Gene expression induced in Escherichia coli O157:H7 upon exposure to model apple juice

Applied and Environmental Microbiology

Volumn 75, Issue 11, 2009, Pages 3542-3553

  Bergholz, Teresa M ^a,b   Vanaja, Sivapriya Kailasan ^a   Whittam, Thomas S ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APPLE JUICE; BEFORE AND AFTER; ESCHERICHIA COLI O157:H7; FOOD MATRIXES; FOOD-BORNE ILLNESS; MULTIPLE STRESS; OPEN READING FRAME; OSMOTIC STRESS; OXIDATIVE STRESS RESPONSE; PARENT STRAIN; STRESS RESPONSE; TRANSCRIPTOMES;

ACIDS; ESCHERICHIA COLI; FRUITS; GENES; TRANSCRIPTION; VEHICLE TRANSMISSIONS;

FRUIT JUICES;

TRANSCRIPTOME;

BACTERIUM; DISEASE PREVALENCE; DISEASE TRANSMISSION; GENE EXPRESSION; MODELING; OSMOSIS; OXIDATION; PLANT EXTRACT; SURVIVAL;

ACIDITY; APPLE JUICE; ARTICLE; BACTERIAL GENE; BACTERIAL SURVIVAL; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; ESCHERICHIA COLI O157; FOOD CONTAMINATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE INDUCTION; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OSMOTIC STRESS; OXIDATIVE STRESS;

BEVERAGES; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MALUS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; STRESS, PHYSIOLOGICAL; UP-REGULATION;

ESCHERICHIA COLI; MALUS X DOMESTICA; SPINACIA OLERACEA;

EID: 66249085888     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02841-08     Document Type: Article

References (94)

