Integrated transcriptomic and proteomic analysis of the physiological response of Escherichia coli O157:H7 Sakai to steady-state conditions of cold and water activity stress

Molecular and Cellular Proteomics

Volumn 11, Issue 1, 2012, Pages

  Kocharunchitt, Chawalit ^a   King, Thea ^b   Gobius, Kari ^b   Bowman, John P ^a   Ross, Tom ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

^b CSIRO   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

EXOPOLYSACCHARIDE; MESSENGER RNA; WATER;

ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; BIOSYNTHESIS; CELL MOTILITY; CHEMOTAXIS; COLD AIR; COLD STRESS; CONTROLLED STUDY; DOWN REGULATION; ESCHERICHIA COLI; GENE EXPRESSION; GROWTH RATE; LOW TEMPERATURE; MUTANT; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; PROTEOMICS; STEADY STATE; TRANSCRIPTOMICS; WILD TYPE;

ESCHERICHIA COLI;

EID: 84856076140     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M111.009019     Document Type: Article

References (88)

1. Riley, L. W., Remis, R. S., Helgerson, S. D., McGee, H. B., Wells, J. G., Davis, B. R., Hebert, R. J., Olcott, E. S., Johnson, L. M., Hargrett, N. T., Blake, P. A., and Cohen, M. L. (1983) Hemorrhagic colitis associated with a rare Escherichia coli serotype. N. Engl. J. Med. 308, 681-685 (Pubitemid 13157770)
2. Cagney, C., Crowley, H., Duffy, G., Sheridan, J. J., Brien, S. O., Carney, E., Anderson, W., McDowell, D. A., Blair, I. S., and Bishop, R. H. (2004) Prevalence and numbers of Escherichia coli O157:H7 in minced beef and beef burgers from butcher shops and supermarkets in the Republic of Ireland. Food Microbiol. 21, 203-212 (Pubitemid 38272205)
3. Hussein, H. S., and Bollinger, L. M. (2005) Prevalence of Shiga toxin-producing Escherichia coli in beef. Meat Sci. 71, 676-689 (Pubitemid 41328606)
4. McClure, P. (2000) The impact of E. coli O157 on the food industry. World J. Microbiol. Biotechnol. 16, 749-755
5. Elder, R. O., Keen, J. E., Siragusa, G. R., Barkocy-Gallagher, G. A., Koohmaraie, M., and Laegreid, W. W. (2000) Correlation of enterohemorrhagic Escherichia coli O157 prevalence in feces, hides, and carcasses of beef cattle during processing. Proc. Natl. Acad. Sci. U.S.A. 97, 2999-3003 (Pubitemid 30183244)
6. Gill, C. O., and Bryant, J. (1997) Assessment of the hygienic performances of two beef carcass cooling processes from product temperature history data or enumeration of bacteria on carcass surfaces. Food Microbiol. 14, 593-602 (Pubitemid 28017203)
7. Lenahan, M., Crowley, H., O'Brien, S. B., Byrne, C., Sweeney, T., and Sheridan, J. J. (2009) The potential use of chilling to control the growth of Enterobacteriaceae on porcine carcasses and the incidence of E. coli O157:H7 in pigs. J. Appl. Microbiol. 106, 1512-1520
8. Aertsen, A., and Michiels, C. W. (2004) Stress and how bacteria cope with death and survival. Crit. Rev. Microbiol. 30, 263-273 (Pubitemid 39557583)
9. Chung, H. J., Bang, W., and Drake, M. A. (2006) Stress response of Escherichia coli. Compr. Rev. Food Sci. Food Saf. 5, 52-64 (Pubitemid 44668740)
10. Ingraham, J. L., and Marr, A. G. (1996) Effect of temperature, pressure, pH, and osmotic stress on growth. In: Neidhardt, F. C., CurtissIII, R., Ingraham, J. L., Lin, E. C. C., Low, K. B., Magasanik, B., Reznikoff, W. S., Riley, M., Schaechter, M., and Umbarger, H. E., eds. Escherichia coli and Salmonella: cellular and molecular biology, pp. 1570-1578, American Society for Microbiology, Washington, D.C.
11. Cao-Hoang, L., Dumont, F., Marechal, P. A., Le-Thanh, M., and Gervais, P. (2008) Rates of chilling to 0°C: implications for the survival of microorganisms and relationship with membrane fluidity modifications. Appl. Microbiol. Biotechnol. 77, 1379-1387
12. Yamanaka, K. (1999) Cold shock response in Escherichia coli. J. Mol. Microbiol. Biotechnol. 1, 193-202
