Fumarate reductase is a major contributor to the generation of reactive oxygen species in the anaerobe Free

Abstract

Despite the detrimental role that endogenously generated reactive oxygen species (ROS) may play in bacteria exposed to aerobic environments, very few sources of ROS have been identified . Such studies are often precluded by the presence of efficient ROS-scavenging pathways, like those found in the aerotolerant anaerobe . Here we demonstrate that deletion of the genes encoding catalase (Kat), alkylhydroperoxide reductase (AhpC) and thioredoxin-dependent peroxidase (Tpx) strongly inhibits HO detoxification in , thereby allowing for the quantification of ROS production. Exogenous fumarate significantly reduced HO production in a ΔΔΔ strain, as did deletion of fumarate reductase subunit c (). Deletion of also increased the aerotolerance of a strain lacking superoxide dismutase, indicating that fumarate reductase is a major contributor to ROS formation in exposed to oxygen.

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2012-02-01
2024-03-28
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References

  1. Baughn A. D., Malamy M. H. ( 2002). A mitochondrial-like aconitase in the bacterium Bacteroides fragilis: implications for the evolution of the mitochondrial Krebs cycle. Proc Natl Acad Sci U S A 99:4662–4667 [View Article][PubMed]
    [Google Scholar]
  2. Baughn A. D., Malamy M. H. ( 2003). The essential role of fumarate reductase in haem-dependent growth stimulation of Bacteroides fragilis . Microbiology 149:1551–1558 [View Article][PubMed]
    [Google Scholar]
  3. Baughn A. D., Malamy M. H. ( 2004). The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen. Nature 427:441–444 [View Article][PubMed]
    [Google Scholar]
  4. Fridovich I. ( 1998). Oxygen toxicity: a radical explanation. J Exp Biol 201:1203–1209[PubMed]
    [Google Scholar]
  5. Fridovich I. ( 1999). Fundamental aspects of reactive oxygen species, or what’s the matter with oxygen?. Ann N Y Acad Sci 893:13–18 [View Article][PubMed]
    [Google Scholar]
  6. Godoy V. G., Dallas M. M., Russo T. A., Malamy M. H. ( 1993). A role for Bacteroides fragilis neuraminidase in bacterial growth in two model systems. Infect Immun 61:4415–4426[PubMed]
    [Google Scholar]
  7. Gort A. S., Imlay J. A. ( 1998). Balance between endogenous superoxide stress and antioxidant defenses. J Bacteriol 180:1402–1410[PubMed]
    [Google Scholar]
  8. Hanahan D., Jessee J., Bloom F. R. ( 1991). Plasmid transformation of Escherichia coli and other bacteria. Methods Enzymol 204:63–113 [View Article][PubMed]
    [Google Scholar]
  9. Herren C. D., Rocha E. R., Smith C. J. ( 2003). Genetic analysis of an important oxidative stress locus in the anaerobe Bacteroides fragilis . Gene 316:167–175 [View Article][PubMed]
    [Google Scholar]
  10. Imlay J. A. ( 1995). A metabolic enzyme that rapidly produces superoxide, fumarate reductase of Escherichia coli . J Biol Chem 270:19767–19777[PubMed]
    [Google Scholar]
  11. Imlay J. A. ( 2003). Pathways of oxidative damage. Annu Rev Microbiol 57:395–418 [View Article][PubMed]
    [Google Scholar]
  12. Imlay J. A. ( 2008). Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77:755–776 [View Article][PubMed]
    [Google Scholar]
  13. Korshunov S., Imlay J. A. ( 2006). Detection and quantification of superoxide formed within the periplasm of Escherichia coli . J Bacteriol 188:6326–6334 [View Article][PubMed]
    [Google Scholar]
  14. Korshunov S., Imlay J. A. ( 2010). Two sources of endogenous hydrogen peroxide in Escherichia coli . Mol Microbiol 75:1389–1401 [View Article][PubMed]
    [Google Scholar]
  15. McCord J. M., Fridovich I. ( 1969). Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055[PubMed]
    [Google Scholar]
  16. Messner K. R., Imlay J. A. ( 2002). Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase. J Biol Chem 277:42563–42571 [View Article][PubMed]
    [Google Scholar]
  17. Pan N., Imlay J. A. ( 2001). How does oxygen inhibit central metabolism in the obligate anaerobe Bacteroides thetaiotaomicron . Mol Microbiol 39:1562–1571 [View Article][PubMed]
    [Google Scholar]
  18. Park S., You X., Imlay J. A. ( 2005). Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx mutants of Escherichia coli . Proc Natl Acad Sci U S A 102:9317–9322 [View Article][PubMed]
    [Google Scholar]
  19. Parsonage D., Karplus P. A., Poole L. B. ( 2008). Substrate specificity and redox potential of AhpC, a bacterial peroxiredoxin. Proc Natl Acad Sci U S A 105:8209–8214 [View Article][PubMed]
    [Google Scholar]
  20. Privalle C. T., Gregory E. M. ( 1979). Superoxide dismutase and O2 lethality in Bacteroides fragilis . J Bacteriol 138:139–145[PubMed]
    [Google Scholar]
  21. Rocha E. R., Smith C. J. ( 1999). Role of the alkyl hydroperoxide reductase (ahpCF) gene in oxidative stress defense of the obligate anaerobe Bacteroides fragilis . J Bacteriol 181:5701–5710[PubMed]
    [Google Scholar]
  22. Rocha E. R., Selby T., Coleman J. P., Smith C. J. ( 1996). Oxidative stress response in an anaerobe, Bacteroides fragilis: a role for catalase in protection against hydrogen peroxide. J Bacteriol 178:6895–6903[PubMed]
    [Google Scholar]
  23. 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 [View Article][PubMed]
    [Google Scholar]
  24. Sund C. J., Rocha E. R., Tzianabos A. O., Wells W. G., Gee J. M., Reott M. A., O’Rourke D. P., Smith C. J. ( 2008). The Bacteroides fragilis transcriptome response to oxygen and H2O2: the role of OxyR and its effect on survival and virulence. Mol Microbiol 67:129–142 [View Article][PubMed]
    [Google Scholar]
  25. Tang Y. P., Malamy M. H. ( 2000). Isolation of Bacteroides fragilis mutants with in vivo growth defects by using Tn4400′, a modified Tn4400 transposition system, and a new screening method. Infect Immun 68:415–419 [View Article][PubMed]
    [Google Scholar]
  26. Tang Y. P., Dallas M. M., Malamy M. H. ( 1999). Characterization of the Batl (Bacteroides aerotolerance) operon in Bacteroides fragilis: isolation of a B. fragilis mutant with reduced aerotolerance and impaired growth in in vivo model systems. Mol Microbiol 32:139–149 [View Article][PubMed]
    [Google Scholar]
  27. Thompson J. S., Malamy M. H. ( 1990). Sequencing the gene for an imipenem-cefoxitin-hydrolyzing enzyme (CfiA) from Bacteroides fragilis TAL2480 reveals strong similarity between CfiA and Bacillus cereus beta-lactamase II. J Bacteriol 172:2584–2593[PubMed]
    [Google Scholar]
  28. Woodcock D. M., Crowther P. J., Doherty J., Jefferson S., DeCruz E., Noyer-Weidner M., Smith S. S., Michael M. Z., Graham M. W. ( 1989). Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res 17:3469–3478 [View Article][PubMed]
    [Google Scholar]
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