1. Allen, K. J., D. Lepp, R. C. McKellar, and M. W. Griffiths. 2008. Examination of stress and virulence gene expression in Escherichia coli O157:H7 using targeted microarray analysis. Foodborne Pathog. Dis. 5:437-447.
2. 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. 183:2178-2186.
3. Arnold, K. W., and C. W. Kaspar. 1995. Starvation- and stationary-phase-induced acid tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 61:2037-2039.
4. Beloin, C., J. Valle, P. Latour-Lambert, P. Faure, M. Kzreminski, D. Balestrino, J. A. Haagensen, S. Molin, G. Prensier, B. Arbeille, and J. M. Ghigo. 2004. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol. Microbiol. 51:659-674.
5. Beltrametti, F., A. U. Kresse, and C. A. Guzman. 1999. Transcriptional regulation of the esp genes of enterohemorrhagic Escherichia coli. J. Bacteriol. 181:3409-3418.
6. Benjamin, M. M., and A. R. Datta. 1995. Acid tolerance of enterohemorrhagic Escherichia coli. Appl. Environ. Microbiol. 61:1669-1672.
7. Bergholz, T. M., L. M. Wick, W. Qi, J. T. Riordan, L. M. Ouellette, and T. S. Whittam. 2007. Global transcriptional response of Escherichia coli O157:H7 to growth transitions in glucose minimal medium. BMC Microbiol. 7:97.
8. Besser, R. E., S. M. Lett., J. T. Weber, M. P. Doyle, T. J. Barrett, J. G. Wells, and P. M. Griffin. 1993. An outbreak of diarrhea and hemolytic uremic syndrome from Escherichia coli O157:H7 in fresh-pressed apple cider. JAMA 269:2217-2220.
9. Bianchi, A. A., and F. Baneyx. 1999. Hyperosmotic shock induces the sigma32 and sigmaE stress regulons of Escherichia coli. Mol. Microbiol. 34:1029-1038.
10. Blauwkamp, T. A., and A. J. Ninfa. 2002. Physiological role of the GlnK signal transduction protein of Escherichia coli: survival of nitrogen starvation. Mol. Microbiol. 46:203-214.
11. Breuer, T., D. H. Benkel, R. L. Shapiro, W. N. Hall, M. M. Winnett, M. J. Linn, J. Neimann, T. J. Barrett, S. Dietrich, F. P. Downes, D. M. Toney, J. L. Pearson, H. Rolka, L. Slutsker, and P. M. Griffin. 2001. A multistate outbreak of Escherichia coli O157:H7 infections linked to alfalfa sprouts grown from contaminated seeds. Emerg. Infect. Dis. 7:977-982.
12. Cayley, S., B. A. Lewis, H. J. Guttman, and M. T. Record, Jr. 1991. Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity. Implications for protein-DNA interactions in vivo. J. Mol. Biol. 222:281-300.
13. Centers for Disease Control and Prevention. 2007. Escherichia coli O157:H7 infection associated with drinking raw milk - Washington and Oregon, November-December 2005. MMWR Morb. Mortal. Wkly. Rep. 56:165-167.
14. Centers for Disease Control and Prevention. 1997. Escherichia coli O157:H7 infections associated with eating a nationally distributed commercial brand of frozen ground beef patties and burgers - Colorado, 1997. MMWR Morb. Mortal. Wkly. Rep. 46:777-778.
15. Centers for Disease Control and Prevention. 1995. Escherichia coli O157:H7 outbreak linked to commercially distributed dry-cured salami - Washington and California, 1994. MMWR Morb. Mortal. Wkly. Rep. 44:157-160.
16. Centers for Disease Control and Prevention. 2006. Ongoing multistate outbreak of Escherichia coli serotype O157:H7 infections associated with consumption of fresh spinach - United States, September 2006. MMWR Morb. Mortal. Wkly. Rep. 55:1045-1046.
17. Centers for Disease Control and Prevention. 1993. Update: multistate outbreak of Escherichia coli O157:H7 infections from hamburgers - western United States, 1992-1993. MMWR Morb. Mortal. Wkly. Rep. 42:258-263.
18. 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. 62:1822-1824.
19. Cody, S. H., M. K. Glynn, J. A. Farrar, K. L. Cairns, P. M. Griffin, J. Kobayashi, M. Fyfe, R. Hoffman, A. S. King, J. H. Lewis, B. Swaminathan, R. G. Bryant, and D. J. Vugia. 1999. An outbreak of Escherichia coli O157:H7 infection from unpasteurized commercial apple juice. Ann. Intern. Med. 130:202-209.
20. Connolly, L., A. De Las Penas, B. M. Alba, and C. A. Gross. 1997. The response to extracytoplasmic stress in Escherichia coli is controlled by partially overlapping pathways. Genes Dev. 11:2012-2021.
21. Csonka, L. N. 1989. Physiological and genetic responses of bacteria to osmotic stress. Microbiol. Rev. 53:121-147.
22. Cui, X., and G. A. Churchill. 2003. Statistical tests for differential expression in cDNA microarray experiments. Genome Biol. 4:210. (Pubitemid 36519482)
