons of serotype 4b and 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species. Nucleic Acids Res. 32:2386-2395.
62. Nightingale, K. K., Y. H. Schukken, C. R. Nightingale, E. D. Fortes, A. J. Ho, Z. Her, Y. T. Grohn, P. L. McDonough, and M. Wiedmann. 2004. Ecology and transmission of Listeria monocytogenes infecting ruminants and in the farm environment. Appl. Environ. Microbiol. 70:4458-4467.
63. Norrung, B., and N. Skovgaard. 1993. Application of multilocus enzyme electrophoresis in studies of the epidemiology of Listeria monocytogenes in Denmark. Appl. Environ. Microbiol. 59:2817-2822.
64. Peel, M., W. Donachie, and A. Shaw. 1988. Temperature-dependent expression of flagella of Listeria monocytogenes studied by electron microscopy, SDS-PAGE and Western blotting. J. Gen. Microbiol. 134:2171-2178.
65. Phadtare, S., J. Alsina, and M. Inouye. 1999. Cold-shock response and cold-shock proteins. Curr. Opin. Microbiol. 2:175-180.
66. Phan-Thanh, L., and T. Gormon. 1995. Analysis of heat and cold shock proteins in Listeria by two-dimensional electrophoresis. Electrophoresis 16:444-450.
67. Posfay-Barbe, K. M., and E. R. Wald. 2004. Listeriosis. Pediatr. Rev. 25:151-159.
68. Pruss, B. M., K. P. Francis, F. von Stetten, and S. Scherer. 1999. Correlation of 16S ribosomal DNA signature sequences with temperature-dependent growth rates of mesophilic and psychrotolerant strains of the Bacillus cereus group. J. Bacteriol. 181:2624-2630.
69. Puttmann, M., N. Ade, and H. Hof. 1993. Dependence of fatty acid composition of Listeria spp. on growth temperature. Res. Microbiol. 144:279-283.
70. Rhodes, D., and A. D. Hanson. 1993. Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44:357-384.
71. Rocourt, J., and J. Bille. 1997. Foodborne listeriosis. World Health Stat. Q. 50:67-73.
72. Rocourt, J., C. Jacquet, and A. Reilly. 2000. Epidemiology of human listeriosis and seafoods. Int. J Food Microbiol. 62:197-209.
73. Rowbury, R. J. 2003. Physiology and molecular basis of stress adaptation with particular reference to the subversion of stress adaptation, and to the involvement of extracellular components in adaptation, p. 247-302. In E. A. Yousef and K. V. Juneja (ed.), Microbial stress adaptation and food safety, CRC Press, London.
74. Ryser, E. T., and E. H. Marth. 1989. "New" food-borne pathogens of public health significance. J. Am. Diet Assoc. 89:948-954.
75. Salotra, P., D. K. Singh, K. P. Seal, N. Krishna, H. Jaffe, and R. Bhatnagar. 1995. Expression of DnaK and GroEL homologs in Leuconostoc esenteroides in response to heat shock, cold shock or chemical stress. FEMS Microbiol. Lett. 131:57-62.
76. Schuchat, A., B. Swaminathan, and C. V. Broome. 1991. Epidemiology of human listeriosis. Clin. Microbiol. Rev. 4:169-183.
77. Senczek, D., R. Stephan, and F. Untermann. 2000. Pulsed-field gel electrophoresis (PFGE) typing of Listeria strains isolated from a meat processing plant over a 2-year period. Int. J. Food. Microbiol. 62:155-159.
78. Sleator, R. D., G. A. Francis, D. O'Beirne, C. G. Gahan, and C. Hill. 2003. Betaine and carnitine uptake systems in Listeria monocytogenes affect growth and survival in foods and during infection. J. Appl. Microbiol. 95:839-846.
79. Sleator, R. D., C. G. Gahan, T. Abee, and C. Hill. 1999. Identification and disruption of BetL, a secondary glycine betaine transport system linked to the salt tolerance of Listeria monocytogenes LO28. Appl. Environ. Microbiol. 65:2078-2083.
80. Sleator, R. D., C. G. Gahan, and C. Hill. 2003. A postgenomic appraisal of osmotolerance in Listeria monocytogenes. Appl. Environ. Microbiol. 69:1-9.
81. Sleator, R. D., C. G. M. Gahan, B. O'Driscoll, and C. Hill. 2000. Analysis of the role of betL in contributing to the growth and survival of Listeria monocytogenes LO28. Int. J. Food Microbiol. 60:261-268.
82. Sleator, R. D., and C. Hill. 2001. Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol. Rev. 26:49-71.
83. Sleator, R. D., J. Wouters, C. G. Gahan, T. Abee, and C. Hill. 2001. Analysis of the role of OpuC, an osmolyte transport system, in salt tolerance and virulence potential of Listeria monocytogenes. Appl. Environ. Microbiol. 67:2692-2698.
