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Formation of manganese oxides by bacterially generated superoxide

Nature Geoscience volume 4, pages 9598 (2011) | Download Citation

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Abstract

Manganese oxide minerals are among the strongest sorbents and oxidants in the environment. The formation of these minerals controls the fate of contaminants, the degradation of recalcitrant carbon, the cycling of nutrients and the activity of anaerobic-based metabolisms1,2,3. Oxidation of soluble manganese(II) ions to manganese(III/IV) oxides has been primarily attributed to direct enzymatic oxidation by microorganisms. However, the physiological reason for this process remains unknown. Here we assess the ability of a common species of marine bacteria—Roseobacter sp. AzwK-3b—to oxidize manganese(II) in the presence of chemical and biological inhibitors. We show that Roseobacter AzwK-3b oxidizes manganese(II) by producing the strong and versatile redox reactant superoxide. The oxidation of manganese(II), and concomitant production of manganese oxides, was inhibited in both the light and dark in the presence of enzymes and metals that scavenge superoxide. Oxidation was also inhibited by various proteases, enzymes that break down bacterial proteins, confirming that the superoxide was bacterially generated. We conclude that bacteria can oxidize manganese(II) indirectly, through the enzymatic generation of extracellular superoxide radicals. We suggest that dark bacterial production of superoxide may be a driving force in metal cycling and mineralization in the environment.

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References

  1. 1.

    , & Occurrence and mechanisms of microbial oxidation of manganese. Adv. Appl. Microbiol. 33, 279–318 (1988).

  2. 2.

    , , & Geomicrobiology of manganese(II) oxidation. Trends Microbiol. 13, 421–428 (2005).

  3. 3.

    , , , & Reviews in Mineralogy Vol. 35, 225–266 (The Mineralogical Society ofAmerica, 1997).

  4. 4.

    & Is dissolved Mn(II) being oxidized by O2 in absence of Mn-bacteria or surface catalysts. Geochim. Et Cosmochim. Acta 48, 1571–1573 (1984).

  5. 5.

    & Manganese(II) oxidation-kinetics on metal-oxide surfaces. J. Colloid Interface Sci. 129, 63–77 (1989).

  6. 6.

    & Numerical dominance of a group of marine bacteria in the alpha-subclass of the class Proteobacteria in coastal seawater. Appl. Environ. Microbiol. 63, 4237–4242 (1997).

  7. 7.

    , & Diverse Mn(II)-oxidizing bacteria isolated from submarine basalts at Loihi Seamount. Geomicrobiol. J. 22, 127–139 (2005).

  8. 8.

    , & Overview of the marine Roseobacter lineage. Appl. Environ. Microbiol. 71, 5665–5677 (2005).

  9. 9.

    , , & New method for the determination of extracellular production of superoxide by marine phytoplankton using the chemiluminescence probes MCLA and red-CLA. Limnol. Oceanogr.-Meth. 7, 682–692 (2009).

  10. 10.

    & The scavenging of superoxide radical by manganous complexes: In vitro. Arch. Biochem. Biophys. 214, 452–463 (1982).

  11. 11.

    , , & Manganous phosphate acts as a superoxide dismutase. J. Am. Chem. Soc. 130, 4604 (2008).

  12. 12.

    & Coupled photochemical and enzymatic Mn(II) oxidation pathways of a planktonic Roseobacter-like bacterium. Appl. Environ. Microbiol. 72, 3543–3549 (2006).

  13. 13.

    , , & Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II). Proc. Natl Acad. Sci. USA102, 5558–5563 (2005).

  14. 14.

    et al. Stimulation of Mn(II) oxidation in Leptothrix discophora SS-1 by Cu2+ and sequence analysis of the region flanking the gene encoding putative multicopper oxidase MofA. Geomicrobiol. J. 17, 25–33 (2000).

  15. 15.

    , & Chemistry of the superoxide radical (O2) in seawater: Reactions with inorganic copper complexes. J. Phys. Chem. A 102, 5693–5700 (1998).

  16. 16.

    , & Chemistry of superoxide radical in seawater: Reactions with organic Cu complexes. Environ. Sci. Technol. 34, 1036–1042 (2000).

  17. 17.

    , , & Effect of yeast extract on speciation and bioavailability of nickel and cobalt in anaerobic bioreactors. Biotechnol. Bioeng. 82, 134–142 (2003).

  18. 18.

    , & NOX family NADPH oxidases: Not just in mammals. Biochimie 89, 1107–1112 (2007).

  19. 19.

    et al. Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol. Microbiol. 42, 729–740 (2001).

  20. 20.

    , , , & Quinone reduction by the Na+-translocating NADH dehydrogenase promotes extracellular superoxide production in Vibrio cholerae. J. Bacteriol. 189, 3902–3908 (2007).

  21. 21.

    & Detection and quantification of superoxide formed within the periplasm of Escherichia coli. J. Bacteriol. 188, 6326–6334 (2006).

  22. 22.

    & In vitro studies indicate a quinone is involved in bacterial Mn(II) oxidation. Arch. Microbiol. 189, 59–69 (2008).

  23. 23.

    et al. Iron requirement for Mn(II) oxidation by Leptothrix discophora SS-1. Appl. Environment. Microbiol. 75, 1229–1235 (2009).

  24. 24.

    & Photoreduction of manganese oxides in seawater. Mar. Chem. 46, 133–152 (1994).

  25. 25.

    & Iron reduction by photoproduced superoxide in seawater. Mar. Chem. 50, 93–102 (1995).

  26. 26.

    , & Dark production of hydrogen peroxide in the Gulf of Alaska. Limnol. Oceanogr. 55, 580–588 (2010).

  27. 27.

    , , & Measurement and implications of nonphotochemically generated superoxide in the equatorial Pacific Ocean. Environ. Sci. Technol. 42, 2387–2393 (2008).

  28. 28.

    , , , & Extracellular production of superoxide by marine diatoms: Contrasting effects on iron redox chemistry and bioavailability. Limnol. Oceanogr. 50, 1172–1180 (2005).

  29. 29.

    , & Kinetic properties of Cu, Zn-superoxide dismutase as a function of metal content—order restored. Free Radical Biol. Med. 41, 937–941 (2006).

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Acknowledgements

We thank A. Knoll, D. Johnston and C. Santelli for helpful comments and discussions. This work was supported by the Geobiology and Low-Temperature Geochemistry Program at the National Science Foundation under grants EAR-0817653 and EAR-1024817/1025077 and by the Radcliffe Institute for Advanced Study at Harvard University.

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Affiliations

  1. School of Engineering and Applied Sciences, Harvard University, 29 Oxford Street, Cambridge, Massachusetts 02138, USA

    • D. R. Learman
    • , A. I. Vazquez-Rodriguez
    •  & C. M. Hansel
  2. Department of Chemistry & Geochemistry, Colorado School of Mines, Golden, Colorado 80401, USA

    • B. M. Voelker

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Contributions

D.R.L. and C.M.H. designed experiments and analysed data. Experiments were conducted by D.R.L. and A.I.V-R. B.M.V. conducted model components and assisted in experimental interpretation. The manuscript was written by D.R.L. with contributions from C.M.H. and B.M.V.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to C. M. Hansel.

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https://doi.org/10.1038/ngeo1055

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