23. Cui, X., J. T. Hwang, J. Qiu, N. J. Blades, and G. A. Churchill. 2005. Improved statistical tests for differential gene expression by shrinking variance components estimates. Biostatistics 6:59-75. (Pubitemid 41240370)
24. Danese, P. N., and T. J. Silhavy. 1998. CpxP, a stress-combative member of the Cpx regulon. J. Bacteriol. 180:831-839. (Pubitemid 28084207)
25. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
26. De Wulf, P., O. Kwon, and E. C. Lin. 1999. The CpxRA signal transduction system of Escherichia coli: growth-related autoactivation and control of unanticipated target operons. J. Bacteriol. 181:6772-6778.
27. De Wulf, P., A. M. McGuire, X. Liu, and E. C. Lin. 2002. Genome-wide profiling of promoter recognition by the two-component response regulator CpxR-P in Escherichia coli. J. Biol. Chem. 277:26652-26661. (Pubitemid 34967164)
28. DiGiuseppe, P. A., and T. J. Silhavy. 2003. Signal detection and target gene induction by the CpxRA two-component system. J. Bacteriol. 185:2432-2440. (Pubitemid 36417966)
29. Dineen, S. S., K. Takeuchi, J. E. Soudah, and K. J. Boor. 1998. Persistence of Escherichia coli O157:H7 in dairy fermentation systems. J. Food Prot. 61:1602-1608.
30. Dziva, F., P. M. van Diemen, M. P. Stevens, A. J. Smith, and T. S. Wallis. 2004. Identification of Escherichia coli O157:H7 genes influencing colonization of the bovine gastrointestinal tract using signature-tagged mutagenesis. Microbiology 150:3631-3645.
31. Ebel, F., C. Deibel, A. U. Kresse, C. A. Guzman, and T. Chakraborty. 1996. Temperature- and medium-dependent secretion of proteins by Shiga toxin-producing Escherichia coli. Infect. Immun. 64:4472-4479. (Pubitemid 26357046)
32. Foster, J. W. 2004. Escherichia coli acid resistance: tales of an amateur acidophile. Nat. Rev. Microbiol. 2:898-907.
33. Hagiwara, D., M. Sugiura, T. Oshima, H. Mori, H. Aiba, T. Yamashino, and T. Mizuno. 2003. Genome-wide analyses revealing a signaling network of the RcsC-YojN-RcsB phosphorelay system in Escherichia coli. J. Bacteriol. 185:5735-5746. (Pubitemid 37176485)
34. Hayes, E. T., J. C. Wilks, P. Sanfilippo, E. Yohannes, D. P. Tate, B. D. Jones, M. D. Radmacher, S. S. BonDurant, and J. L. Slonczewski. 2006. Oxygen limitation modulates pH regulation of catabolism and hydrogenases, multidrug transporters, and envelope composition in Escherichia coli K-12. BMC Microbiol. 6:89.
35. Hengge-Aronis, R. 1996. Back to log phase: sigma S as a global regulator in the osmotic control of gene expression in Escherichia coli. Mol. Microbiol. 21:887-893. (Pubitemid 26297756)
36. Hilborn, E. D., J. H. Mermin, P. A. Mshar, J. L. Hadler, A. Voetsch, C. Wojtkunski, M. Swartz, R. Mshar, M. A. Lambert-Fair, J. A. Farrar, M. K. Glynn, and L. Slutsker. 1999. A multistate outbreak of Escherichia coli O157:H7 infections associated with consumption of mesclun lettuce. Arch. Intern. Med. 159:1758-1764.
37. Hilborn, E. D., P. A. Mshar, T. R. Fiorentino, Z. F. Dembek, T. J. Barrett, R. T. Howard, and M. L. Cartter. 2000. An outbreak of Escherichia coli O157:H7 infections and haemolytic uraemic syndrome associated with consumption of unpasteurized apple cider. Epidemiol. Infect. 124:31-36.
38. Iyoda, S., and H. Watanabe. 2004. Positive effects of multiple pch genes on expression of the locus of enterocyte effacement genes and adherence of enterohaemorrhagic Escherichia coli O157:H7 to HEp-2 cells. Microbiology 150:2357-2571.
39. Jenkins, D. E., S. A. Chaisson, and A. Matin. 1990. Starvation-induced cross protection against osmotic challenge in Escherichia coli. J. Bacteriol. 172:2779-2781.
40. 2 challenge in Escherichia coli. J. Bacteriol. 170:3910-3914.
41. Jordan, K. N., L. Oxford, and C. P. O'Byrne. 1999. Survival of low-pH stress by Escherichia coli O157:H7: correlation between alterations in the cell envelope and increased acid tolerance. Appl. Environ. Microbiol. 65:3048-3055.
42. Jubelin, G., A. Vianney, C. Beloin, J. M. Ghigo, J. C. Lazzaroni, P. Lejeune, and C. Dorel. 2005. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J. Bacteriol. 187:2038-2049. (Pubitemid 40316234)
43. Kannan, G., J. C. Wilks, D. M. Fitzgerald, B. D. Jones, S. S. Bondurant, and J. L. Slonczewski. 2008. Rapid acid treatment of Escherichia coli: transcriptomic response and recovery. BMC Microbiol. 8:37.
