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Volume 160, Issue 2

Expression of a bacterial catalase in a strictly anaerobic methanogen significantly increases tolerance to hydrogen peroxide but not oxygen Free

Abstract

Haem-dependent catalase is an antioxidant enzyme that degrades HO, producing HO and O, and is common in aerobes. Catalase is present in some strictly anaerobic methane-producing archaea (methanogens), but the importance of catalase to the antioxidant system of methanogens is poorly understood. We report here that a survey of the sequenced genomes of methanogens revealed that the majority of species lack genes encoding catalase. Moreover, is a methanogen capable of synthesizing haem and encodes haem-dependent catalase in its genome; yet, cells lack detectable catalase activity. However, inducible expression of the haem-dependent catalase from (EcKatG) in the chromosome of resulted in a 100-fold increase in the endogenous catalase activity compared with uninduced cells. The increased catalase activity conferred a 10-fold increase in the resistance of EcKatG-induced cells to HO compared with uninduced cells. The EcKatG-induced cells were also able to grow when exposed to levels of HO that inhibited or killed uninduced cells. However, despite the significant increase in catalase activity, growth studies revealed that EcKatG-induced cells did not exhibit increased tolerance to O compared with uninduced cells. These results support the lack of catalase in the majority of methanogens, since methanogens are more likely to encounter O rather than high concentrations of HO in the natural environment. Catalase appears to be a minor component of the antioxidant system in methanogens, even those that are aerotolerant, including . Importantly, the experimental approach used here demonstrated the feasibility of engineering beneficial traits, such as HO tolerance, in methanogens.

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2014-02-01
2024-04-19
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References

