1887

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
2021-10-21
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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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