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Title: Mn(II,III) oxidation and MnO2 mineralization by an expressed bacterial multicopper oxidase

Abstract

Reactive Mn(IV) oxide minerals are ubiquitous in the environment and control the bioavailability and distribution of many toxic and essential elements and organic compounds. Their formation is thought to be dependent on microbial enzymes, because spontaneous Mn(II) to Mn(IV) oxidation is slow. Several species of marine Bacillus spores oxidize Mn(II) on their exosporium, the outermost layer of the spore, encrusting them with Mn(IV) oxides. Molecular studies have identified the mnx (Mn oxidation) genes, including mnxG, encoding a putative multicopper oxidase (MCO), as responsible for this two-electron oxidation, a surprising finding because MCOs only catalyze single-electron transfer reactions. Characterization of the enzymatic mechanism has been hindered by the lack of purified protein. By purifying active protein from the mnxDEFG expression construct, we found that the resulting enzyme is a blue (absorption maximum 590 nm) complex containing MnxE, MnxF, and MnxG proteins. Further, by analyzing the Mn(II)- and (III)-oxidizing activity in the presence of a Mn(III) chelator, pyrophosphate, we found that the complex facilitates both electron transfers from Mn(II) to Mn(III) and from Mn(III) to Mn(IV). X-ray absorption spectroscopy of the Mn mineral product confirmed its similarity to Mn(IV) oxides generated by whole spores. Our results demonstrate that Mn oxidation from solublemore » Mn(II) to Mn(IV) oxides is a two-step reaction catalyzed by an MCO-containing complex. Lastly, with the purification of active Mn oxidase, we will be able to uncover its mechanism, broadening our understanding of Mn mineral formation and the bioinorganic capabilities of MCOs.« less

Authors:
 [1];  [2];  [1];  [2];  [1]
  1. Oregon Health and Science Univ., Beaverton, OR (United States)
  2. Univ. of Washington, Seattle, WA (United States)
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1128890
Report Number(s):
SLAC-REPRINT-2014-043
Journal ID: ISSN 0027-8424
Grant/Contract Number:  
AC02-76SF00515
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 110; Journal Issue: 29; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES; biomineralization; biogeochemistry; microbial redox; metal cycling

Citation Formats

Butterfield, Cristina N., Soldatova, Alexandra V., Lee, Sung -Woo, Spiro, Thomas G., and Tebo, Bradley M. Mn(II,III) oxidation and MnO2 mineralization by an expressed bacterial multicopper oxidase. United States: N. p., 2013. Web. doi:10.1073/pnas.1303677110.
Butterfield, Cristina N., Soldatova, Alexandra V., Lee, Sung -Woo, Spiro, Thomas G., & Tebo, Bradley M. Mn(II,III) oxidation and MnO2 mineralization by an expressed bacterial multicopper oxidase. United States. doi:10.1073/pnas.1303677110.
Butterfield, Cristina N., Soldatova, Alexandra V., Lee, Sung -Woo, Spiro, Thomas G., and Tebo, Bradley M. Mon . "Mn(II,III) oxidation and MnO2 mineralization by an expressed bacterial multicopper oxidase". United States. doi:10.1073/pnas.1303677110. https://www.osti.gov/servlets/purl/1128890.
@article{osti_1128890,
title = {Mn(II,III) oxidation and MnO2 mineralization by an expressed bacterial multicopper oxidase},
author = {Butterfield, Cristina N. and Soldatova, Alexandra V. and Lee, Sung -Woo and Spiro, Thomas G. and Tebo, Bradley M.},
abstractNote = {Reactive Mn(IV) oxide minerals are ubiquitous in the environment and control the bioavailability and distribution of many toxic and essential elements and organic compounds. Their formation is thought to be dependent on microbial enzymes, because spontaneous Mn(II) to Mn(IV) oxidation is slow. Several species of marine Bacillus spores oxidize Mn(II) on their exosporium, the outermost layer of the spore, encrusting them with Mn(IV) oxides. Molecular studies have identified the mnx (Mn oxidation) genes, including mnxG, encoding a putative multicopper oxidase (MCO), as responsible for this two-electron oxidation, a surprising finding because MCOs only catalyze single-electron transfer reactions. Characterization of the enzymatic mechanism has been hindered by the lack of purified protein. By purifying active protein from the mnxDEFG expression construct, we found that the resulting enzyme is a blue (absorption maximum 590 nm) complex containing MnxE, MnxF, and MnxG proteins. Further, by analyzing the Mn(II)- and (III)-oxidizing activity in the presence of a Mn(III) chelator, pyrophosphate, we found that the complex facilitates both electron transfers from Mn(II) to Mn(III) and from Mn(III) to Mn(IV). X-ray absorption spectroscopy of the Mn mineral product confirmed its similarity to Mn(IV) oxides generated by whole spores. Our results demonstrate that Mn oxidation from soluble Mn(II) to Mn(IV) oxides is a two-step reaction catalyzed by an MCO-containing complex. Lastly, with the purification of active Mn oxidase, we will be able to uncover its mechanism, broadening our understanding of Mn mineral formation and the bioinorganic capabilities of MCOs.},
doi = {10.1073/pnas.1303677110},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 29,
volume = 110,
place = {United States},
year = {2013},
month = {7}
}

