Transcriptomic analysis of Escherichia coli O157:H7 and K-12 cultures exposed to inorganic and organic acids in stationary phase reveals acidulant- and strain-specific acid tolerance responses

Applied and Environmental Microbiology

Volumn 76, Issue 19, 2010, Pages 6514-6528

  King, Thea ^a   Lucchini, Sacha ^b   Hinton, Jay C D ^b,c   Gobius, Kari ^a  

^a CSIRO   (Australia)

^b INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^c TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ACID TOLERANCE RESPONSE; ACIDIC ENVIRONMENT; COLD STRESS; E. COLI; E.COLI O157:H7; ENERGY PRODUCTIONS; ESCHERICHIA COLI O157:H7; FOOD-BORNE PATHOGENS; HEAT SHOCK RESPONSE; INTERGENIC REGIONS; IRON AND MANGANESE; MICROBIAL INACTIVATION; MOLECULAR BASIS; MOLECULAR MECHANISM; PH LEVELS; PH-DEPENDENT; STATIONARY PHASE; WEAK ORGANIC ACIDS;

ACETIC ACID; ESCHERICHIA COLI; FOOD PROCESSING; GENES; HYDROCHLORIC ACID; MANGANESE; METAL ANALYSIS; ORGANIC ACIDS; STRAIN;

ACID RESISTANCE;

ACID; CARBOXYLIC ACID; ESCHERICHIA COLI PROTEIN;

ADAPTATION; COLD TOLERANCE; COLIFORM BACTERIUM; FOOD PROCESSING; HYDROCHLORIC ACID; METABOLISM; NUTRIENT UPTAKE; ORGANIC ACID; OSMOREGULATION; PATHOGEN; PH; TOLERANCE;

ARTICLE; BIOSYNTHESIS; COMPARATIVE STUDY; DRUG EFFECT; ESCHERICHIA COLI K 12; ESCHERICHIA COLI O157; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ACIDS; CARBOXYLIC ACIDS; ESCHERICHIA COLI K12; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; STRESS, PHYSIOLOGICAL;

ESCHERICHIA COLI; ESCHERICHIA COLI K12;

EID: 78049290979     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02392-09     Document Type: Article

References (86)

