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Title: Biogenic manganese oxide nanoparticle formation by a multimeric multicopper oxidase Mnx

Abstract

Bacteria that produce Mn oxides are extraordinarily skilled engineers of nanomaterials that contribute significantly to global biogeochemical cycles. Their enzyme-based reaction mechanisms may be genetically tailored for environmental remediation applications or bioenergy production. However, significant challenges exist for structural characterization of the enzymes responsible for biomineralization. The active Mn oxidase, Mnx, in Bacillus sp. PL-12 is a complex composed of a multicopper oxidase (MCO), MnxG, and two accessory proteins MnxE and MnxF. MnxG shares sequence similarity with other, structurally characterized MCOs. However, MnxE and MnxF have no similarity to any characterized proteins. The ~200 kDa complex has been recalcitrant to crystallization, so its structure is unknown. In this study, native mass spectrometry defines the subunit topology and copper binding of the Mnx complex, while high resolution electron microscopy visualizes the protein and nascent Mn oxide minerals. Furthermore, these data provide critical structural information for conceptualizing how Mnx produces nanoparticulate Mn oxides.

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3];  [3];  [2];  [2];  [2];  [1]
  1. Oregon Health & Science Univ., Portland, OR (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. The Ohio State Univ., Columbus, OH (United States)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1406743
Report Number(s):
PNNL-SA-124759
Journal ID: ISSN 2041-1723; 48903; KP1704020
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Environmental Molecular Sciences Laboratory

Citation Formats

Romano, Christine A., Zhou, Mowei, Song, Yang, Wysocki, Vicki H., Dohnalkova, Alice C., Kovarik, Libor, Pasa-Tolic, Ljiljana, and Tebo, Bradley M. Biogenic manganese oxide nanoparticle formation by a multimeric multicopper oxidase Mnx. United States: N. p., 2017. Web. doi:10.1038/s41467-017-00896-8.
Romano, Christine A., Zhou, Mowei, Song, Yang, Wysocki, Vicki H., Dohnalkova, Alice C., Kovarik, Libor, Pasa-Tolic, Ljiljana, & Tebo, Bradley M. Biogenic manganese oxide nanoparticle formation by a multimeric multicopper oxidase Mnx. United States. https://doi.org/10.1038/s41467-017-00896-8
Romano, Christine A., Zhou, Mowei, Song, Yang, Wysocki, Vicki H., Dohnalkova, Alice C., Kovarik, Libor, Pasa-Tolic, Ljiljana, and Tebo, Bradley M. 2017. "Biogenic manganese oxide nanoparticle formation by a multimeric multicopper oxidase Mnx". United States. https://doi.org/10.1038/s41467-017-00896-8. https://www.osti.gov/servlets/purl/1406743.
@article{osti_1406743,
title = {Biogenic manganese oxide nanoparticle formation by a multimeric multicopper oxidase Mnx},
author = {Romano, Christine A. and Zhou, Mowei and Song, Yang and Wysocki, Vicki H. and Dohnalkova, Alice C. and Kovarik, Libor and Pasa-Tolic, Ljiljana and Tebo, Bradley M.},
abstractNote = {Bacteria that produce Mn oxides are extraordinarily skilled engineers of nanomaterials that contribute significantly to global biogeochemical cycles. Their enzyme-based reaction mechanisms may be genetically tailored for environmental remediation applications or bioenergy production. However, significant challenges exist for structural characterization of the enzymes responsible for biomineralization. The active Mn oxidase, Mnx, in Bacillus sp. PL-12 is a complex composed of a multicopper oxidase (MCO), MnxG, and two accessory proteins MnxE and MnxF. MnxG shares sequence similarity with other, structurally characterized MCOs. However, MnxE and MnxF have no similarity to any characterized proteins. The ~200 kDa complex has been recalcitrant to crystallization, so its structure is unknown. In this study, native mass spectrometry defines the subunit topology and copper binding of the Mnx complex, while high resolution electron microscopy visualizes the protein and nascent Mn oxide minerals. Furthermore, these data provide critical structural information for conceptualizing how Mnx produces nanoparticulate Mn oxides.},
doi = {10.1038/s41467-017-00896-8},
url = {https://www.osti.gov/biblio/1406743}, journal = {Nature Communications},
issn = {2041-1723},
number = 1,
volume = 8,
place = {United States},
year = {Fri Sep 29 00:00:00 EDT 2017},
month = {Fri Sep 29 00:00:00 EDT 2017}
}

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Cited by: 51 works
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Works referenced in this record:

Direction-Specific Interactions Control Crystal Growth by Oriented Attachment
journal, May 2012


