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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 Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (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:
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. 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, and Tebo, Bradley M. Fri . "Biogenic manganese oxide nanoparticle formation by a multimeric multicopper oxidase Mnx". United States. doi: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},
journal = {Nature Communications},
number = 1,
volume = 8,
place = {United States},
year = {2017},
month = {9}
}

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Works referenced in this record:

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


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

  • Robinson, David M.; Go, Yong Bok; Mui, Michelle
  • Journal of the American Chemical Society, Vol. 135, Issue 9
  • DOI: 10.1021/ja310286h

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


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


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


Nonspecific aggregation in native electrokinetic nanoelectrospray ionization
journal, September 2017

  • Davidson, Kimberly L.; Oberreit, Derek R.; Hogan, Christopher J.
  • International Journal of Mass Spectrometry, Vol. 420
  • DOI: 10.1016/j.ijms.2016.09.013

Inter-relationships of MnO2 precipitation, siderophore–Mn(III) complex formation, siderophore degradation, and iron limitation in Mn(II)-oxidizing bacterial cultures
journal, December 2007

  • Parker, Dorothy L.; Morita, Takami; Mozafarzadeh, Mylene L.
  • Geochimica et Cosmochimica Acta, Vol. 71, Issue 23
  • DOI: 10.1016/j.gca.2007.03.042

Bacterial enzymes involved in lignin degradation
journal, October 2016


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


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

  • Learman, D. R.; Wankel, S. D.; Webb, S. M.
  • Geochimica et Cosmochimica Acta, Vol. 75, Issue 20
  • DOI: 10.1016/j.gca.2011.07.026

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

  • Quintyn, Royston S.; Zhou, Mowei; Dagan, Shai
  • International Journal for Ion Mobility Spectrometry, Vol. 16, Issue 2
  • DOI: 10.1007/s12127-013-0126-4

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

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

  • Huynh, Michael; Shi, Chenyang; Billinge, Simon J. L.
  • Journal of the American Chemical Society, Vol. 137, Issue 47
  • DOI: 10.1021/jacs.5b06382

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

  • Zhou, Mowei; Wysocki, Vicki H.
  • Accounts of Chemical Research, Vol. 47, Issue 4
  • DOI: 10.1021/ar400223t

Manganous Phosphate Acts as a Superoxide Dismutase
journal, April 2008

  • Barnese, Kevin; Gralla, Edith B.; Cabelli, Diane E.
  • Journal of the American Chemical Society, Vol. 130, Issue 14
  • DOI: 10.1021/ja710162n

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


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

  • Yang, Jianyi; Yan, Renxiang; Roy, Ambrish
  • Nature Methods, Vol. 12, Issue 1
  • DOI: 10.1038/nmeth.3213

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

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

  • Chasteen, N. Dennis; Harrison, Pauline M.
  • Journal of Structural Biology, Vol. 126, Issue 3
  • DOI: 10.1006/jsbi.1999.4118

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

  • Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2089

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

  • Butterfield, C. N.; Soldatova, A. V.; Lee, S. -W.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 29
  • DOI: 10.1073/pnas.1303677110

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


Fungal laccases – occurrence and properties
journal, March 2006


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

  • Quintanar, Liliana; Stoj, Christopher; Taylor, Alexander B.
  • Accounts of Chemical Research, Vol. 40, Issue 6
  • DOI: 10.1021/ar600051a

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

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

  • Honarmand Ebrahimi, Kourosh; Bill, Eckhard; Hagedoorn, Peter-Leon
  • Nature Chemical Biology, Vol. 8, Issue 11
  • DOI: 10.1038/nchembio.1071

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

  • Durão, Paulo; Chen, Zhenjia; Fernandes, André T.
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 13, Issue 2
  • DOI: 10.1007/s00775-007-0312-0

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

  • Popa, Vlad; Trecroce, Danielle A.; McAllister, Robert G.
  • The Journal of Physical Chemistry B, Vol. 120, Issue 23
  • DOI: 10.1021/acs.jpcb.6b03035

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

  • Anderson, C. R.; Johnson, H. A.; Caputo, N.
  • Applied and Environmental Microbiology, Vol. 75, Issue 12
  • DOI: 10.1128/AEM.02890-08

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

  • Butterfield, Cristina N.; Tao, Lizhi; Chacón, Kelly N.
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1854, Issue 12
  • DOI: 10.1016/j.bbapap.2015.08.012

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


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


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

  • Geszvain, Kati; Smesrud, Logan; Tebo, Bradley M.
  • Applied and Environmental Microbiology, Vol. 82, Issue 13
  • DOI: 10.1128/AEM.00046-16

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

  • Benesch, Justin L. P.; Ruotolo, Brandon T.; Simmons, Douglas A.
  • Chemical Reviews, Vol. 107, Issue 8
  • DOI: 10.1021/cr068289b

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

  • Nakama, Katherine; Medina, Michael; Lien, Ahn
  • Applied and Environmental Microbiology, Vol. 80, Issue 21
  • DOI: 10.1128/AEM.01873-14

Surface-Induced Dissociation of Homotetramers with D2 Symmetry Yields their Assembly Pathways and Characterizes the Effect of Ligand Binding
journal, May 2015


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

  • Turano, P.; Lalli, D.; Felli, I. C.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 2
  • DOI: 10.1073/pnas.0908082106

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

  • Johnson, J. E.; Webb, S. M.; Thomas, K.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 28
  • DOI: 10.1073/pnas.1305530110

Substrate specificity and copper loading of the manganese-oxidizing multicopper oxidase Mnx from Bacillus sp. PL-12
journal, January 2017

  • Butterfield, Cristina N.; Tebo, Bradley M.
  • Metallomics, Vol. 9, Issue 2
  • DOI: 10.1039/C6MT00239K

Multicopper Oxidases and Oxygenases
journal, January 1996

  • Solomon, Edward I.; Sundaram, Uma M.; Machonkin, Timothy E.
  • Chemical Reviews, Vol. 96, Issue 7
  • DOI: 10.1021/cr950046o

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

  • Heck, Albert J. R.; van den Heuvel, Robert H. H.
  • Mass Spectrometry Reviews, Vol. 23, Issue 5
  • DOI: 10.1002/mas.10081

The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium
journal, May 2013


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


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


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

  • Learman, Deric R.; Voelker, Bettina M.; Madden, Andrew S.
  • Frontiers in Microbiology, Vol. 4
  • DOI: 10.3389/fmicb.2013.00262

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


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

  • Larsen, E. I.; Sly, Lindsay I.; McEwan, Alastair G.
  • Archives of Microbiology, Vol. 171, Issue 4
  • DOI: 10.1007/s002030050708

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


Manganese oxidation by Leptothrix discophora.
journal, February 1987