  1. Angel R., Matthies D., Conrad R. ( 2011). Activation of methanogenesis in arid biological soil crusts despite the presence of oxygen. PLoS ONE 6:e20453 [View Article][PubMed]
     [Google Scholar]
  2. Angel R., Claus P., Conrad R. ( 2012). Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J 6:847–862 [View Article][PubMed]
     [Google Scholar]
  3. Bradford M. M. ( 1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254 [View Article][PubMed]
     [Google Scholar]
  4. Brioukhanov A. L., Netrusov A. I. ( 2004). Catalase and superoxide dismutase: distribution, properties, and physiological role in cells of strict anaerobes. Biochemistry (Mosc) 69:949–962 [View Article][PubMed]
     [Google Scholar]
  5. Brioukhanov A. L., Netrusov A. I. ( 2012). The positive effect of exogenous hemin on a resistance of strict anaerobic archaeon Methanobrevibacter arboriphilus to oxidative stresses. Curr Microbiol 65:375–383 [View Article][PubMed]
     [Google Scholar]
  6. Brioukhanov A. L., Netrusov A. I., Eggen R. I. ( 2006). The catalase and superoxide dismutase genes are transcriptionally up-regulated upon oxidative stress in the strictly anaerobic archaeon Methanosarcina barkeri. Microbiology 152:1671–1677 [View Article][PubMed]
     [Google Scholar]
  7. Carpena X., Loprasert S., Mongkolsuk S., Switala J., Loewen P. C., Fita I. ( 2003). Catalase-peroxidase KatG of Burkholderia pseudomallei at 1.7 Å resolution. J Mol Biol 327:475–489 [View Article][PubMed]
     [Google Scholar]
  8. Colt J. ( 1984). Computation of Dissolved Gas Concentrations in Water as Functions of Temperature, Salinity, and Pressure Bethesda, MD: American Fisheries Society;
     [Google Scholar]
  9. Cruz F., Ferry J. G. ( 2006). Interaction of iron-sulfur flavoprotein with oxygen and hydrogen peroxide. Biochim Biophys Acta 1760:858–864 [View Article][PubMed]
     [Google Scholar]
  10. Díaz A., Loewen P. C., Fita I., Carpena X. ( 2012). Thirty years of heme catalases structural biology. Arch Biochem Biophys 525:102–110 [View Article][PubMed]
     [Google Scholar]
  11. Ferry J. G., Lessner D. J. ( 2008). Methanogenesis in marine sediments. Ann N Y Acad Sci 1125:147–157 [View Article][PubMed]
     [Google Scholar]
  12. Fetzer S., Bak F., Conrad R. ( 1993). Sensitivity of methanogenic bacteria from paddy soil to oxygen and desiccation. FEMS Microbiol Ecol 12:107–115 [View Article]
     [Google Scholar]
  13. Guss A. M., Rother M., Zhang J. K., Kulkkarni G., Metcalf W. W. ( 2008). New methods for tightly regulated gene expression and highly efficient chromosomal integration of cloned genes for Methanosarcina species. Archaea 2:193–203 [View Article][PubMed]
     [Google Scholar]
  14. Guss A. M., Kulkarni G., Metcalf W. W. ( 2009). Differences in hydrogenase gene expression between Methanosarcina acetivorans and Methanosarcina barkeri. J Bacteriol 191:2826–2833 [View Article][PubMed]
     [Google Scholar]
  15. Horne A. J., Lessner D. J. ( 2013). Assessment of the oxidant tolerance of Methanosarcina acetivorans. FEMS Microbiol Lett 343:13–19 [View Article][PubMed]
     [Google Scholar]
  16. Imlay J. A. ( 2002). How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis. Adv Microb Physiol 46:111–153 [View Article][PubMed]
     [Google Scholar]
  17. Imlay J. A. ( 2003). Pathways of oxidative damage. Annu Rev Microbiol 57:395–418 [View Article][PubMed]
     [Google Scholar]
  18. Jenney F. E. Jr, Verhagen M. F., Cui X., Adams M. W. ( 1999). Anaerobic microbes: oxygen detoxification without superoxide dismutase. Science 286:306–309 [View Article][PubMed]
     [Google Scholar]
  19. Lessner D. J., Li L., Li Q., Rejtar T., Andreev V. P., Reichlen M., Hill K., Moran J. J., Karger B. L., Ferry J. G. ( 2006). An unconventional pathway for reduction of CO2 to methane in CO-grown Methanosarcina acetivorans revealed by proteomics. Proc Natl Acad Sci U S A 103:17921–17926 [View Article][PubMed]
     [Google Scholar]
  20. Lessner D. J., Lhu L., Wahal C. S., Ferry J. G. ( 2010). An engineered methanogenic pathway derived from the domains Bacteria and Archaea. . mBiol 1:e000243-10
     [Google Scholar]
  21. Li Q., Li L., Rejtar T., Karger B. L., Ferry J. G. ( 2005a). Methanosarcina acetivorans Part II: comparison of protein levels in acetate- and methanol-grown cells. J Proteome Res 4:129–135 [View Article][PubMed]
     [Google Scholar]
  22. Li Q., Li L., Rejtar T., Karger B. L., Ferry J. G. ( 2005b). Methanosarcina acetivorans Part I: an expanded view of the biology of the cell. J Proteome Res 4:112–128 [View Article][PubMed]
     [Google Scholar]
  23. 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 [View Article][PubMed]
     [Google Scholar]
  24. Passardi F., Zamocky M., Favet J., Jakopitsch C., Penel C., Obinger C., Dunand C. ( 2007). Phylogenetic distribution of catalase-peroxidases: are there patches of order in chaos. Gene 397:101–113 [View Article][PubMed]
     [Google Scholar]
  25. Shima S., Netrusov A., Sordel M., Wicke M., Hartmann G. C., Thauer R. K. ( 1999). Purification, characterization, and primary structure of a monofunctional catalase from Methanosarcina barkeri.. Arch Microbiol 171:317–323 [View Article][PubMed]
     [Google Scholar]
  26. Shima S., Sordel-Klippert M., Brioukhanov A., Netrusov A., Linder D., Thauer R. K. ( 2001). Characterization of a heme-dependent catalase from Methanobrevibacter arboriphilus. Appl Environ Microbiol 67:3041–3045 [View Article][PubMed]
     [Google Scholar]
  27. Sowers K. R., Baron S. F., Ferry J. G. ( 1984). Methanosarcina acetivorans sp. nov., an acetotrophic methane-producing bacterium isolated from marine sediments. Appl Environ Microbiol 47:971–978[PubMed]
     [Google Scholar]
  28. Thauer R. K., Kaster A. K., Seedorf H., Buckel W., Hedderich R. ( 2008). Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6:579–591 [View Article][PubMed]
     [Google Scholar]
  29. Tholen A., Pester M., Brune A. ( 2007). Simultaneous methanogenesis and oxygen reduction by Methanobrevibacter cuticularis at low oxygen fluxes. FEMS Microbiol Ecol 62:303–312 [View Article][PubMed]
     [Google Scholar]
  30. Zamocky M., Furtmüller P. G., Obinger C. ( 2008). Evolution of catalases from bacteria to humans. Antioxid Redox Signal 10:1527–1548 [View Article][PubMed]
     [Google Scholar]
  31. Zámocký M., Gasselhuber B., Furtmüller P. G., Obinger C. ( 2012). Molecular evolution of hydrogen peroxide degrading enzymes. Arch Biochem Biophys 525:131–144 [View Article][PubMed]
     [Google Scholar]
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Expression of a bacterial catalase in a strictly anaerobic methanogen significantly increases tolerance to hydrogen peroxide but not oxygen
Microbiology 160, 270 (2014); https://doi.org/10.1099/mic.0.070763-0
/content/journal/micro/10.1099/mic.0.070763-0
/content/journal/micro/10.1099/mic.0.070763-0
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