Mn(II) Binding and Subsequent Oxidation by the Multicopper Oxidase MnxG Investigated by Electron Paramagnetic Resonance Spectroscopy
journal, August 2015


Photochemical Water Oxidation by Crystalline Polymorphs of Manganese Oxides: Structural Requirements for Catalysis
journal, February 2013


Function and molecular evolution of multicopper blue proteins
journal, August 2005


Superoxide dismutases: Ancient enzymes and new insights
journal, November 2011


Nonspecific aggregation in native electrokinetic nanoelectrospray ionization
journal, September 2017


Shall We Dance? How a Multicopper Oxidase Chooses Its Electron Transfer Partner
journal, September 2007


Bacterial enzymes involved in lignin degradation
journal, October 2016


Principles of assembly reveal a periodic table of protein complexes
journal, December 2015


Computational identification of self-inhibitory peptides from envelope proteins
journal, June 2012


Metal Sulfide Cluster Complexes and their Biogeochemical Importance in the Environment
journal, October 2005


Coupled biotic–abiotic Mn(II) oxidation pathway mediates the formation and structural evolution of biogenic Mn oxides
journal, October 2011


Ligand binding and unfolding of tryptophan synthase revealed by ion mobility-tandem mass spectrometry employing collision and surface induced dissociation
journal, March 2013


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


Heterologous Expression and Characterization of the Manganese-Oxidizing Protein from Erythrobacter sp. Strain SD21
journal, August 2014


Surface Induced Dissociation: Dissecting Noncovalent Protein Complexes in the Gas phase
journal, February 2014


Manganous Phosphate Acts as a Superoxide Dismutase
journal, April 2008


Multicopper oxidases: a workshop on copper coordination chemistry, electron transfer, and metallophysiology
journal, October 2009


Mn(II) Oxidation Is Catalyzed by Heme Peroxidases in "Aurantimonas manganoxydans" Strain SI85-9A1 and Erythrobacter sp. Strain SD-21
journal, May 2009


Water-oxidation catalysis by manganese in a geochemical-like cycle
journal, May 2011


The I-TASSER Suite: protein structure and function prediction
journal, December 2014


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


Mineralization in Ferritin: An Efficient Means of Iron Storage
journal, June 1999


NIH Image to ImageJ: 25 years of image analysis
journal, June 2012


Mn(II,III) oxidation and MnO2 mineralization by an expressed bacterial multicopper oxidase
journal, July 2013


Fungal laccases – occurrence and properties
journal, March 2006


Shall We Dance? How A Multicopper Oxidase Chooses Its Electron Transfer Partner
journal, June 2007


Multicopper Oxidases and Oxygenases
journal, January 1996


Identification of a Third Mn(II) Oxidase Enzyme in Pseudomonas putida GB-1
journal, April 2016


Copper incorporation into recombinant CotA laccase from Bacillus subtilis: characterization of fully copper loaded enzymes
journal, October 2007


Non-heme manganese catalase – The ‘other’ catalase
journal, September 2012


Collision-Induced Dissociation of Electrosprayed Protein Complexes: An All-Atom Molecular Dynamics Model with Mobile Protons
journal, May 2016


Multicopper manganese oxidase accessory proteins bind Cu and heme
journal, December 2015


The catalytic center of ferritin regulates iron storage via Fe(II)-Fe(III) displacement
journal, September 2012


Protein Complexes in the Gas Phase:  Technology for Structural Genomics and Proteomics
journal, August 2007


NMR reveals pathway for ferric mineral precursors to the central cavity of ferritin
journal, December 2009


Mn(II,III) oxidation and MnO2 mineralization by an expressed bacterial multicopper oxidase
journal, July 2013


Investigation of intact protein complexes by mass spectrometry
journal, January 2004


Manganous Phosphate Acts as a Superoxide Dismutase
journal, April 2008


Manganese binding and oxidation by spores of a marine bacillus.
journal, January 1982


Metal Sulfide Cluster Complexes and their Biogeochemical Importance in the Environment
journal, October 2005


Mineralization in Ferritin: An Efficient Means of Iron Storage
journal, June 1999


Manganese (Mn) Oxidation Increases Intracellular Mn in Pseudomonas putida GB-1
journal, October 2013


Constraints on superoxide mediated formation of manganese oxides
journal, January 2013


Ligand binding and unfolding of tryptophan synthase revealed by ion mobility-tandem mass spectrometry employing collision and surface induced dissociation
journal, March 2013


Function and molecular evolution of multicopper blue proteins
journal, August 2005


ZDOCK server: interactive docking prediction of protein-protein complexes and symmetric multimers
journal, February 2014