13. O'Byrne, C. P., and Booth, I. R. (2002) Osmoregulation and its importance to foodborne microorganisms. Int. J. Food Microbiol. 74, 203-216 (Pubitemid 34203695)
14. Hayashi, T., Makino, K., Ohnishi, M., Kurokawa, K., Ishii, K., Yokoyama, K., Han, C. G., Ohtsubo, E., Nakayama, K., Murata, T., Tanaka, M., Tobe, T., Iida, T., Takami, H., Honda, T., Sasakawa, C., Ogasawara, N., Yasunaga, T., Kuhara, S., Shiba, T., Hattori, M., and Shinagawa, H. (2001) Complete Genome Sequence of enterohemorrphagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res. 8, 11-22 (Pubitemid 33617542)
15. Watanabe, H., Wada, A., Inagaki, Y., Itoh, K., and Tamura, K. (1996) Outbreaks of enterohaemorrhagic Escherichia coli O157:H7 infection by two different genotype strains in Japan. Lancet 348, 831-832 (Pubitemid 26308502)
16. Datsenko, K. A., and Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97, 6640-6645 (Pubitemid 30412767)
17. Chirife, J., and Resnik, S. L. (1984) Unsaturated solutions of sodium chloride as reference sources of water activity at various temperatures. J. Food Sci. 49, 1486-1488
18. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., and Speed, T. P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264
19. Delahunty, C., and Yates, J. R., 3rd (2005) Protein identification using 2D-LC-MS/MS. Methods 35, 248-255 (Pubitemid 40255590)
20. Rauch, A., Bellew, M., Eng, J., Fitzgibbon, M., Holzman, T., Hussey, P., Igra, M., Maclean, B., Lin, C. W., Detter, A., Fang, R., Faca, V., Gafken, P., Zhang, H., Whiteaker, J., States, D., Hanash, S., Paulovich, A., and McIntosh, M. W. (2006) Computational proteomics analysis system (CPAS): an extensible, open-source analytic system for evaluating and publishing proteomic data and high throughput biological experiments. J. Proteome Res. 5, 112-121 (Pubitemid 43100802)
21. Craig, R., and Beavis, R. C. (2004) TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20, 1466-1467 (Pubitemid 38931421)
22. Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658 (Pubitemid 37082259)
23. Keller, A., Nesvizhskii, A. I., Kolker, E., and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392 (Pubitemid 35215372)
24. Choi, H., and Nesvizhskii, A. I. (2008) False discovery rates and related statistical concepts in mass spectrometry-based proteomics. J. Proteome Res. 7, 47-50 (Pubitemid 351171114)
25. Liu, H., Sadygov, R. G., and Yates, J. R. 3rd (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 76, 4193-4201 (Pubitemid 38943698)
26. Old, W. M., Meyer-Arendt, K., Aveline-Wolf, L., Pierce, K. G., Mendoza, A., Sevinsky, J. R., Resing, K. A., and Ahn, N. G. (2005) Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol. Cell Proteomics 4, 1487-1502 (Pubitemid 41555475)
27. Fu, X., Gharib, S. A., Green, P. S., Aitken, M. L., Frazer, D. A., Park, D. R., Vaisar, T., and Heinecke, J. W. (2008) Spectral index for assessment of differential protein expression in shotgun proteomics. J. Proteome Res. 7, 845-854
28. Boorsma, A., Foat, B. C., Vis, D., Klis, F., and Bussemaker, H. J. (2005) T-profiler: scoring the activity of predefined groups of genes using gene expression data. Nucleic Acids Res. 33, W592-W595 (Pubitemid 44529991)
29. Price, N. L., and Raivio, T. L. (2009) Characterization of the Cpx regulon in Escherichia coli strain MC4100. J. Bacteriol. 191, 1798-1815
30. E stress response in related genomes. PLoS Biol. 4, e2
31. 32, reveals a multifaceted cellular response to heat stress. Genes Dev. 20, 1776-1789
32. Patten, C. L., Kirchhof, M. G., Schertzberg, M. R., Morton, R. A., and Schellhorn, H. E. (2004) Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol. Genet. Genomics 272, 580-591 (Pubitemid 40193078)
33. S-dependent genes and identification of their promoter sequences. J. Bacteriol. 186, 7186-7195
