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

Alexandra V. Soldatova, Cristina Butterfield, Oyeyemi F. Oyerinde, Bradley Tebo, Thomas G. Spiro

Research output: Contribution to journalArticle

32 Citations (Scopus)

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 O 2 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.

Original languageEnglish (US)
Pages (from-to)1151-1158
Number of pages8
JournalJournal of Biological Inorganic Chemistry
Volume17
Issue number8
DOIs
StatePublished - Dec 2012

Fingerprint

Oxidoreductases
Oxidation
Bacteria
Azides
Electrons
Manganese
Catalysis
Bacilli
Chelating Agents
Fungi
Bacillus
Catalytic Domain
Genes
Enzymes
Experiments

Keywords

  • Bacillus sp. SG-1
  • Biogenic Mn oxides
  • Manganese oxidation
  • Multicopper oxidase

ASJC Scopus subject areas

  • Biochemistry
  • Inorganic Chemistry
  • Medicine(all)

Cite this

Multicopper oxidase involvement in both Mn(II) and Mn(III) oxidation during bacterial formation of MnO2 . / Soldatova, Alexandra V.; Butterfield, Cristina; Oyerinde, Oyeyemi F.; Tebo, Bradley; Spiro, Thomas G.

In: Journal of Biological Inorganic Chemistry, Vol. 17, No. 8, 12.2012, p. 1151-1158.

Research output: Contribution to journalArticle

Soldatova, Alexandra V. ; Butterfield, Cristina ; Oyerinde, Oyeyemi F. ; Tebo, Bradley ; Spiro, Thomas G. / Multicopper oxidase involvement in both Mn(II) and Mn(III) oxidation during bacterial formation of MnO2 . In: Journal of Biological Inorganic Chemistry. 2012 ; Vol. 17, No. 8. pp. 1151-1158.
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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 O 2 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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AB - 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 O 2 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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