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Works referenced in this record:

The oxidation of chlorophenols adsorbed to manganese oxide surfaces
journal, April 1989

  • Ulrich, Hans Jakob; Stone, Alan T.
  • Environmental Science & Technology, Vol. 23, Issue 4
  • DOI: 10.1021/es00181a006

Reduction and dissolution of manganese(III) and manganese(IV) oxides by organics. 1. Reaction with hydroquinone
journal, June 1984

  • Stone, Alan T.; Morgan, James J.
  • Environmental Science & Technology, Vol. 18, Issue 6
  • DOI: 10.1021/es00124a011

Reduction and dissolution of manganese(III) and manganese(IV) oxides by organics: 2. Survey of the reactivity of organics
journal, August 1984

  • Stone, Alan T.; Morgan, James J.
  • Environmental Science & Technology, Vol. 18, Issue 8
  • DOI: 10.1021/es00126a010

BIOGENIC MANGANESE OXIDES: Properties and Mechanisms of Formation
journal, May 2004


Bacterial Variability within an Iron-Silica-Manganese-rich Hydrothermal Mound Located Off-axis at the Cleft Segment, Juan de Fuca Ridge
journal, November 2009

  • Davis, Richard E.; Stakes, Debra S.; Wheat, C. Geoffrey
  • Geomicrobiology Journal, Vol. 26, Issue 8
  • DOI: 10.1080/01490450902889080

Manganese oxide minerals: Crystal structures and economic and environmental significance
journal, March 1999


Identification and molecular analysis of the Leptothrix discophora SS‐1 mofA gene, a gene putatively encoding a manganese‐oxidizing protein with copper domains
journal, April 1997

  • Corstjens, P. L. A. M.; de Vrind, J. P. M.; Goosen, T.
  • Geomicrobiology Journal, Vol. 14, Issue 2
  • DOI: 10.1080/01490459709378037

Elimination of Manganese(II,III) Oxidation in Pseudomonas putida GB-1 by a Double Knockout of Two Putative Multicopper Oxidase Genes
journal, November 2012

  • Geszvain, Kati; McCarthy, James K.; Tebo, Bradley M.
  • Applied and Environmental Microbiology, Vol. 79, Issue 1
  • DOI: 10.1128/AEM.01850-12

A multicopper oxidase is essential for manganese oxidation and laccase-like activity in Pedomicrobium sp. ACM 3067
journal, April 2007


Manganese(II)-Oxidizing Bacillus Spores in Guaymas Basin Hydrothermal Sediments and Plumes
journal, May 2006


Enzymatic Manganese(II) Oxidation by Metabolically Dormant Spores of Diverse Bacillus Species
journal, February 2002


Localization of Mn(II)-oxidizing activity and the putative multicopper oxidase, MnxG, to the exosporium of the marine Bacillus sp. strain SG-1
journal, December 2002


Oxidation of manganese by spores of a marine bacillus: Kinetic and thermodynamic considerations
journal, August 1986


In situ characterization of Mn(II) oxidation by spores of the marine Bacillus sp. strain SG-1
journal, August 2000