1. Altuvia, S. 2004. Regulatory small RNAs: the key to coordinating global regulatory circuits. J. Bacteriol. 186:6679-6680.
2. Antal, M., V. Bordeau, V. Douchin, and B. Felden. 2005. A small bacterial RNA regulates a putative ABC transporter. J. Biol. Chem. 280:7901-7908.
3. Antón, J., A. Oren, S. Benlloch, F. Rodríguez-Valera, R. Amann, and R. Rosselló-Mora. 2002. Salinibacter ruber gen. nov., sp. nov., a novel, extremely halophilic member of the Bacteria from saltern crystallizer ponds. Int. J. Syst. Evol. Microbiol. 52:485-491.
4. Argaman, L., R. Hershberg, J. Vogel, G. Bejerano, E. G. H. Wagner, H. Margalit, and S. Altuvia. 2001. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr. Biol. 11:941-950.
5. 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.
6. Arnold, K. W., and C. W. Kaspar. 1995. Starvation-and stationary-phaseinduced acid tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 61:2037-2039.
7. Benjamin, M. M., and A. R. Datta. 1995. Acid tolerance of enterohemorrhagic Escherichia coli. Appl. Environ. Microbiol. 61:1669-1672.
8. Berry, E. D., G. A. Barkocy-Gallagher, and G. R. Siragusa. 2004. Stationary phase acid resistance and injury of recent bovine Escherichia coli O157 and non-O157 biotype I Escherichia coli isolates. J. Food Prot. 67:583-590.
9. Berry, E. D., and C. N. Cutter. 2000. Effects of acid adaptation of Escherichia coli O157:H7 on efficacy of acetic acid spray washes to decontaminate beef carcass tissue. Appl. Environ. Microbiol. 66:1493-1498.
10. 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.
11. Blattner, F. R., G. Plunkett III, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, J. Collado-Vides, J. D. Glasner, C. K. Rode, G. F. Mayhew, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden, D. J. Rose, B. Mau, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1462. (Pubitemid 27449228)
12. Buchanan, R. L., and S. G. Edelson. 1996. Culturing enterohemorrhagic Escherichia coli in the presence and absence of glucose as a simple means of evaluating the acid tolerance of stationary-phase cells. Appl. Environ. Microbiol. 62:4009-4013.
13. Buchanan, R. L., and S. G. Edelson. 1999. pH-dependent stationary-phase acid resistance response of enterohemorrhagic Escherichia coli in the presence of various acidulants. J. Food Prot. 62:211-218.
14. Buchanan, R. L., S. G. Edelson, and G. Boyd. 1999. Effects of pH and acid resistance on the radiation resistance of enterohemorrhagic Escherichia coli. J. Food Prot. 62:219-228.
15. Cameron, S., C. Walker, and M. Beers. 1995. Enterohemorrhagic Escherichia coli outbreak in South Australia associated with the consumption of Mettwurst. Commun. Dis. Intell. 19:70-71.
16. Carruthers, M. D., and C. Minion. 2009. Transcriptome analysis of Escherichia coli O157:H7 EDL933 during heat shock. FEMS Microbiol. Lett. 295:96-102.
17. 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. 181:3525-3535.
18. Cheng, L., J. Moghraby, and P. W. Piper. 1999. Weak organic acid treatment causes a trehalose accumulation in low-pH cultures of Saccharomyces cerevisiae, not displayed by the more preservative-resistant Zygosaccharomyces bailii. FEMS Microbiol. Lett. 170:89-95.
19. Crépin, S., M. G. Lamarche, P. Garneau, J. Séguin, J. Proulx, C. M. Dozois, and J. Harel. 2008. Genome-wide transcriptional response of an avian pathogenic Escherichia coli (APEC) pst mutant. BMC Genomics 9:568.
20. Dartigalongue, C., D. Missiakas, and S. Raina. 2001. Characterization of the Escherichia coli sigma E regulon. J. Biol. Chem. 276:20866-20875.
21. David, G., K. Blondeau, M. Schiltz, S. Penel, and A. Lewit-Bentley. 2003. YodA from Escherichia coli is a metal-binding, lipocalin-like protein. J. Biol. Chem. 278:43728-43735.
22. Duffy, L. L., F. H. Grau, and P. B. Vanderlinde. 2000. Acid resistance of enterohaemorrhagic and generic Escherichia coli associated with foodborne disease and meat. Int. J. Food Microbiol. 60:83-89.
23. Echave, P., J. Tamarit, E. Cabiscol, and J. Ros. 2003. Novel antioxidant role of alcohol dehydrogenase E from Escherichia coli. J. Biol. Chem. 278:30193-30198.
24. Faith, J. J., B. Hayete, J. T. Thaden, I. Mogno, J. Wierzbowski, G. Cottarel, S. Kasif, J. J. Collins, and T. S. Gardner. 2007. Large-scale mapping and validation of Escherichia coli transcriptional regulation from a compendium of expression profiles. PLoS. Biol. 5:e8.
25. Foster, J. W. 2004. Escherichia coli acid resistance: tales of an amateur acidophile. Nat. Rev. Microbiol. 2:898-907.
26. Foster, J. W. 2000. Microbial responses to acid stress, p. 99-115. In G. Storz and R. Hengge-Aronis (ed.), Bacterial stress responses. ASM Press, Washington, DC.
27. Foster, J. W., and B. Bearson. 1994. Acid-sensitive mutants of Salmonella typhimurium identified through a dinitrophenol lethal screening strategy. J. Bacteriol. 176:2596-2602.
28. Garren, D. M., M. A. Harrison, and S. M. Russell. 1998. Acid tolerance and acid shock response of Escherichia coli O157:H7 and non-O157:H7 isolates provide cross protection to sodium lactate and sodium chloride. J. Food Prot. 61:158-161.
