1887

Abstract

An unusual non-haem diiron protein, reverse rubrerythrin (revRbr), is known to be massively upregulated in response to oxidative stress in the strictly anaerobic bacterium . In the present study both and results demonstrate an HO and O detoxification pathway in involving revRbr, rubredoxin (Rd) and NADH : rubredoxin oxidoreductase (NROR). RevRbr exhibited both NADH peroxidase (NADH : HO oxidoreductase) and NADH oxidase (NADH : O oxidoreductase) activities in assays using NROR as the electron-transfer intermediary from NADH to revRbr. Rd increased the NADH consumption rate by serving as an intermediary electron-transfer shuttle between NROR and revRbr. While HO was found to be the preferred substrate for revRbr, its relative oxidase activity was found to be significantly higher than that reported for other Rbrs. A revRbr-overexpressing strain of showed significantly increased tolerance to HO and O exposure. RevRbr thus appears to protect against oxidative stress by functioning as the terminal component of an NADH peroxidase and NADH oxidase.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.022756-0
2009-01-01
2024-10-10
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/1/16.html?itemId=/content/journal/micro/10.1099/mic.0.022756-0&mimeType=html&fmt=ahah

References

  1. Bermejo L. L., Welker N. E., Papoutsakis E. T. 1998; Expression of Clostridium acetobutylicum ATCC 824 genes in Escherichia coli for acetone production and acetate detoxification. Appl Environ Microbiol 64:1079–1085
    [Google Scholar]
  2. Bertram J., Dürre P. 1989; Conjugal transfer and expression of streptococcal transposons in Clostridium acetobutylicum . Arch Microbiol 151:551–557
    [Google Scholar]
  3. Bradford M. M. 1976; A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72:248–254
    [Google Scholar]
  4. Coulter E. D., Kurtz D. M. Jr 2001; A role for rubredoxin in oxidative stress protection in Desulfovibrio vulgaris. Catalytic electron transfer to rubrerythrin and two-iron superoxide reductase. Arch Biochem Biophys 394:76–86
    [Google Scholar]
  5. Coulter E. D., Shenvi N. V., Kurtz D. M. Jr 1999; NADH peroxidase activity of rubrerythrin. Biochem Biophys Res Commun 255:317–323
    [Google Scholar]
  6. Dolla A., Fournier M., Dermoun Z. 2006; Oxygen defense in sulfate-reducing bacteria. J Biotechnol 126:87–100
    [Google Scholar]
  7. Fournier M., Zhang Y., Wildschut J. D., Dolla A., Voordouw J. K., Schriemer D. C., Voordouw G. 2003; Function of oxygen resistance proteins in the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. J Bacteriol 185:71–79
    [Google Scholar]
  8. Geissmann T. A., Teuber M., Meile L. 1999; Transcriptional analysis of the rubrerythrin and superoxide dismutase genes of Clostridium perfringens . J Bacteriol 181:7136–7139
    [Google Scholar]
  9. Girbal L., Von Abendroth G., Winkler M., Benton P. M. C., Meynial-Salles I., Croux C., Peters J. W., Happe T., Soucaille P. 2005; Homologous and heterologous overexpression in Clostridium acetobutylicum and characterization of purified clostridial and algal Fe-only hydrogenases with high specific activities. Appl Environ Microbiol 71:2777–2781
    [Google Scholar]
  10. Guedon E., Petitdemange H. 2001; Identification of the gene encoding NADH-rubredoxin oxidoreductase in Clostridium acetobutylicum . Biochem Biophys Res Commun 285:496–502
    [Google Scholar]
  11. Gupta N., Bonomi F., Kurtz D. M. Jr, Ravi N., Wang D. L., Huynh B. H. 1995; Recombinant Desulfovibrio vulgaris rubrerythrin. Isolation and characterization of the diiron domain. Biochemistry 34:3310–3318
    [Google Scholar]
  12. Hillmann F., Fischer R.-J., Bahl H. 2006; The rubrerythrin-like protein Hsp21 of Clostridium acetobutylicum is a general stress protein. Arch Microbiol 185:270–276
    [Google Scholar]
  13. Hillmann F., Fischer R.-J., Bahl H. 2008; PerR acts as a switch for oxygen tolerance in the strict anaerobe Clostridium acetobutylicum . Mol Microbiol 68:848–860
    [Google Scholar]
  14. Imlay J. A. 2002; How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis. Adv Microb Physiol 46:111–153
    [Google Scholar]
  15. Imlay J. A. 2003; Pathways of oxidative damage. Annu Rev Microbiol 57:395–418
    [Google Scholar]
  16. Iyer R. B., Silaghi-Dumitrescu R., Kurtz D. M. Jr, Lanzilotta W. N. 2005; High-resolution crystal structures of Desulfovibrio vulgaris nigerythrin: facile, redox-dependent iron movement, domain interface variability, and peroxidase activity in the rubrerythrins. J Biol Inorg Chem 10:407–416
    [Google Scholar]
  17. Jin S., Kurtz D. M. Jr, Liu Z.-J., Rose J., Wang B. C. 2004a; Displacement of iron by zinc at the diiron site of Desulfovibrio vulgaris rubrerythrin. X-ray crystal structure and anomalous scattering analysis. J Inorg Biochem 98:786–796
    [Google Scholar]
  18. Jin S., Kurtz D. M. Jr, Liu Z.-J., Rose J., Wang B. C. 2004b; X-ray crystal structure of Desulfovibrio vulgaris rubrerythrin with zinc substituted into the [Fe(SCys)4] site and alternative diiron site structures. Biochemistry 43:3204–3213
