1887

Abstract

, a strictly anaerobic bacterium, is able to survive when exposed to oxygen for short periods of time and exhibits a complex adaptive response to reactive oxygen species, both under aerobic and anaerobic conditions. However, this adaptive response is not completely understood. possesses specialized genes that might be involved in this adaptive process, such as those encoding superoxide dismutase (SOD), superoxide reductase and alkyl hydroperoxide reductase, but their contribution to the oxidative stress response and their control mechanisms are unknown. By a combination of functional complementation of strains impaired in either SOD, alkyl hydroperoxide reductase (AhpC) or catalase activity (Cat), transcription analysis and characterization of mutants impaired in regulatory genes, it was concluded that: (i) the product of the gene is certainly essential to scavenge superoxide radicals, (ii) the gene, which is fully induced in all oxidative stress conditions, is probably involved in the scavenging of all intracellular peroxides, (iii) the three rubrerythrin () genes of do not encode proteins with HO reductase activity, and (iv) the two rubredoxin () genes do not contribute to the hypothetical superoxide reductase activity, but are likely to belong to an electron transfer chain involved in energy metabolism.

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2004-06-01
2024-03-28
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References

  1. Altschul S. F., Boguski M. S., Gish W., Wooton J. C. 1994; Issues in searching molecular sequence databases. Nat Genet 6:119–129 [CrossRef]
    [Google Scholar]
  2. Azeddoug H., Hubert J., Reysset G. 1992; Stable inheritance of shuttle vectors based on plasmid pIM13 in a mutant strain of Clostridium acetobutylicum. J Gen Microbiol 138:1371–1378 [CrossRef]
    [Google Scholar]
  3. Bebien M., Lagniel G., Garin J., Touati D., Labarre J., Verméglio A. 2002; Involvement of superoxide dismutases in the response of Escherichia coli to selenium oxides. J Bacteriol 184:1556–1564 [CrossRef]
    [Google Scholar]
  4. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein. Anal Biochem 72:248–254 [CrossRef]
    [Google Scholar]
  5. Briolat V., Reysset G. 2002; Identification of the Clostridium perfringens genes involved in the adaptive response to oxidative stress. J Bacteriol 184:2333–2343 [CrossRef]
    [Google Scholar]
  6. Carlioz A., Touati D. 1986; Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life?. EMBO J 5:623–630
    [Google Scholar]
  7. Coulter E. D., Shenvi N. V., Kurtz D. M., Jr. 1999; NADH peroxidase activity of rubrerythrin. Biochem Biophys Res Commun 255:317–323 [CrossRef]
    [Google Scholar]
  8. Das A., Coulter E. D., Ljungdahl L. G., Kurtz D. M., Jr. 2001; Five-gene cluster in Clostridium thermoaceticum consisting of two divergent operons encoding rubredoxin oxidoreductase-rubredoxin and rubrerythrin-type A flavoprotein-high-molecular-weight rubredoxin. J Bacteriol 183:1560–1567 [CrossRef]
    [Google Scholar]
  9. Dupuy B., Sonenshein A. L. 1998; Regulated transcription of Clostridium difficile toxin genes. Mol Microbiol 27:107–120 [CrossRef]
    [Google Scholar]
  10. Emerson J. P., Coulter E. D., Cabelli D. E., Phillips R. S., Kurtz D. M., Jr. 2002; Kinetics and mechanism of superoxide reduction by two-iron superoxide reductase from Desulfovibrio vulgaris. Biochemistry 41:4348–4357 [CrossRef]
    [Google Scholar]
  11. 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]
  12. Gomes C. M., Silva G., Oliveira S., Legall J., Liu M.-Y., Antonio X. V., Rodrigues-Pousada C., Teixeira M. 1997; Studies on the redox centers of the terminal oxidase from Desulfovibrio gigas and evidence for its interaction with rubredoxin. J Biol Chem 272:22502–22508 [CrossRef]
