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Multicopper oxidase involvement in both Mn(II) and Mn(III) oxidation during bacterial formation of MnO2

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Abstract

Global cycling of environmental manganese requires catalysis by bacteria and fungi for MnO2 formation, since abiotic Mn(II) oxidation is slow under ambient conditions. Genetic evidence from several bacteria indicates that multicopper oxidases (MCOs) are required for MnO2 formation. However, MCOs catalyze one-electron oxidations, whereas the conversion of Mn(II) to MnO2 is a two-electron process. Trapping experiments with pyrophosphate (PP), a Mn(III) chelator, have demonstrated that Mn(III) is an intermediate in Mn(II) oxidation when mediated by exosporium from the Mn-oxidizing bacterium Bacillus SG-1. The reaction of Mn(II) depends on O2 and is inhibited by azide, consistent with MCO catalysis. We show that the subsequent conversion of Mn(III) to MnO2 also depends on O2 and is inhibited by azide. Thus, both oxidation steps appear to be MCO-mediated, likely by the same enzyme, which is indicated by genetic evidence to be the MnxG gene product. We propose a model of how the manganese oxidase active site may be organized to couple successive electron transfers to the formation of polynuclear Mn(IV) complexes as precursors to MnO2 formation.

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Abbreviations

HEPES:

4-(2-Hydroxyethyl)piperazine-1-ethanesulfonic acid

MCO:

Multicopper oxidase

PP:

Pyrophosphate

TEM:

Transmission electron microscopy

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Acknowledgments

We thank Radhika Rajendran for developing the linear least squares fitting algorithm in VBA Excel and Satya Chinni for producing some of the exosporium preparations. This work was partially funded by NSF grants OCE-1031200 and OCE-1129553 to BMT.

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Author notes

  1. Oyeyemi F. Oyerinde

    Present address: Celanese Chemicals, 9502 Bayport Blvd., Pasadena, TX, 77507, USA

Authors and Affiliations

  1. Department of Chemistry, University of Washington, Box 351700, Seattle, WA, 98195, USA

    Alexandra V. Soldatova, Oyeyemi F. Oyerinde & Thomas G. Spiro

  2. Division of Environmental and Biomolecular Systems, Oregon Health and Science University, 20000 NW Walker Road, Beaverton, OR, 97006, USA

    Cristina Butterfield & Bradley M. Tebo

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  1. Alexandra V. Soldatova
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  2. Cristina Butterfield
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Correspondence to Thomas G. Spiro.

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Soldatova, A.V., Butterfield, C., Oyerinde, O.F. et al. Multicopper oxidase involvement in both Mn(II) and Mn(III) oxidation during bacterial formation of MnO2 . J Biol Inorg Chem 17, 1151–1158 (2012). https://doi.org/10.1007/s00775-012-0928-6

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  • DOI: https://doi.org/10.1007/s00775-012-0928-6

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