44. Kaur, J., D. A. Ledward, R. W. Park, and R. L. Robson. 1998. Factors affecting the heat resistance of Escherichia coli O157:H7. Lett. Appl. Microbiol. 26:325-330.
45. Kenny, B., A. Abe, M. Stein, and B. B. Finlay. 1997. Enteropathogenic Escherichia coli protein secretion is induced in response to conditions similar to those in the gastrointestinal tract. Infect. Immun. 65:2606-2612.
46. Kerr, M. K. 2003. Linear models for microarray data analysis: hidden similarities and differences. J. Comput. Biol. 10:891-901.
47. S- dependent genes and identification of their promoter sequences. J. Bacteriol. 186:7186-7195.
48. Lange, R., and R. Hengge-Aronis. 1991. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol. Microbiol. 5:49-59. (Pubitemid 21895940)
49. Lee, S. M., and J. Chen. 2004. Survival of Escherichia coli O157:H7 in set yogurt as influenced by the production of an exopolysaccharide, colanic acid. J. Food Prot. 67:252-255.
50. 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. 62:3094-3100.
51. Marques, P. A., D. Worcman-Barninka, S. C. Lannes, and M. Landgraf. 2001. Acid tolerance and survival of Escherichia coli O157:H7 inoculated in fruit pulps stored under refrigeration. J. Food Prot. 64:1674-1678.
52. Mattick, L. R., and J. C. Moyer. 1983. Composition of apple juice. J. Assoc. Off. Anal. Chem. 66:1251-1255.
53. Maurer, L. M., E. Yohannes, S. S. Bondurant, M. Radmacher, and J. L. Slonczewski. 2005. pH regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12. J. Bacteriol. 187:304-319.
54. 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.
55. Michino, H., K. Araki, S. Minami, S. Takaya, N. Sakai, M. Miyazaki, A. Ono, and H. Yanagawa. 1999. Massive outbreak of Escherichia coli O157:H7 infection in schoolchildren in Sakai City, Japan, associated with consumption of white radish sprouts. Am. J. Epidemiol. 150:787-796.
56. Murphy, K. C., and K. G. Campellone. 2003. Lambda Red-mediated recombinogenic engineering of enterohemorrhagic and enteropathogenic E. coli. BMC Mol. Biol. 4:11.
57. Neidhardt, F. C., P. L. Bloch, and D. F. Smith. 1974. Culture medium for enterobacteria. J. Bacteriol. 119:736-747.
58. Nonaka, G., M. Blankschien, C. Herman, C. A. Gross, and V. A. Rhodius. 2006. Regulon and promoter analysis of the E. coli heat-shock factor, sigma32, reveals a multifaceted cellular response to heat stress. Genes Dev. 20:1776-1789.
59. Patten, C. L., M. G. Kirchhof, M. R. Schertzberg, R. A. Morton, and H. E. Schellhorn. 2004. Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol. Genet. Genomics 272:580-591.
60. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
61. Price, S. B., J. C. Wright, F. J. DeGraves, M. P. Castanie-Cornet, and J. W. Foster. 2004. Acid resistance systems required for survival of Escherichia coli O157:H7 in the bovine gastrointestinal tract and in apple cider are different. Appl. Environ. Microbiol. 70:4792-4799.
62. Rangel, J. M., P. H. Sparling, C. Crowe, P. M. Griffin, and D. L. Swerdlow. 2005. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002. Emerg. Infect. Dis. 11:603-609.
63. R Core Development Team. 2005. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
64. Reinders, R. D., S. Biesterveld, and P. G. Bijker. 2001. Survival of Escherichia coli O157:H7 ATCC 43895 in a model apple juice medium with different concentrations of proline and caffeic acid. Appl. Environ. Microbiol. 67:2863-2866.
65. Reitzer, L. 2003. Nitrogen assimilation and global regulation in Escherichia coli. Annu. Rev. Microbiol. 57:155-176.
66. 54-dependent genes in Escherichia coli. Microbiol. Mol. Biol. Rev. 65:422-444.
67. Ren, D., L. A. Bedzyk, S. M. Thomas, R. W. Ye, and T. K. Wood. 2004. Gene expression in Escherichia coli biofilms. Appl. Microbiol. Biotechnol. 64:515-524.
68. Rhodius, V. A., W. C. Suh, G. Nonaka, J. West, and C. A. Gross. 2006. Conserved and variable functions of the sigmaE stress response in related genomes. PLoS Biol. 4:e2.
69. 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. 186:6032-6041.
70. Riley, L. W., R. S. Remis, S. D. Helgerson, H. B. McGee, J. G. Wells, B. R. Davis, R. J. Hebert, E. S. Olcott, L. M. Johnson, N. T. Hargrett, P. A. Blake, and M. L. Cohen. 1983. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N. Engl. J. Med. 308:681-685.