    [Google Scholar]
  13. Green J., Scott C., Guest J. R. 2001; Functional versatility in the CRP-FNR superfamily of transcription factors: FNR and FLP. Adv Microbiol Physiol 44:1–34
    [Google Scholar]
  14. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580 [CrossRef]
    [Google Scholar]
  15. Hérouart D., Sigaud S., Moreau S., Frendo P., Touati D., Puppo A. 1996; Cloning and characterization of the katA gene of Rhizobium meliloti encoding a hydrogen peroxide-inducible catalase. J Bacteriol 178:6802–6809
    [Google Scholar]
  16. Heym B., Cole S. 1992; Isolation and characterisation of isoniazid-resistant mutants of Mycobacterium smegmatis and M. aurum. Res Microbiol 143:721–730 [CrossRef]
    [Google Scholar]
  17. Hwang C. S., Rhie G. E., Oh J. H., Huh W. K., Yim H. S., Kang S. O. 2002; Copper- and zinc-containing superoxide dismutase (Cu/ZnSOD) is required for the protection of Candida albicans against oxidative stresses and the expression of its full virulence. Microbiology 148:3705–3713
    [Google Scholar]
  18. Imlay J. A. 2002; How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis. Adv Microbial Physiol 46:111–153
    [Google Scholar]
  19. Jenney F. E., Jr, Verhagen M. F. J. M., Cui X., Adams M. W. W. 1999; Anaerobic microbes: oxygen detoxification without superoxide dismutase. Science 286:306–309 [CrossRef]
    [Google Scholar]
  20. Kurtz D. M. Jr, Coulter E. D. 2002; The mechanism(s) of superoxide reduction by superoxide reductases in vitro and in vivo. J Biological Inorg Chem 7:653–658 [CrossRef]
    [Google Scholar]
  21. 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]
  22. Liochev S. I., Fridovich I. 1997; A mechanism for complementation of the sodA sodB defect in Escherichia coli by overproduction of the rub gene product (desulfoferrodoxin) from Desulfofoarculus baarsii. J Biol Chem 272:25573–25575 [CrossRef]
    [Google Scholar]
  23. 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]
  24. 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 [CrossRef]
    [Google Scholar]
  25. Lynch M. C., Kuramitsu H. K. 1999; Role of superoxide dismutase activity in the physiology of Porphyromonas gingivalis. Infect Immun 67:3367–3375
    [Google Scholar]
  26. Mahony D. E., Moore T. I. 1976; Stable L-forms of Clostridium perfringens and their growth on glass surface. Can J Microbiol 22:953–959 [CrossRef]
    [Google Scholar]
  27. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  28. Nakayama K. 1994; Rapid viability loss on exposure to air in a superoxide dismutase-deficient mutant of Porphyromonas gingivalis. J Bacteriol 176:1939–1943
    [Google Scholar]
  29. O'Brien D. K., Melville S. B. 2000; The anaerobic pathogen Clostridium perfringens can escape the phagosome of macrophages under aerobic conditions. Cell Microbiol 2:505–519 [CrossRef]
    [Google Scholar]
  30. Pan N., Imlay J. A. 2001; How does oxygen inhibit central metabolism in the obligate anaerobe Bacteroides thetaiotaomicron. Mol Microbiol 39:1562–1571 [CrossRef]
    [Google Scholar]
  31. Pianzzola M. J., Soubes M., Touati D. 1996; Overproduction of the rbo gene product from Desulfovibrio species suppresses all deleterious effects of lack of superoxide dismutase inEscherichia coli. J Bacteriol 178:6736–6742
    [Google Scholar]
  32. Poyart C., Pellegrini E., Gaillot O., Boumaila C., Baptista M., Trieu-Cuot P. 2001; Contribution of Mn-cofactored superoxide dismutase (SodA) to the virulence of Streptococcus agalactiae. Infect Immun 69:5098–5106 [CrossRef]
    [Google Scholar]