34. S-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187, 1591-1603
35. Hagiwara, D., Sugiura, M., Oshima, T., Mori, H., Aiba, H., Yamashino, T., and Mizuno, T. (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)
36. de Hoon, M. J., Imoto, S., Nolan, J., and Miyano, S. (2004) Open source clustering software. Bioinformatics 20, 1453-1454 (Pubitemid 38931415)
37. Saldanha, A. J. (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics 20, 3246-3248
38. Bergmaier, D., Lacroix, C., Guadalupe Macedo, M., and Champagne, C. P. (2001) New method for exopolysaccharide determination in culture broth using stirred ultrafiltration cells. Appl. Microbiol. Biotechnol. 57, 401-406 (Pubitemid 32972353)
39. Obadia, B., Lacour, S., Doublet, P., Baubichon-Cortay, H., Cozzone, A. J., and Grangeasse, C. (2007) Influence of tyrosine-kinase Wzc activity on colanic acid production in Escherichia coli K12 Cells. J. Mol. Biol. 367, 42-53 (Pubitemid 46274714)
40. Dische, Z., and Shettles, L. B. (1951) A new spectrophotometric test for the detection of methylpentose. J. Biol. Chem. 192, 579-582
41. Vizcaino, J. A., Cote, R., Reisinger, F., Barsnes, H., Foster, J. M., Rameseder, J., Hermjakob, H., and Martens, L. (2010) The proteomics identifications database: 2010 update. Nucleic Acids Res. 38(Database issue), D736-D742
42. Ross, T., Ratkowsky, D. A., Mellefont, L. A., and McMeekin, T. A. (2003) Modelling the effects of temperature, water activity, pH and lactic acid concentration on the growth rate of Escherichia coli. Int. J. Food Microbiol. 82, 33-43 (Pubitemid 36043925)
43. Gyaneshwar, P., Paliy, O., McAuliffe, J., Jones, A., Jordan, M. I., and Kustu, S. (2005) Lessons from Escherichia coli genes similarly regulated in response to nitrogen and sulfur limitation. Proc. Natl. Acad. Sci. U.S.A. 102, 3453-3458 (Pubitemid 40328066)
44. Klumpp, S., Zhang, Z., and Hwa, T. (2009) Growth rate-dependent global effects on gene expression in bacteria. Cell 139, 1366-1375
45. Elias, J. E., Haas, W., Faherty, B. K., and Gygi, S. P. (2005) Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations. Nat. Methods 2, 667-675 (Pubitemid 41223093)
46. Chen, G., Gharib, T. G., Huang, C. C., Taylor, J. M., Misek, D. E., Kardia, S. L., Giordano, T. J., Iannettoni, M. D., Orringer, M. B., Hanash, S. M., and Beer, D. G. (2002) Discordant protein and mRNA expression in lung adenocarcinomas. Mol. Cell Proteomics 1, 304-313
47. Griffin, T. J., Gygi, S. P., Ideker, T., Rist, B., Eng, J., Hood, L., and Aebersold, R. (2002) Complementary profiling of gene expression at the transcriptome and proteome levels in Saccharomyces cerevisiae. Mol. Cell Proteomics 1, 323-333
48. Ideker, T., Thorsson, V., Ranish, J. A., Christmas, R., Buhler, J., Eng, J. K., Bumgarner, R., Goodlett, D. R., Aebersold, R., and Hood, L. (2001) Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 292, 929-934 (Pubitemid 32422490)
49. Tian, Q., Stepaniants, S. B., Mao, M., Weng, L., Feetham, M. C., Doyle, M. J., Yi, E. C., Dai, H., Thorsson, V., Eng, J., Goodlett, D., Berger, J. P., Gunter, B., Linseley, P. S., Stoughton, R. B., Aebersold, R., Collins, S. J., Hanlon, W. A., and Hood, L. E. (2004) Integrated genomic and proteomic analyses of gene expression in mammalian cells. Mol. Cell Proteomics 3, 960-969 (Pubitemid 40361231)
50. Hatzimanikatis, V., Choe, L. H., and Lee, K. H. (1999) Proteomics: theoretical and experimental considerations. Biotechnol. Prog. 15, 312-318 (Pubitemid 29270675)
51. Hatzimanikatis, V., and Lee, K. H. (1999) Dynamical analysis of gene networks requires both mRNA and protein expression information. Metab. Eng. 1, 275-281 (Pubitemid 129499385)
52. Gygi, S. P., Rochon, Y., Franza, B. R., and Aebersold, R. (1999) Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 19, 1720-1730 (Pubitemid 29098230)