29. Gentleman, R., V. Carey, D. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, J. Gentry, K. Hornik, T. Hothorn, W. Huber, S. Iacus, R. Irizarry, F. Leisch, C. Li, M. Maechler, A. Rossini, G. Sawitzki, C. Smith, G. Smyth, L. Tierney, J. Yang, and J. Zhang. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80.
30. Gerdes, K., S. K. Christensen, and A. Lobner-Olesen. 2005. Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3:371-382.
31. Goodson, M., and R. J. Rowbury. 1989. Habituation to normally lethal acidity by prior growth of Escherichia coli at a sub-lethal acid pH value. Lett. Appl. Microbiol. 8:77-79.
32. 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 20c°C: optimization and modeling. Appl. Environ. Microbiol. 69:3945-3951.
33. Hankins, J. S., C. Zappavigna, A. Prud'homme-Genereux, and G. A. Mackie. 2007. Role of RNA structure and susceptibility to RNase E in regulation of a cold shock mRNA, cspA mRNA. J. Bacteriol. 189:4353-4358.
34. Hantke, K. 2005. Bacterial zinc uptake and regulators. Curr. Opin. Microbiol. 8:196-202.
35. Hayashi, T., K. Makino, M. Ohnishi, K. Kurokawa, K. Ishii, K. Yokoyama, C.-G. Han, E. Ohtsubo, K. Nakayama, T. Murata, M. Tanaka, T. Tobe, T. Iida, H. Takami, T. Honda, C. Sasakawa, N. Ogasawara, T. Yasunaga, S. Kuhara, T. Shiba, M. Hattori, and H. Shinagawa. 2001. Complete genome sequence of enterohemorrhagic Eschelichia coli O157:H7 and genomic comparison with a laboratory strain, K-12. DNA Res. 8:11-22.
36. 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.
37. Hengge-Aronis, R. 1996. Regulation of gene expression during entry into stationary phase, p. 1458-1496. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella:cellular and molecular biology. ASM Press, Washington, DC.
38. Hengge-Aronis, R. 2002. Signal transduction and regulatory mechanisms involved in control of the αS (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 66:373-395.
39. Hengge-Aronis, R., W. Klein, R. Lange, M. Rimmele, and W. Boos. 1991. Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli. J. Bacteriol. 173:7918-7924.
40. Hershberg, R., S. Altuvia, and H. Margalit. 2003. A survey of small RNAencoding genes in Escherichia coli. Nucleic Acids Res. 31:1813-1820.
41. Hinton, J. C. D. 1997. The Escherichia coli genome sequence: the end of an era or the start of the FUN? Mol. Microbiol. 26:417-422.
42. Huang, H.-Y., H.-Y. Chang, C.-H. Chou, C.-P. Tseng, S.-Y. Ho, C.-D. Yang, Y.-W. Ju, and H.-D. Huang. 2009. sRNAMap: genomic maps for small non-coding RNAs, their regulators and their targets in microbial genomes. Nucleic Acids Res. 37:D150-D154.
43. Huang, Y.-J., T.-Y. Tsai, and T.-M. Pan. 2007. Physiological response and protein expression under acid stress of Escherichia coli O157:H7 TWC01 isolated from Taiwan. J. Agric. Food Chem. 55:7182-7191.
44. Hughes, T. R., C. J. Roberts, H. Dai, A. R. Jones, M. R. Meyer, D. Slade, J. Burchard, S. Dow, T. R. Ward, M. J. Kidd, S. H. Friend, and M. J. Marton. 2000. Widespread aneuploidy revealed by DNA microarray expression profiling. Nat. Genet. 25:333-337.
45. Ichikawa, J. K., A. Norris, M. G. Bangera, G. K. Geiss, A. B. van 't Wout, R. E. Bumgarner, and S. Lory. 2000. Interaction of Pseudomonas aeruginosa with epithelial cells: identification of differentially regulated genes by expression microarray analysis of human cDNAs. Proc. Natl. Acad. Sci. U. S. A. 97:9659-9664.
46. Imlay, J. A. 2003. Pathways of oxidative damage. Annu. Rev. Microbiol. 57:395-418.
47. Irizarry, R. A., L. Gautier, and L. M. Cope. 2003. An R package for analyses of Affymetrix oligonucleotide arrays, p. 102-119. In G. Parmigiani, E. S. Garrett, R. A. Irizarry, and S. L. Zeger (ed.), The analysis of gene expression data: methods and software. Springer-Verlag London, London, United Kingdom.
48. Irizarry, R. A., B. Hobbs, F. Collin, Y. D. Beazer-Barclay, K. J. Antonellis, U. Scherf, and T. P. Speed. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249-264.
49. Jiang, W., Y. Hou, and M. Inouye. 1997. CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J. Biol. Chem. 272:196-202.
50. Jones, P. G., M. Mitta, Y. Kim, W. Jiang, and M. Inouye. 1996. Cold shock induces a major ribosome-associated protein that unwinds double-stranded RNA in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 93:76-80.
51. 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.
52. 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.
53. Kershaw, C. J., N. L. Brown, C. Constantinidou, M. D. Patel, and J. L. Hobman. 2005. The expression profile of Escherichia coli K-12 in response to minimal, optimal and excess copper concentrations. Microbiology 151:1187-1198.
54. Kirkpatrick, C., L. M. Maurer, N. E. Oyelakin, Y. N. Yoncheva, R. Maurer, and J. L. Slonczewski. 2001. Acetate and formate stress: opposite responses in the proteome of Escherichia coli. J. Bacteriol. 183:6466-6477.