Identification and characterization of a gene cluster involved in manganese oxidation by spores of the marine Bacillus sp. strain SG-1.
journal, June 1996


Surface architecture of endospores of the Bacillus cereus/anthracis/thuringiensis family at the subnanometer scale
journal, September 2011

  • Kailas, L.; Terry, C.; Abbott, N.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 38
  • DOI: 10.1073/pnas.1109419108

Direct Identification of a Bacterial Manganese(II) Oxidase, the Multicopper Oxidase MnxG, from Spores of Several Different Marine Bacillus Species
journal, December 2007

  • Dick, G. J.; Torpey, J. W.; Beveridge, T. J.
  • Applied and Environmental Microbiology, Vol. 74, Issue 5
  • DOI: 10.1128/AEM.01240-07

An X-ray structural study of human ceruloplasmin in relation to ferroxidase activity
journal, August 1997

  • Lindley, P. F.; Card, Graeme; Zaitseva, Irina
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 2, Issue 4
  • DOI: 10.1007/s007750050156

A Labile Regulatory Copper Ion Lies Near the T1 Copper Site in the Multicopper Oxidase CueO
journal, June 2003

  • Roberts, Sue A.; Wildner, Günter F.; Grass, Gregor
  • Journal of Biological Chemistry, Vol. 278, Issue 34
  • DOI: 10.1074/jbc.M302963200

Multicopper oxidase involvement in both Mn(II) and Mn(III) oxidation during bacterial formation of MnO2
journal, August 2012

  • Soldatova, Alexandra V.; Butterfield, Cristina; Oyerinde, Oyeyemi F.
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 17, Issue 8
  • DOI: 10.1007/s00775-012-0928-6

Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II)
journal, March 2005

  • Webb, S. M.; Dick, G. J.; Bargar, J. R.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 15
  • DOI: 10.1073/pnas.0409119102

Biotic and abiotic products of Mn(II) oxidation by spores of the marine Bacillus sp. strain SG-1
journal, January 2005

  • Bargar, John R.; Tebo, Bradley M.; Bergmann, Uwe
  • American Mineralogist, Vol. 90, Issue 1
  • DOI: 10.2138/am.2005.1557

Structural Influences of Sodium and Calcium Ions on the Biogenic Manganese Oxides Produced by the Marine Bacillus Sp., Strain SG-1
journal, April 2005


Structure of Synthetic K-rich Birnessite Obtained by High-Temperature Decomposition of KMnO 4 . I. Two-Layer Polytype from 800 °C Experiment
journal, December 2003

  • Gaillot, Anne-Claire; Flot, David; Drits, Victor A.
  • Chemistry of Materials, Vol. 15, Issue 24
  • DOI: 10.1021/cm021733g

Natural speciation of Zn at the micrometer scale in a clayey soil using X-ray fluorescence, absorption, and diffraction
journal, June 2004

  • Manceau, Alain; Marcus, Matthew A.; Tamura, Nobumichi
  • Geochimica et Cosmochimica Acta, Vol. 68, Issue 11
  • DOI: 10.1016/j.gca.2003.11.021

Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry
journal, February 2007

  • Elias, Joshua E.; Gygi, Steven P.
  • Nature Methods, Vol. 4, Issue 3
  • DOI: 10.1038/nmeth1019

ATHENA , ARTEMIS , HEPHAESTUS : data analysis for X-ray absorption spectroscopy using IFEFFIT
journal, June 2005


    Works referencing / citing this record:

    Surface Induced Dissociation Coupled with High Resolution Mass Spectrometry Unveils Heterogeneity of a 211 kDa Multicopper Oxidase Protein Complex
    journal, January 2018

    • Zhou, Mowei; Yan, Jing; Romano, Christine A.
    • Journal of The American Society for Mass Spectrometry, Vol. 29, Issue 4
    • DOI: 10.1007/s13361-017-1882-x

    Surface Induced Dissociation Coupled with High Resolution Mass Spectrometry Unveils Heterogeneity of a 211 kDa Multicopper Oxidase Protein Complex
    journal, January 2018

    • Zhou, Mowei; Yan, Jing; Romano, Christine A.
    • Journal of The American Society for Mass Spectrometry, Vol. 29, Issue 4
    • DOI: 10.1007/s13361-017-1882-x