Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II)

Samuel M. Webb, Gregory J. Dick, John R. Bargar, Bradley Tebo

Research output: Contribution to journalArticle

206 Citations (Scopus)

Abstract

Bacterial oxidation of Mn(II) to Mn(IV) is believed to drive the oxidative segment of the global biogeochemical Mn cycle and regulates the concentration of dissolved Mn(II) in the oceanic water column, where it is a critical nutrient for planktonic primary productivity. Mn(II) oxidizing activity is expressed by numerous phylogenetically diverse bacteria and fungi, suggesting that it plays a fundamental and ubiquitous role in the environment. This important redox system is believed to be driven by an enzyme or enzyme complex involving a multicopper oxidase, although the biochemical mechanism has never been conclusively demonstrated. Here, we show that Mn(II) oxidation by spores of the marine Bacillus sp. strain SG-1 is a result of two sequential one-step electron transfer processes, both requiring the putative multicopper oxidase, MnxG, in which Mn(III) is a transient intermediate. A kinetic model of the oxidation pathway is presented, which shows that the Mn(II) to Mn(III) step is the rate-limiting step. Thus, oxidation of Mn(II) appears to involve a unique multicopper oxidase system capable of the overall two-electron oxidation of its substrate. This enzyme system may serve as a source for environmental Mn(III), a strong oxidant and competitor for siderophorebound Fe(III) in nutrient-limited environments. That metabolically dormant spores catalyze an important biogeochemical process intimately linked to the C, N, Fe, and S cycles requires us to rethink the role of spores in the environment.

Original languageEnglish (US)
Pages (from-to)5558-5563
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume102
Issue number15
DOIs
StatePublished - Apr 12 2005
Externally publishedYes

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Spores
Oxidoreductases
Enzymes
Electrons
Food
Oxidants
Bacillus
Oxidation-Reduction
Fungi
Bacteria
Water

Keywords

  • Kinetics
  • Multicopper oxidase
  • Spores
  • X-ray absorption near-edge spectroscopy

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II). / Webb, Samuel M.; Dick, Gregory J.; Bargar, John R.; Tebo, Bradley.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 102, No. 15, 12.04.2005, p. 5558-5563.

Research output: Contribution to journalArticle

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AB - Bacterial oxidation of Mn(II) to Mn(IV) is believed to drive the oxidative segment of the global biogeochemical Mn cycle and regulates the concentration of dissolved Mn(II) in the oceanic water column, where it is a critical nutrient for planktonic primary productivity. Mn(II) oxidizing activity is expressed by numerous phylogenetically diverse bacteria and fungi, suggesting that it plays a fundamental and ubiquitous role in the environment. This important redox system is believed to be driven by an enzyme or enzyme complex involving a multicopper oxidase, although the biochemical mechanism has never been conclusively demonstrated. Here, we show that Mn(II) oxidation by spores of the marine Bacillus sp. strain SG-1 is a result of two sequential one-step electron transfer processes, both requiring the putative multicopper oxidase, MnxG, in which Mn(III) is a transient intermediate. A kinetic model of the oxidation pathway is presented, which shows that the Mn(II) to Mn(III) step is the rate-limiting step. Thus, oxidation of Mn(II) appears to involve a unique multicopper oxidase system capable of the overall two-electron oxidation of its substrate. This enzyme system may serve as a source for environmental Mn(III), a strong oxidant and competitor for siderophorebound Fe(III) in nutrient-limited environments. That metabolically dormant spores catalyze an important biogeochemical process intimately linked to the C, N, Fe, and S cycles requires us to rethink the role of spores in the environment.

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