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Formation of manganese oxides by bacterially generated superoxide

Nature Geoscience volume 4, pages 95–98 (2011)Cite this article

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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Figure 1: The ROS superoxide mediates Mn(II) oxidation.
Figure 2: Mn(III) is an intermediate of the Mn(II) oxidation pathway.
Figure 3: Cu slows oxidation of Mn(II) by R. AzwK-3b.
Figure 4: NADH is a substrate used in the enzymatic production of superoxide.

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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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Authors and 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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  1. D. R. Learman
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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.

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Correspondence to C. M. Hansel.

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Learman, D., Voelker, B., Vazquez-Rodriguez, A. et al. Formation of manganese oxides by bacterially generated superoxide. Nature Geosci 4, 95–98 (2011). https://doi.org/10.1038/ngeo1055

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