1887

Abstract

Micro-organisms may simultaneously encounter multiple stresses in their environment. To investigate the protection that several known O157 : H7 acid-resistance systems might provide against both oxidative and acid stress, the addition of diamide, a membrane-permeable thiol-specific oxidizing agent, or hydrogen peroxide were used concurrent with acid challenge at pH 2.5 to determine bacterial survival. The addition of either diamide or hydrogen peroxide decreased bacterial survival in a dose-dependent manner for O157 : H7 during challenge at pH 2.5 following overnight growth in LB MES pH 5.5 (acid-resistance system 1, AR1). In contrast, the presence of either glutamate or arginine during challenge provided significant protection against diamide- and hydrogen peroxide-induced oxidative stress during pH 2.5 acid challenge. Oxidative stress protection during acid challenge required and for the glutamate- (AR2) and arginine- (AR3) dependent acid-resistance systems, respectively. In addition, maximal protection against oxidative stress in the presence of glutamate required a low external pH (pH 2.5), since pH 5.5 did not protect. This study demonstrates that the glutamate- and arginine-dependent acid-resistance systems of O157 : H7 can simultaneously protect against oxidative stress during extreme acid challenge.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.022905-0
2009-03-01
2019-10-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/3/805.html?itemId=/content/journal/micro/10.1099/mic.0.022905-0&mimeType=html&fmt=ahah