53. Weber, A., and Jung, K. (2002) Profiling early osmostress-dependent gene expression in Escherichia coli using DNA macroarrays. J. Bacteriol. 184, 5502-5507 (Pubitemid 35024398)
54. Moen, B., Janbu, A. O., Langsrud, S., Langsrud, O., Hobman, J. L., Constantinidou, C., Kohler, A., and Rudi, K. (2009) Global responses of Escherichia coli to adverse conditions determined by microarrays and FT-IT spectroscopy. Can. J. Microbiol. 55, 714-728
55. Kim, Y. H., Han, K. Y., Lee, K., and Lee, J. (2005) Proteome response of Escherichia coli fed-batch culture to temperature downshift. Appl. Microbiol. Biotechnol. 68, 786-793 (Pubitemid 41545623)
56. Weber, A., Kögl, S. A., and Jung, K. (2006) Time-dependent proteome alterations under osmotic stress during aerobic and anaerobic growth in Escherichia coli. J. Bacteriol. 188, 7165-7175 (Pubitemid 44547621)
57. Pin, C., Rolfe, M. D., Munoz-Cuevas, M., Hinton, J. C., Peck, M. W., Walton, N. J., and Baranyi, J. (2009) Network analysis of the transcriptional pattern of young and old cells of Escherichia coli during lag phase. BMC Syst. Biol. 3, 108
58. Benoit, S., Abaibou, H., and Mandrand-Berthelot, M. A. (1998) Topological analysis of the aerobic membrane-bound formate dehydrogenase of Escherichia coli. J. Bacteriol. 180, 6625-6634 (Pubitemid 29006077)
59. Ophir, T., and Gutnick, D. L. (1994) A role for exopolysaccharides in the protection of microorgansims from desiccation. Appl. Environ. Microbiol. 60, 740-745 (Pubitemid 24045225)
60. Chen, J., Lee, S. M., and Mao, Y. (2004) Protective effect of exopolysaccharide colanic acid of Escherichia coli O157:H7 to osmotic and oxidative stress. Int. J. Food Microbiol. 93, 281-286 (Pubitemid 38681002)
61. Mao, Y., Doyle, M. P., and Chen, J. (2006) Role of colanic acid exopolysaccharide in the survival of enterohaemorrhagic Escherichia coli O157:H7 in simulated gastrointestinal fluids. Lett. Appl. Microbiol. 42, 642-647 (Pubitemid 43780582)
62. Danese, P. N., Pratt, L. A., and Kolter, R. (2000) Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J. Bacteriol. 182, 3593-3596 (Pubitemid 30341626)
63. Meredith, T. C., Mamat, U., Kaczynski, Z., Lindner, B., Holst, O., and Woodard, R. W. (2007) Modification of lipopolysaccharide with colanic acid (M-antigen) repeats in Escherichia coli. J. Biol. Chem. 282, 7790-7798 (Pubitemid 47093581)
64. Laubacher, M. E., and Ades, S. E. (2008) The Rcs phosphorelay is a cell envelope stress response activated by peptidoglycan stress and contributes to intrinsic antibiotics resistance. J. Bacteriol. 190, 2065-2074 (Pubitemid 351355330)
65. Ionescu, M., and Belkin, S. (2009) Overproduction of exopolysaccharides by an Escherichia coli K-12 rpoS mutant in response to osmotic stress. Appl. Environ. Microbiol. 75, 483-492
66. Gottesman, S., and Stout, V. (1991) Regulation of capsular polysaccharide synthesis in Escherichia coli K12. Mol. Microbiol. 5, 1599-1606 (Pubitemid 21896188)
67. E and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr. Opin. Microbiol. 2, 159-165
68. Bergholz, T. M., Wick, L. M., Qi, W., Riordan, J. T., Ouellette, L. M., and Whittam, T. S. (2007) Global transcriptional response of Escherichia coli O157:H7 to growth transitions in glucose minimal medium. BMC Microbiol. 7, 97-123
69. Ferrières, L., and Clarke, D. J. (2003) The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the expression of a regulon in response to growth on a solid surface. Mol. Microbiol. 50, 1665-1682 (Pubitemid 38010460)
70. Brenner, M., and Ames, B. N. (1971) The histidine operon and its regulation. In: Vogel, H. J., ed. Metabolic pathways, Academic Press Inc, New York