84. Smith, L. T. 1996. Role of osmolytes in adaptation of osmotically stressed and chill-stressed Listeria monocytogenes grown in liquid media and on processed meat surfaces. Appl. Environ. Microbiol. 62:3088-3093.
85. Sommerville, J., and M. Ladomery. 1996. Masking of mRNA by Y-box proteins. FASEB J. 10:435-443.
86. Suutari, M., and S. Laakso. 1994. Microbial fatty acids and thermal adaptation. Crit. Rev. Microbiol. 20:285-328.
87. Suzuki, I., Y. Kanesaki, K. Mikami, M. Kanehisa, and N. Murata. 2001. Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol. Microbiol. 40:235-244.
88. Tappero, J. W., A. Schuchat, K. A. Deaver, L. Mascola, and J. D. Wenger. 1995. Reduction in the incidence of human listeriosis in the United States-effectiveness of prevention efforts? The Listeriosis Study Group. JAMA 273:1118-1122.
89. Thieringer, H. A., P. G. Jones, and M. Inouye. 1998. Cold shock and adaptation. Bioessays 20:49-57.
90. Trussel, M. 1989. The occurrence of Listeria in the production of processed meat, salami and mettwurst. Schweiz Arch. Tierheilkd. 131:417-421.
91. VanBogelen, R. A., and F. C. Neidhardt. 1990. Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc. Natl. Acad. Sci. USA 87:5589-5593.
92. van Schaik, W., and T. Abee. 2005. The role of sigmaB in the stress response of gram-positive bacteria-targets for food preservation and safety. Curr. Opin. Biotechnol. 16:218-224.
93. Vazquez-Boland, J. A., M. Kuhn, P. Berche, T. Chakraborty, G. Dominguez-Bernal, W. Goebel, B. Gonzalez-Zorn, J. Wehland, and J. Kreft. 2001. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14:584-640.
94. Verheul, A., A. Hagting, M. R. Amezaga, I. R. Booth, F. M. Rombouts, and T. Abee. 1995. A di- and tripeptide transport system can supply Listeria monocytogenes Scott A with amino acids essential for growth. Appl. Environ. Microbiol. 61:226-233.
95. Verheul, A., F. M. Rombouts, and T. Abee. 1998. Utilization of oligopeptides by Listeria monocytogenes Scott A. Appl. Environ. Microbiol. 64:1059-1065.
96. Verbeul, A., F. M. Rombouts, R. R. Beumer, and T. Abee. 1995. An ATP-dependent L-carnitine transporter in Listeria monocytogenes Scott A is involved in osmoprotection. J. Bacteriol. 177:3205-3212.
97. Vigh, L., 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. 23:369-374.
98. Walker, S. J., P. Archer, and J. G. Banks. 1990. Growth of Listeria monocytogenes at refrigeration temperatures. J. Appl. Bacteriol. 68:157-162.
99. Way, S. S., L. J. Thompson, J. E. Lopes, A. M. Hajjar, T. R. Kollmann, N. E. Freitag, and C. B. Wilson. 2004. Characterization of flagellin expression and its role in Listeria monocytogenes infection and immunity. Cell Microbiol. 6:235-242.
100. 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. 68:456-463.
101. Wemekamp-Kamphuis, H. H., R. D. Sleator, J. A. Wouters, C. Hill, and T. Abee. 2004. Molecular and physiological analysis of the role of osmolyte transporters BetL, Gbu, and OpuC in growth of Listeria monocytogenes at low temperatures. Appl. Environ. Microbiol. 70:2912-2918.
102. Wemekamp-Kamphuis, H. H., J. A. Wouters, P. P. de Leeuw, T. Hain, T. Chakraborty, and T. Abee. 2004. Identification of sigma factor sigma 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.
103. West, A. H., and A. M. Stock. 2001. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci. 26:369-376.
104. Wiedmann, M. 2002. Molecular subtyping methods for Listeria monocytogenes. J. AOAC Int. 85:524-531.
105. Williams, T., S. Bauer, D. Beier, and M. Kuhn. 2005. Construction and characterization of Listeria monocytogenes mutants with inframe deletions in the response regulator genes identified in the genome sequence. Infect. Immun. 73:3152-3159.
106. Wouters, J. A., F. M. Rombouts, O. P. Kuipers, W. M. de Vos, and T. Abee. 2000. The role of cold-shock proteins in low-temperature adaptation of food-related bacteria. Syst. Appl. Microbiol. 23:165-173.
107. Yamanaka, K., L. Fang, and M. Inouye. 1998. The CspA family in Escherichia coli: multiple gene duplication for stress adaptation. Mol. Microbiol. 27:247-255.
108. Zhang, S., J. M. Scott, and W. G. Haldenwang. 2001. Loss of ribosomal protein L11 blocks stress activation of the Bacillus subtilis transcription factor sigma(B). J. Bacteriol. 183:2316-2321.
109. Zheng, W., and S. Kathariou. 1994. Transposon-induced mutants of Listeria monocytogenes incapable of growth at low temperature (4 degrees C). FEMS Microbiol. Lett. 121:287-291.