71. 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. 67:4901-4907.
72. Ruiz, N., and T. J. Silhavy. 2005. Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr. Opin. Microbiol. 8:122-126.
73. Seputiene, V., D. Motiejunas, K. Suziedelis, H. Tomenius, S. Normark, O. Melefors, and E. Suziedeliene. 2003. Molecular characterization of the acid-inducible asr gene of Escherichia coli and its role in acid stress response. J. Bacteriol. 185:2475-2484.
74. Seputiene, V., K. Suziedelis, S. Normark, O. Melefors, and E. Suziedeliene. 2004. Transcriptional analysis of the acid-inducible asr gene in enterobacteria. Res. Microbiol. 155:535-542.
75. Shin, S., M. P. Castanie-Cornet, J. W. Foster, J. A. Crawford, C. Brinkley, and J. B. Kaper. 2001. An activator of glutamate decarboxylase genes regulates the expression of enteropathogenic Escherichia coli virulence genes through control of the plasmid-encoded regulator, Per. Mol. Microbiol. 41:1133-1150.
76. Sledjeski, D. D., and S. Gottesman. 1996. Osmotic shock induction of capsule synthesis in Escherichia coli K-12. J. Bacteriol. 178:1204-1206.
77. Snyder, J. D. 1982. From pedialyte to popsicles: a look at oral rehydration therapy used in the United States and Canada. Am. J. Clin. Nutr. 35:157-161.
78. Stancik, L. M., D. M. Stancik, B. Schmidt, D. M. Barnhart, Y. N. Yoncheva, and J. L. Slonczewski. 2002. pH-dependent expression of periplasmic proteins and amino acid catabolism in Escherichia coli. J. Bacteriol. 184:4246-4258. (Pubitemid 34774306)
79. 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 142:1311-1320. (Pubitemid 26154942)
80. Subramanian, A., P. Tamayo, V. K. Mootha, S. Mukherjee, B. L. Ebert, M. A. Gillette, A. Paulovich, S. L. Pomeroy, T. R. Golub, E. S. Lander, and J. P. Mesirov. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102:15545-15550.
81. Tobe, T., H. Ando, H. Ishikawa, H. Abe, K. Tashiro, T. Hayashi, S. Kuhara, and N. Sugimoto. 2005. Dual regulatory pathways integrating the RcsCRcsD-RcsB signalling system control enterohaemorrhagic Escherichia coli pathogenicity. Mol. Microbiol. 58:320-333.
82. Tobe, T., S. A. Beatson, H. Taniguchi, H. Abe, C. M. Bailey, A. Fivian, R. Younis, S. Matthews, O. Marches, G. Frankel, T. Hayashi, and M. J. Pallen. 2006. An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination. Proc. Natl. Acad. Sci. USA 103:14941-14946.
83. Tucker, D. L., N. Tucker, and T. Conway. 2002. Gene expression profiling of the pH response in Escherichia coli. J. Bacteriol. 184:6551-6558.
84. Verheul, A., J. A. Wouters, F. M. Rombouts, and T. Abee. 1998. A possible role of ProP, ProU and CaiT in osmoprotection of Escherichia coli by carnitine. J. Appl. Microbiol. 85:1036-1046.
85. Weagant, S. D., J. L. Bryant, and D. H. Bark. 1994. Survival of Escherichia coli O157:H7 in mayonnaise and mayonnaise-based sauces at room and refrigerated temperatures. J. Food Prot. 57:629-631.
86. Weber, A., and K. Jung. 2002. Profiling early osmostress-dependent gene expression in Escherichia coli using DNA macroarrays. J. Bacteriol. 184:5502-5507.
87. Weber, A., S. A. Kogl, and K. Jung. 2006. Time-dependent proteome alterations under osmotic stress during aerobic and anaerobic growth in Escherichia coli. J. Bacteriol. 188:7165-7175. (Pubitemid 44547621)
88. S-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187:1591-1603.
89. Wick, L. M., and T. Egli. 2004. Molecular components of physiological stress responses in Escherichia coli. Adv. Biochem. Eng. Biotechnol. 89:1-45.
90. Yuk, H. G., and D. L. Marshall. 2004. Adaptation of Escherichia coli O157:H7 to pH alters membrane lipid composition, verotoxin secretion, and resistance to simulated gastric fluid acids. Appl. Environ. Microbiol. 70:3500-3505.
91. Zhang, X. S., R. Garcia-Contreras, and T. K. Wood. 2007. YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. J. Bacteriol. 189:3051-3062.
92. Zhao, T., and M. P. Doyle. 1994. Fate of enterohemorrhagic Escherichia coli O157:H7 in commercial mayonnaise. J. Food Prot. 57:780-783.
93. 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. 183:4562-4570.
94. Zimmer, D. P., E. Soupene, H. L. Lee, V. F. Wendisch, A. B. Khodursky, B. J. Peter, R. A. Bender, and S. Kustu. 2000. Nitrogen regulatory protein C-controlled genes of Escherichia coli: scavenging as a defense against nitrogen limitation. Proc. Natl. Acad. Sci. USA 97:14674-14679.