    [Google Scholar]
  19. Kawasaki S., Ishikura J., Watamura Y., Niimura Y. 2004; Identification of O2-induced peptides in an obligatory anaerobe, Clostridium acetobutylicum . FEBS Lett 571:21–25
    [Google Scholar]
  20. Kawasaki S., Watamura Y., Ono M., Watanabe T., Takeda K., Niimura Y. 2005; Adaptive responses to oxygen stress in obligatory anaerobes Clostridium acetobutylicum and Clostridium aminovalericum . Appl Environ Microbiol 71:8442–8450
    [Google Scholar]
  21. Kawasaki S., Ono M., Watamura Y., Sakai Y., Satoh T., Arai T., Satoh J., Niimura Y. 2007; An O2-inducible rubrerythrin-like protein, rubperoxin, is functional as a H2O2 reductase in an obligatory anaerobe Clostridium acetobutylicum . FEBS Lett 581:2460–2464
    [Google Scholar]
  22. Kurtz D. M. Jr 2006; Avoiding high-valent iron intermediates: superoxide reductase and rubrerythrin. J Inorg Biochem 100:679–693
    [Google Scholar]
  23. Kurtz D. M. Jr 2007; Flavo-diiron enzymes: nitric oxide or dioxygen reductases?. Dalton Trans4115–4121
    [Google Scholar]
  24. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 227:680–685
    [Google Scholar]
  25. Lehmann Y., Meile L., Teuber M. 1996; Rubrerythrin from Clostridium perfringens: cloning of the gene, purification of the protein, and characterization of its superoxide dismutase function. J Bacteriol 178:7152–7158
    [Google Scholar]
  26. Lumppio H. L., Shenvi N. V., Garg R. P., Summers A. O., Kurtz D. M. Jr 1997; A rubrerythrin operon and nigerythrin gene in Desulfovibrio vulgaris (Hildenborough. J Bacteriol 179:4607–4615
    [Google Scholar]
  27. Lumppio H. L., Shenvi N. V., Summers A. O., Voordouw G., Kurtz D. M. Jr 2001; Rubrerythrin and rubredoxin oxidoreductase in Desulfovibrio vulgaris: a novel oxidative stress protection system. J Bacteriol 183:101–108
    [Google Scholar]
  28. May A., Hillmann F., Riebe O., Fischer R.-J., Bahl H. 2004; A rubrerythrin-like oxidative stress protein of Clostridium acetobutylicum is encoded by a duplicated gene and identical to the heat shock protein Hsp21. FEMS Microbiol Lett 238:249–254
    [Google Scholar]
  29. Mermelstein L. D., Papoutsakis E. D. 1993; In vivo methylation in Escherichia coli by the Bacillus subtilis phage phi 3T I methyltransferase to protect plasmids from restriction upon transformation of Clostridium acetobutylicum ATCC 824. Appl Environ Microbiol 59:1077–1081
    [Google Scholar]
  30. Mydel P., Takahashi Y., Yumoto H., Sztukowska M., Kubica M., Kurtz D. M. Jr, Travis J., Collins L. V., Gibson F. C. III other authors 2006; Roles of the host oxidative immune response and bacterial antioxidant rubrerythrin during Porphyromonas gingivalis infection. PLoS Pathog 2:e76
    [Google Scholar]
  31. Nölling J., Breton G., Omelchenko M. V., Makarova K. S., Zeng Q., Gibson R., Lee H. M., Dubois J., Qiu D. other authors 2001; Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum . J Bacteriol 183:4823–4838
    [Google Scholar]
  32. O'Brien R. W., Morris J. G. 1971; Oxygen and the growth and metabolism of Clostridium acetobutylicum . J Gen Microbiol 68:307–318
    [Google Scholar]
  33. Riebe O., Fischer R.-J., Bahl H. 2007; Desulfoferrodoxin of Clostridium acetobutylicum functions as a superoxide reductase. FEBS Lett 581:5605–5610
    [Google Scholar]
  34. Roos J. W., McLaughlin J. K., Papoutsakis E. T. 1985; The effect of pH on nitrogen supply, cell lysis and solvent production in fermentations of Clostridium acetobutylicum . Biotechnol Bioeng 27:681–694
    [Google Scholar]
  35. Schmidt T. G. M., Skerra A. 2007; The Strep-tag system for one-step purification and high-affinity detection or capturing of proteins. Nat Protoc 2:1528–1535
    [Google Scholar]
  36. Seaver L. C., Imlay J. A. 2001; Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli . J Bacteriol 183:7173–7181
    [Google Scholar]
  37. Smith A. L., Rosenberg I., Averill D. R., Moxon E. R., Stossel T., Smith D. H. 1974; Brain polymorphonuclear leukocyte quantitation by peroxidase assay. Infect Immun 10:356–360
    [Google Scholar]
  38. Sztukowska M., Bugno M., Potempa J., Travis J., Kurtz D. M. Jr 2002; Role of rubrerythrin in the oxidative stress response of Porphyromonas gingivalis . Mol Microbiol 44:479–488
    [Google Scholar]
  39. Valentine J. S., Wertz D. L., Lyons T. J., Liou L. L., Goto J. J., Gralla E. B. 1998; The dark side of dioxygen biochemistry. Curr Opin Chem Biol 2:253–262
    [Google Scholar]
  40. Weinberg M. V., Jenney F. E. Jr, Cui X., Adams M. W. 2004; Rubrerythrin from the hyperthermophilic archaeon Pyrococcus furiosus is a rubredoxin-dependent, iron-containing peroxidase. J Bacteriol 186:7888–7895
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.022756-0
Loading
/content/journal/micro/10.1099/mic.0.022756-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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