References

  1. Aslund, F. & Beckwith, J. ( 1999; ). The thioredoxin superfamily: redundancy, specificity, and gray-area genomics. J Bacteriol 181, 1375–1379.
    [Google Scholar]
  2. Becker-Hapak, M. & Eisenstark, A. ( 1995; ). Role of rpoS in the regulation of glutathione oxidoreductase (gor) in Escherichia coli. FEMS Microbiol Lett 134, 39–44.
    [Google Scholar]
  3. Blankenhorn, D., Phillips, J. & Slonczewski, J. L. ( 1999; ). Acid- and base-induced proteins during aerobic and anaerobic growth of Escherichia coli revealed by two-dimensional gel electrophoresis. J Bacteriol 181, 2209–2216.
    [Google Scholar]
  4. Cabiscol, E., Tamarit, J. & Ros, J. ( 2000; ). Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3, 3–8.
    [Google Scholar]
  5. Carmel-Harel, O. & 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.[CrossRef]
    [Google Scholar]
  6. Castanie-Cornet, M. P., Penfound, T. A., Smith, D., Elliott, J. F. & Foster, J. W. ( 1999; ). Control of acid resistance in Escherichia coli. J Bacteriol 181, 3525–3535.
    [Google Scholar]
  7. Cherepanov, P. P. & Wackernagel, W. ( 1995; ). Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158, 9–14.[CrossRef]
    [Google Scholar]
  8. Datsenko, K. A. & 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.[CrossRef]
    [Google Scholar]
  9. Demple, B. ( 1991; ). Regulation of bacterial oxidative stress genes. Annu Rev Genet 25, 315–337.[CrossRef]
    [Google Scholar]
  10. Demple, B. & Halbrook, J. ( 1983; ). Inducible repair of oxidative DNA damage in Escherichia coli. Nature 304, 466–468.[CrossRef]
    [Google Scholar]
  11. Foster, J. W. ( 2004; ). Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2, 898–907.[CrossRef]
    [Google Scholar]
  12. Geiszt, M., Witta, J., Baffi, J., Lekstrom, K. & Leto, T. L. ( 2003; ). Dual oxidases represent novel hydrogen peroxide sources supporting mucosal surface host defense. FASEB J 17, 1502–1504.
    [Google Scholar]
  13. Gonzalez-Flecha, B. & Demple, B. ( 1995; ). Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J Biol Chem 270, 13681–13687.[CrossRef]
    [Google Scholar]
  14. Griffin, P. M., Ostroff, S. M., Tauxe, R. V., Greene, K. D., Wells, J. G., Lewis, J. H. & Blake, P. A. ( 1988; ). Illnesses associated with Escherichia coli O157 : H7 infections. A broad clinical spectrum. Ann Intern Med 109, 705–712.[CrossRef]
    [Google Scholar]
  15. Halliwell, B., Clement, M. V. & Long, L. H. ( 2000; ). Hydrogen peroxide in the human body. FEBS Lett 486, 10–13.[CrossRef]
    [Google Scholar]
  16. 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]
    [Google Scholar]
  17. Hengge-Aronis, R., Lange, R., Henneberg, N. & Fischer, D. ( 1993; ). Osmotic regulation of rpoS-dependent genes in Escherichia coli. J Bacteriol 175, 259–265.
    [Google Scholar]
  18. Hersh, B. M., Farooq, F. T., Barstad, D. N., Blankenhorn, D. L. & Slonczewski, J. L. ( 1996; ). A glutamate-dependent acid resistance gene in Escherichia coli. J Bacteriol 178, 3978–3981.
    [Google Scholar]
  19. Imlay, J. A. & Fridovich, I. ( 1991; ). Assay of metabolic superoxide production in Escherichia coli. J Biol Chem 266, 6957–6965.
    [Google Scholar]
  20. Jenkins, D. E., Schultz, J. E. & Matin, A. ( 1988; ). Starvation-induced cross protection against heat or H2O2 challenge in Escherichia coli. J Bacteriol 170, 3910–3914.
    [Google Scholar]
  21. Karch, H., Tarr, P. I. & Bielaszewska, M. ( 2005; ). Enterohaemorrhagic Escherichia coli in human medicine. Int J Med Microbiol 295, 405–418.[CrossRef]
    [Google Scholar]
  22. Kosower, N. S. & Kosower, E. M. ( 1995; ). Diamide: an oxidant probe for thiols. Methods Enzymol 251, 123–133.
    [Google Scholar]
  23. Large, T. M., Walk, S. T. & Whittam, T. S. ( 2005; ). Variation in acid resistance among shiga toxin-producing clones of pathogenic Escherichia coli. Appl Environ Microbiol 71, 2493–2500.[CrossRef]
    [Google Scholar]
  24. Lin, J., Lee, I. S., Frey, J., Slonczewski, J. L. & Foster, J. W. ( 1995; ). Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J Bacteriol 177, 4097–4104.
    [Google Scholar]
  25. Lin, J., Smith, M. P., Chapin, K. C., Baik, H. S., Bennett, G. N. & Foster, J. W. ( 1996; ). Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl Environ Microbiol 62, 3094–3100.
    [Google Scholar]
  26. Maurer, L. M., Yohannes, E., Bondurant, S. S., Radmacher, M. & Slonczewski, J. L. ( 2005; ). pH regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12. J Bacteriol 187, 304–319.[CrossRef]
    [Google Scholar]
  27. McCann, M. P., Kidwell, J. P. & Matin, A. ( 1991; ). The putative sigma factor KatF has a central role in development of starvation-mediated general resistance in Escherichia coli. J Bacteriol 173, 4188–4194.
    [Google Scholar]
  28. Prinz, W. A., Aslund, F., Holmgren, A. & Beckwith, J. ( 1997; ). The role of the thioredoxin and glutaredoxin pathways in reducing protein disulfide bonds in the Escherichia coli cytoplasm. J Biol Chem 272, 15661–15667.[CrossRef]
    [Google Scholar]
  29. Richard, H. & Foster, J. W. ( 2004; ). Escherichia coli glutamate- and arginine-dependent acid resistance systems increase internal pH and reverse transmembrane potential. J Bacteriol 186, 6032–6041.[CrossRef]
    [Google Scholar]
  30. Ritz, D., Patel, H., Doan, B., Zheng, M., Aslund, F., Storz, G. & Beckwith, J. ( 2000; ). Thioredoxin 2 is involved in the oxidative stress response in Escherichia coli. J Biol Chem 275, 2505–2512.[CrossRef]
    [Google Scholar]
  31. Sato, E. F., Choudhury, T., Nishikawa, T. & Inoue, M. ( 2008; ). Dynamic aspect of reactive oxygen and nitric oxide in oral cavity. J Clin Biochem Nutr 42, 8–13.[CrossRef]
    [Google Scholar]
  32. Stancik, L. M., Stancik, D. M., Schmidt, B., Barnhart, D. M., Yoncheva, Y. N. & Slonczewski, J. L. ( 2002; ). pH-dependent expression of periplasmic proteins and amino acid catabolism in Escherichia coli. J Bacteriol 184, 4246–4258.[CrossRef]
    [Google Scholar]
  33. Storz, G. & Imlay, J. A. ( 1999; ). Oxidative stress. Curr Opin Microbiol 2, 188–194.[CrossRef]
    [Google Scholar]
  34. Vogel, H. J. & Bonner, D. M. ( 1956; ). Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem 218, 97–106.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.022905-0
Loading
/content/journal/micro/10.1099/mic.0.022905-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error