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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:
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. Fri . "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},
journal = {Nature Communications},
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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Coupled biotic–abiotic Mn(II) oxidation pathway mediates the formation and structural evolution of biogenic Mn oxides
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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

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  • Journal of the American Chemical Society, Vol. 137, Issue 12
  • DOI: 10.1021/jacs.5b00507

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

  • Xu, Yongtao; Rahman, Noorsaadah A. B. D.; Othman, Rozana
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Confirmation of intersubunit connectivity and topology of designed protein complexes by native MS
journal, January 2018

  • Sahasrabuddhe, Aniruddha; Hsia, Yang; Busch, Florian
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 6
  • DOI: 10.1073/pnas.1713646115

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

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

  • Harvey, Sophie R.; Seffernick, Justin T.; Quintyn, Royston S.
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 17
  • DOI: 10.1073/pnas.1817632116