Direction-Specific Interactions Control Crystal Growth by Oriented Attachment
journal, May 2012


Superoxide dismutases: Ancient enzymes and new insights
journal, November 2011


Identification of catalytically important amino acids in human ceruloplasmin by site-directed mutagenesis
journal, May 2002


Manganese oxidation by Leptothrix discophora.
journal, February 1987


Photochemical Water Oxidation by Crystalline Polymorphs of Manganese Oxides: Structural Requirements for Catalysis
journal, February 2013


Bacterial enzymes involved in lignin degradation
journal, October 2016


Protein Oxidation Implicated as the Primary Determinant of Bacterial Radioresistance
journal, March 2007


Water-oxidation catalysis by manganese in a geochemical-like cycle
journal, May 2011


The I-TASSER Suite: protein structure and function prediction
journal, December 2014


Manganese(II) adsorption and oxidation by whole cells and a membrane fraction of Pedomicrobium sp. ACM 3067
journal, March 1999


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


Nature of Activated Manganese Oxide for Oxygen Evolution
journal, November 2015


Multicopper oxidases: a workshop on copper coordination chemistry, electron transfer, and metallophysiology
journal, October 2009


Partial purification and characterization of manganese-oxidizing factors of Pseudomonas fluorescens GB-1.
journal, January 1997


Multicopper manganese oxidase accessory proteins bind Cu and heme
journal, December 2015


Protein Complexes in the Gas Phase: Technology for Structural Genomics and Proteomics
journal, November 2007


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


The catalytic center of ferritin regulates iron storage via Fe(II)-Fe(III) displacement
journal, September 2012


Drilling accurate nanopores for biosensors by energetic multi-wall carbon nanotubes: a molecular dynamics investigation
journal, September 2022


Non-heme manganese catalase – The ‘other’ catalase
journal, September 2012


Protein Complexes in the Gas Phase: Technology for Structural Genomics and Proteomics
journal, November 2007


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


Origin of the Breit-Wigner-Fano lineshape of the tangential G -band feature of metallic carbon nanotubes
journal, March 2001


Diastereoselective Carbonyl Allylation with Simple Olefins Enabled by Palladium Complex-Catalyzed C–H Oxidative Borylation
journal, March 2015


Manganese (Mn) Oxidation Increases Intracellular Mn in Pseudomonas putida GB-1
journal, October 2013


Function and molecular evolution of multicopper blue proteins
journal, August 2005


Manganese-oxidizing photosynthesis before the rise of cyanobacteria
journal, June 2013


Nature of Activated Manganese Oxide for Oxygen Evolution
journal, November 2015


Multicopper Oxidases and Oxygenases
journal, January 1996


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


Coupled biotic–abiotic Mn(II) oxidation pathway mediates the formation and structural evolution of biogenic Mn oxides
journal, October 2011


Collision-Induced Dissociation of Electrosprayed Protein Complexes: An All-Atom Molecular Dynamics Model with Mobile Protons
journal, May 2016


Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria.
journal, January 1981


Manganese and Defenses against Oxygen Toxicity in Lactobacillus plantarum
journal, January 1981


Manganese(II) adsorption and oxidation by whole cells and a membrane fraction of Pedomicrobium sp. ACM 3067
journal, March 1999


NMR reveals pathway for ferric mineral precursors to the central cavity of ferritin
journal, December 2009


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


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


Manganese oxidation by Leptothrix discophora.
journal, February 1987


Towards a mechanistic understanding of carbon stabilization in manganese oxides
journal, July 2015


Protein Oxidation Implicated as the Primary Determinant of Bacterial Radioresistance
journal, March 2007


Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria.
journal, January 1981


Manganese and Defenses against Oxygen Toxicity in Lactobacillus plantarum
journal, January 1981


Manganese binding and oxidation by spores of a marine bacillus.
journal, January 1982


Partial purification and characterization of manganese-oxidizing factors of Pseudomonas fluorescens GB-1.
journal, January 1997


Diastereoselective Carbonyl Allylation with Simple Olefins Enabled by Palladium Complex-Catalyzed C–H Oxidative Borylation
journal, March 2015


Computational identification of self-inhibitory peptides from envelope proteins
journal, June 2012


Works referencing / citing this record:

Plasmid binding to metal oxide nanoparticles inhibited lateral transfer of antibiotic resistance genes
journal, January 2019


Confirmation of intersubunit connectivity and topology of designed protein complexes by native MS
journal, January 2018


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


Relative interfacial cleavage energetics of protein complexes revealed by surface collisions
journal, April 2019