71. Kawamura, D., Yamashita, I., Nimi, O., and Toh-e, A. (1994) Cloning and nucleotide sequence of a gene conferring ability to grow at a low temperature on Saccharomyces cerevisiae tryptophan auxotrophs. J. Ferment. Bioeng. 77, 1-9 (Pubitemid 24077826)
72. O'Donovan, G. A., and Ingraham, J. L. (1965) Cold-sensitive mutants of Escherichia coli resulting from increased feedback inhibition. Proc. Natl. Acad. Sci. U.S.A. 54, 451-457
73. Phadtare, S., and Inouye, M. (2004) Genome-wide transcriptional analysis of the cold shock response in wild-type and cold-sensitive, quadruple-csp- deletion strains of Escherichia coli. J. Bacteriol. 186, 7007-7014 (Pubitemid 39332139)
74. Casadesus, J., and Roth, J. R. (1989) Absence of insertions among spontaneous mutants of Salmonella typhimurium. Mol. Gen. Genet. 216, 210-216 (Pubitemid 19117839)
75. Frandsen, N., and D'Ari, R. (1993) Excess histidine enzymes cause AICAR-independent filamentation in Escherichia coli. Mol. Gen. Genet. 240, 348-354 (Pubitemid 23285948)
76. Horinouchi, T., Tamaoka, K., Furusawa, C., Ono, N., Suzuki, S., Hirasawa, T., Yomo, T., and Shimizu, H. (2010) Transcriptome analysis of parallel-evolved Escherichia coli strains under ethanol stress. BMC Genomics 11, 579
77. Liu, C. E., and Ames, G. F.-L. (1997) Characterization of transport through the periplasmic histidine permease using proteoliposomes reconstituted by dialysis. J. Biol. Chem. 272, 859-866 (Pubitemid 27034574)
78. Blanchard, J. L., Wholey, W. Y., Conlon, E. M., and Pomposiello, P. J. (2007) Rapid changes in gene expression dynamics in response to superoxide reveal SoxRS-depedent and independent transcriptional networks. PLoS ONE 2, e1186
79. Varghese, S., Wu, A., Park, S., Imlay, K. R., and Imlay, J. A. (2007) Submicromolar hydrogen peroxide disrupts the ability of Fur protein to control free-iron levels in Escherichia coli. Mol. Microbiol. 64, 822-830 (Pubitemid 46653221)
80. Cheung, K. J., Badarinarayana, V., Selinger, D. W., Janse, D., and Church, G. M. (2003) A microarray-based antibiotic screen identifies a regulatory role for supercoiling in the osmotic stress response of Escherichia coli. Genome Res. 13, 206-215 (Pubitemid 36575769)
81. Francez-Charlot, A., Laugel, B., Van Gemert, A., Dubarry, N., Wiorowski, F., Castanié-Cornet, M. P., Gutierrez, C., and Cam, K. (2003) RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli. Mol. Microbiol. 49, 823-832 (Pubitemid 36918699)
82. Smirnova, G. V., Zakirova, O. N., and Oktyabrskii, O. N. (2001) The role of antioxidant systems in the cold stress response of Escherichia coli. Microbiology 70, 45-50 (Pubitemid 33752836)
83. Gunasekera, T. S., Csonka, L. N., and Paliy, O. (2008) Genome-wide transcriptional responses of Escherichia coli K-12 to continuous osmotic and heat stresses. J. Bacteriol. 190, 3712-3720
84. Carmel-Harel, O., and Storz, G. (2000) Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu. Rev. Microbiol. 54, 439-461
85. Polissi, A., Laurentis, W. D., Zangrossi, S., Briani, F., Longhi, V., Pesole, G., and Deho, G. (2003) Changes in Escherichia coli transcriptome during acclimatization at low temperature. Res. Microbiol. 154, 573-580 (Pubitemid 37177001)
86. Shabala, L., Bowman, J., Brown, J., Ross, T., McMeekin, T., and Shabala, S. (2009) Ion transport and osmotic adjustment in Escherichia coli in response to ionic and non-ionic osmotica. Environ. Microbiol. 11, 137-148
87. Zheng, M., Wang, X., Templeton, L. J., Smulski, D. R., LaRossa, R. A., and Storz, G. (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 183, 4562-4570 (Pubitemid 32646006)
88. Tramonti, A., Visca, P., De Canio, M., Falconi, M., and De Biase, D. (2002) Functional characterization and regulation of gadX, a gene encoding an AraC/XylS-like transcriptional activator of the Escherichia coli glutamic acid decarboxylase system. J. Bacteriol. 184, 2603-2613 (Pubitemid 34457026)