55. Kobayashi, A., H. Hirakawa, T. Hirata, K. Nishino, and A. Yamaguchi. 2006. Growth phase-dependent expression of drug exporters in Escherichia coli and its contribution to drug tolerance. J. Bacteriol. 188:5693-5703.
56. Lambert, L. A., K. Abshire, D. Blankenhorn, and J. L. Slonczewski. 1997. Proteins induced in Escherichia coli by benzoic acid. J. Bacteriol. 179:7595-7599.
57. Lewinson, O., E. Padan, and E. Bibi. 2004. Alkalitolerance: a biological function for a multidrug transporter in pH homeostasis. Proc. Natl. Acad. Sci. U. S. A. 101:14073-14078.
58. Leyer, G. J., L. L. Wang, and E. A. Johnson. 1995. Acid adaptation of Escherichia coli O157:H7 increases survival in acidic foods. Appl. Environ. Microbiol. 61:3752-3755.
59. 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. 177:4097-4104.
60. Masse, E., N. Majdalani, and S. Gottesman. 2001. Regulatory roles for small RNAs in bacteria. Curr. Opin. Microbiol. 6:120-124.
61. 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.
62. Morgan, D., C. P. Newman, D. N. Hutchinson, A. M. Walker, B. Rowe, and F. Majid. 1993. Verotoxin producing Escherichia coli O157 infections associated with consumption of yogurt. Epidemiol. Infect. 111:181-187.
63. Nishino, K., and A. Yamaguchi. 2001. Analysis of a complete library of putative drug transporter genes in Escherichia coli. J. Bacteriol. 183:5803-5812.
64. 32, reveals a multifaceted cellular response to heat stress. Genes Dev. 20:1776-1789.
65. Ogasawara, H., Y. Ishida, K. Yamada, K. Yamamoto, and A. Ishihama. 2007. PdhR (pyruvate dehydrogenase complex regulator) controls the respiratory electron transport system in Escherichia coli. J. Bacteriol. 189:5534-5541.
66. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
67. Piddock, L. J. V. 2006. Multidrug-resistance efflux pumps-not just for resistance. Nat. Rev. Microbiol. 4:629-636.
68. Piper, P., C. Ortiz Calderon, K. Hatzixanthis, and M. Mollapour. 2001. Weak acid adaptation: the stress response that confers yeasts with resistance to organic acid food preservatives. Microbiology 147:2635-2642. (Pubitemid 32976304)
69. 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. 66:632-637.
70. 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. 28:263-275.
71. Rezuchova, B., H. Miticka, D. Homerova, M. Roberts, and J. Kormanec. 2003. New members of the Escherichia coli αE regulon identified by a twoplasmid system. FEMS Microbiol. Lett. 225:1-7.
72. Russell, J. B. 1992. Another explanation for the toxicity of fermentation acids at low pH: anion accumulation versus uncoupling. J. Appl. Microbiol. 73:363-370.
73. Šeputiene•, V., K. Sužiedelie•ne• and E.Sužiedelie•ne• 2004. Gene expression profiling of the low-pH response in Escherichia coli. Biologija 3:6-12.
74. Shah, D., Z. Zhang, A. Khodursky, N. Kaldalu, K. Kurg, and K. Lewis. 2006 Persisters: a distinct physiological state of E. coli. BMC Microbiol. 6:53.
75. Slonczewski, J. L., and J. W. Foster. 1996. pH-related genes and survival at extreme pH, p. 1539-1552. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella:cellular and molecular biology, 2nd ed. ASM Press, Washington, DC.
76. Smyth, G. K. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3:Article3.
77. 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.
78. Tsilibaris, V., G. Maenhaut-Michel, N. Mine, and L. Van Melderen. 2007. What is the benefit to Escherichia coli of having multiple toxin-antitoxin systems in its genome? J. Bacteriol. 189:6101-6108.
79. Tucker, D. L., N. Tucker, and T. Conway. 2002. Gene expression profiling of the pH response in Escherichia coli. J. Bacteriol. 184:6551-6558.
80. Vorachek-Warren, M. K., S. Ramirez, R. J. Cotter, and C. R. H. Raetz. 2002. A triple mutant of Escherichia coli lacking secondary acyl chains on lipid A. J. Biol. Chem. 277:14194-14205.
81. Wang, S., K. Deng, S. Zaremba, X. Deng, C. Lin, Q. Wang, M. L. Tortorello, and W. Zhang. 2009. Transcriptomic response of Escherichia coli O157:H7 to oxidative stress. Appl. Environ. Microbiol. 75:6110-6123.
82. Weagant, S. D., J. L. Bryant, and D. H. Bark. 1994. Survival of Escherichia coli O157:H7 in mayonnaise-based sauces at room and refrigerated temperatures. J. Food Prot. 57:629-631.
83. Weber, H., T. Polen, J. Heuveling, V. F. Wendisch, and R. Hengge. 2005. Genome-wide analysis of the general stress response network in Escherichia coli: αS-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187:1591-1603.
84. Weerasinghe, J. P., T. Dong, M. R. Schertzberg, M. G. Kirchhof, Y. Sun, and H. E. Schellhorn. 2006. Stationary phase expression of the arginine biosynthetic operon argCBH in Escherichia coli. BMC Microbiol. 6:1471-2180.
85. Wolfe, A. J. 2005. The acetate switch. Microbiol. Mol. Biol. Rev. 69:12-50.
86. Zhang, G., S. Brokx, and J. H. Weiner. 2005. Extracellular accumulation of recombinant proteins fused to the carrier protein YebF in Escherichia coli. Nat. Biotechnol. 24:100-104.