skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [1];  [2];  [1]
  1. Oregon Health and Science Univ., Beaverton, OR (United States)
  2. Univ. of Washington, Seattle, WA (United States)
+ Show Author Affiliations

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.

Research Organization:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-76SF00515
OSTI ID:
1128890
Report Number(s):
SLAC-REPRINT-2014-043
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 110, Issue 29; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 113 works
Citation information provided by
Web of Science

References (28)

The oxidation of chlorophenols adsorbed to manganese oxide surfaces journal April 1989
Reduction and dissolution of manganese(III) and manganese(IV) oxides by organics. 1. Reaction with hydroquinone journal June 1984
Reduction and dissolution of manganese(III) and manganese(IV) oxides by organics: 2. Survey of the reactivity of organics journal August 1984
BIOGENIC MANGANESE OXIDES: Properties and Mechanisms of Formation journal May 2004
Characterization of Mn oxides in cemented streambed crusts from Pinal Creek, Arizona, U.S.A., and in hot-spring deposits from Yuno-Taki Falls, Hokkaido, Japan journal April 2002
Bacterial Variability within an Iron-Silica-Manganese-rich Hydrothermal Mound Located Off-axis at the Cleft Segment, Juan de Fuca Ridge journal November 2009
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
Elimination of Manganese(II,III) Oxidation in Pseudomonas putida GB-1 by a Double Knockout of Two Putative Multicopper Oxidase Genes journal November 2012
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
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
Genetic analysis of the marine manganese-oxidizing Bacillus sp. strain SG-1: protoplast transformation, Tn917 mutagenesis, and identification of chromosomal loci involved in manganese oxidation. journal December 1993
Surface architecture of endospores of the Bacillus cereus/anthracis/thuringiensis family at the subnanometer scale journal September 2011
An X-ray structural study of human ceruloplasmin in relation to ferroxidase activity journal August 1997
A Labile Regulatory Copper Ion Lies Near the T1 Copper Site in the Multicopper Oxidase CueO journal June 2003
Multicopper oxidase involvement in both Mn(II) and Mn(III) oxidation during bacterial formation of MnO2 journal August 2012
Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II) journal March 2005
Biotic and abiotic products of Mn(II) oxidation by spores of the marine Bacillus sp. strain SG-1 journal January 2005
Structural Influences of Sodium and Calcium Ions on the Biogenic Manganese Oxides Produced by the Marine Bacillus Sp., Strain SG-1 journal April 2005
Structural characterization of biogenic Mn oxides produced in seawater by the marine bacillus sp. strain SG-1 journal August 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
Natural speciation of Zn at the micrometer scale in a clayey soil using X-ray fluorescence, absorption, and diffraction journal June 2004
Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry journal February 2007
ATHENA , ARTEMIS , HEPHAESTUS : data analysis for X-ray absorption spectroscopy using IFEFFIT journal June 2005

Cited By (16)

Manganese Cycling in the Oceans reference-book December 2019
Oxidative Alkene Cleavage Catalysed by Manganese-Dependent Cupin TM1459 from Thermotoga maritima journal October 2015
Laccases of prokaryotic origin: enzymes at the interface of protein science and protein technology journal January 2015
Surface Induced Dissociation Coupled with High Resolution Mass Spectrometry Unveils Heterogeneity of a 211 kDa Multicopper Oxidase Protein Complex journal January 2018
Microbe–microbe interactions trigger Mn(II)-oxidizing gene expression journal August 2016
Biogenic manganese oxide nanoparticle formation by a multimeric multicopper oxidase Mnx journal September 2017
Mn oxide formation by phototrophs: Spatial and temporal patterns, with evidence of an enzymatic superoxide-mediated pathway journal December 2019
Redox of Fungal Multicopper Oxidase: A Potential Driving Factor for the Silicate Mineral Weathering journal October 2018
Extracellular haem peroxidases mediate Mn(II) oxidation in a marine R oseobacter bacterium via superoxide production : Peroxidases mediate superoxide-based Mn oxidation journal June 2015
Unravelling the one-carbon metabolism of the acetogen S poromusa strain An4 by genome and proteome analysis: Unravelling one-carbon metabolism in Sporomusa An4 journal August 2015
Comparative proteomics of Mn(II)-oxidizing and non-oxidizing R oseobacter clade bacteria reveal an operative manganese transport system but minimal Mn(II)-induced expression of manganese oxidation and antioxidant enzymes : Mn(II) response of the journal May 2014
Insights into microbial involvement in desert varnish formation retrieved from metagenomic analysis: The desert varnish microbiome journal March 2018
Low Mid-Proterozoic atmospheric oxygen levels and the delayed rise of animals journal October 2014
Oxidative Formation and Removal of Complexed Mn(III) by Pseudomonas Species journal April 2018
Evidence that fodipir (DPDP) binds neurotoxic Pt2+ with a high affinity: An electron paramagnetic resonance study journal November 2019
Surface Mn(II) oxidation actuated by a multicopper oxidase in a soil bacterium leads to the formation of manganese oxide minerals journal June 2015

Similar Records

Biogenic manganese oxide nanoparticle formation by a multimeric multicopper oxidase Mnx
Journal Article · Fri Sep 29 00:00:00 EDT 2017 · Nature Communications · OSTI ID:1128890
+5 more
Crystal structures of a dodecameric multicopper oxidase from Marinithermus hydrothermalis
Journal Article · Wed Sep 29 00:00:00 EDT 2021 · Acta Crystallographica. Section D. Structural Biology · OSTI ID:1128890
+1 more
Surface Induced Dissociation Coupled with High Resolution Mass Spectrometry Unveils Heterogeneity of a 211 kDa Multicopper Oxidase Protein Complex
Journal Article · Wed Jan 31 00:00:00 EST 2018 · Journal of the American Society for Mass Spectrometry · OSTI ID:1128890
+3 more

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
biomineralization
biogeochemistry
microbial redox
metal cycling