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.

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2009-01-01
2020-08-05
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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 Microbiol64:1079–1085
    [Google Scholar]
  2. Bertram J., Dürre P.. 1989; Conjugal transfer and expression of streptococcal transposons in Clostridium acetobutylicum. Arch Microbiol151:551–557
    [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 Biochem72:248–254
    [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 Biophys394:76–86
    [Google Scholar]
  5. Coulter E. D., Shenvi N. V., Kurtz D. M. Jr. 1999; NADH peroxidase activity of rubrerythrin. Biochem Biophys Res Commun255:317–323
    [Google Scholar]
  6. Dolla A., Fournier M., Dermoun Z.. 2006; Oxygen defense in sulfate-reducing bacteria. J Biotechnol126:87–100
    [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 Bacteriol185:71–79
    [Google Scholar]
  8. Geissmann T. A., Teuber M., Meile L.. 1999; Transcriptional analysis of the rubrerythrin and superoxide dismutase genes of Clostridium perfringens. J Bacteriol181:7136–7139
    [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 Microbiol71:2777–2781
    [Google Scholar]
  10. Guedon E., Petitdemange H.. 2001; Identification of the gene encoding NADH-rubredoxin oxidoreductase in Clostridium acetobutylicum. Biochem Biophys Res Commun285:496–502
    [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. Biochemistry34:3310–3318
    [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 Microbiol185:270–276
    [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 Microbiol68:848–860
    [Google Scholar]
  14. Imlay J. A.. 2002; How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis. Adv Microb Physiol46:111–153
    [Google Scholar]
  15. Imlay J. A.. 2003; Pathways of oxidative damage. Annu Rev Microbiol57:395–418
    [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 Chem10:407–416
    [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 Biochem98:786–796
    [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. Biochemistry43:3204–3213
    [Google Scholar]
  19. Kawasaki S., Ishikura J., Watamura Y., Niimura Y.. 2004; Identification of O2-induced peptides in an obligatory anaerobe, Clostridium acetobutylicum. FEBS Lett571:21–25
    [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 Microbiol71:8442–8450
    [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 Lett581:2460–2464
    [Google Scholar]
  22. Kurtz D. M. Jr. 2006; Avoiding high-valent iron intermediates: superoxide reductase and rubrerythrin. J Inorg Biochem100:679–693
    [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. Nature227:680–685
    [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 Bacteriol178:7152–7158
    [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 Bacteriol179:4607–4615
    [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 Bacteriol183:101–108
    [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 Lett238:249–254
    [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 Microbiol59:1077–1081
    [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 Pathog2: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 Bacteriol183:4823–4838
    [Google Scholar]
  32. O'Brien R. W., Morris J. G.. 1971; Oxygen and the growth and metabolism of Clostridium acetobutylicum. J Gen Microbiol68:307–318
    [Google Scholar]
  33. Riebe O., Fischer R.-J., Bahl H.. 2007; Desulfoferrodoxin of Clostridium acetobutylicum functions as a superoxide reductase. FEBS Lett581:5605–5610
    [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 Bioeng27:681–694
    [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 Protoc2:1528–1535
    [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 Bacteriol183:7173–7181
    [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 Immun10:356–360
    [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 Microbiol44:479–488
    [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 Biol2:253–262
    [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 Bacteriol186:7888–7895
    [Google Scholar]
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