  33. Privitera G., Dublanchet A., Sebald M. 1979; Transfer of multiple antibiotic resistance between subspecies of Bacteroides fragilis. J Infect Dis 139:97–101 [CrossRef]
    [Google Scholar]
  34. Rutherford K., Parkhill J., Crook J., Horsnell T., Rice P., Rajandream M.-A., Barrell B. 2000; Artemis: sequence visualization and annotation. Bioinformatics 16:944–945 [CrossRef]
    [Google Scholar]
  35. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  36. Santos H., Fareleira P., Xavier A. V., Chen L., Liu M.-Y., LeGall J. 1993; Aerobic metabolism of carbon reserves by the ‘obligate anaerobe’ Desulfovibrio gigas. Biochem Biophys Res Commun 193:100–105 [CrossRef]
    [Google Scholar]
  37. Schneider W. C. 1957; Determination of nucleic acids in tissues by pentose analysis. Methods Enzymol 3:680–684
    [Google Scholar]
  38. Seaver L. C., Imlay A. J. 2001; Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183:7173–7181 [CrossRef]
    [Google Scholar]
  39. Seyler R. W., Olson J. W., Maier R. J. 2001; Superoxide dismutase-deficient mutants of Helicobacter pylori are hypersensitive to oxidative stress and defective in host colonization. Infect Immun 69:4034–4040 [CrossRef]
    [Google Scholar]
  40. Shimizu T., Ohtani K., Hirakawa H.7 other authors 2002; Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc Natl Acad Sci U S A 99:996–1001 [CrossRef]
    [Google Scholar]
  41. Sies H. 1986; Biochemistry of oxidative stress. Angew Chem Int Ed Engl 25:1058–1071 [CrossRef]
    [Google Scholar]
  42. Staden R., Judge D. P., Bonfield J. K. 2003; Analysing sequences using the Staden package and emboss. In Introduction to Bioinformatics. A Theoretical and Practical Approach pp. 393–410 Edited by Krawetz S. A., Womble D. D. Totawa: Humana Press;
    [Google Scholar]
  43. Sztukowska M., Bugno M., Potempa J., Travis J., Kurtz D. M. 2002; Role of rubrerythrin in the oxidative stress response of Porphyromonas gingivalis. Mol Microbiol 44:479–488 [CrossRef]
    [Google Scholar]
  44. Takeshita S. M., Sato M., Toba M., Masahashi W., Hashimoto-Gotoh T. 1987; High-copy-number and low-copy-number plasmid vectors for lacZ alpha-complementation and chloramphenicol- or kanamycin-resistance selection. Gene 61:63–74 [CrossRef]
    [Google Scholar]
  45. Tartaglia L. A., Storz G., Brodsky M. H., Lai A., Ames B. N. 1990; Alkyl hydroperoxide reductase from Salmonella typhimurium. J Biol Chem 265:10535–10540
    [Google Scholar]
  46. Touati D. 2000; Iron and oxidative stress in bacteria. Arch Biochem Biophys 373:1–6 [CrossRef]
    [Google Scholar]
  47. Touati D., Jaques M., Tardat B., Bouchard L., Despied S. 1995; Lethal oxidative damage and mutagenesis are generated by iron in Δfur mutants of Escherichia coli: protective role of superoxide dismutase. J Bacteriol 177:2305–2314
    [Google Scholar]
  48. Trinh S., Briolat V., Reysset G. 2000; Growth response of Clostridium perfringens to oxidative stress. Anaerobe 6:233–240 [CrossRef]
    [Google Scholar]
  49. Voordouw J. K., Voordouw G. 1998; Deletion of the rbo gene increases the oxygen sensitivity of the sulfate-reducing bacteriumDesulfovibrio vulgaris Hildenborough. Appl Environ Microbiol 64:2882–2887
    [Google Scholar]
  50. Voyich J. M., Sturdevant D. E., Braughton K. R., Kobayashi S. D., Lei B., Virtaneva K., Dorward D. W., Musser J. M., DeLeo F. R. 2003; Genome-wide protective response used by group A Streptococcus to evade destruction by human polymorphonuclear leukocytes. Proc Natl Acad Sci U S A 100:1996–2001 [CrossRef]
    [Google Scholar]
  51. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119 [CrossRef]
    [Google Scholar]
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