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Title: Abiotic protein fragmentation by manganese oxide: Implications for a mechanism to supply soil biota with oligopeptides

Abstract

The ability of plants and microorganisms to take up organic nitrogen in the form of free amino acids and oligopeptides has received increasing attention over the last two decades, yet the mechanisms for the formation of such compounds in soil environments remain poorly understood. We used Nuclear Magnetic Resonance (NMR) and Electron Paramagnetic Resonance (EPR) spectroscopies to distinguish the reaction of a model protein with a pedogenic oxide (Birnessite, MnO2) from its response to a phyllosilicate (Kaolinite). Our data demonstrate that birnessite fragments the model protein while kaolinite does not, resulting in soluble peptides that would be available to soil biota and confirming the existence of an abiotic pathway for the formation of organic nitrogen compounds for direct uptake by plants and microorganisms. The absence of reduced Mn(II) in the solution suggests that birnessite acts as a catalyst rather than an oxidant in this reaction. NMR and EPR spectroscopies are shown to be valuable tools to observe these reactions and capture the extent of protein transformation together with the extent of mineral response.

Authors:
 [1];  [2];  [1];  [1];  [1];  [3]
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  2. Oregon State Univ., Corvallis, OR (United States)
  3. Oregon State Univ., Corvallis, OR (United States); Institut fur Bodenlandschaftforschung, Leibniz Zentrum fur Agrarlandschaftsforschung (ZALF), Muncheberg (Germany)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1254585
Alternate Identifier(s):
OSTI ID: 1580807
Report Number(s):
PNNL-SA-108407
Journal ID: ISSN 0013-936X; 48183; 48364; KP1704020
Grant/Contract Number:  
AC05-76RL01830; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Science and Technology
Additional Journal Information:
Journal Volume: 50; Journal Issue: 7; Journal ID: ISSN 0013-936X
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Environmental Molecular Sciences Laboratory

Citation Formats

Reardon, Patrick N., Chacon, Stephany S., Walter, Eric D., Bowden, Mark E., Washton, Nancy M., and Kleber, Markus W. Abiotic protein fragmentation by manganese oxide: Implications for a mechanism to supply soil biota with oligopeptides. United States: N. p., 2016. Web. doi:10.1021/acs.est.5b04622.
Reardon, Patrick N., Chacon, Stephany S., Walter, Eric D., Bowden, Mark E., Washton, Nancy M., & Kleber, Markus W. Abiotic protein fragmentation by manganese oxide: Implications for a mechanism to supply soil biota with oligopeptides. United States. https://doi.org/10.1021/acs.est.5b04622
Reardon, Patrick N., Chacon, Stephany S., Walter, Eric D., Bowden, Mark E., Washton, Nancy M., and Kleber, Markus W. Mon . "Abiotic protein fragmentation by manganese oxide: Implications for a mechanism to supply soil biota with oligopeptides". United States. https://doi.org/10.1021/acs.est.5b04622. https://www.osti.gov/servlets/purl/1254585.
@article{osti_1254585,
title = {Abiotic protein fragmentation by manganese oxide: Implications for a mechanism to supply soil biota with oligopeptides},
author = {Reardon, Patrick N. and Chacon, Stephany S. and Walter, Eric D. and Bowden, Mark E. and Washton, Nancy M. and Kleber, Markus W.},
abstractNote = {The ability of plants and microorganisms to take up organic nitrogen in the form of free amino acids and oligopeptides has received increasing attention over the last two decades, yet the mechanisms for the formation of such compounds in soil environments remain poorly understood. We used Nuclear Magnetic Resonance (NMR) and Electron Paramagnetic Resonance (EPR) spectroscopies to distinguish the reaction of a model protein with a pedogenic oxide (Birnessite, MnO2) from its response to a phyllosilicate (Kaolinite). Our data demonstrate that birnessite fragments the model protein while kaolinite does not, resulting in soluble peptides that would be available to soil biota and confirming the existence of an abiotic pathway for the formation of organic nitrogen compounds for direct uptake by plants and microorganisms. The absence of reduced Mn(II) in the solution suggests that birnessite acts as a catalyst rather than an oxidant in this reaction. NMR and EPR spectroscopies are shown to be valuable tools to observe these reactions and capture the extent of protein transformation together with the extent of mineral response.},
doi = {10.1021/acs.est.5b04622},
journal = {Environmental Science and Technology},
number = 7,
volume = 50,
place = {United States},
year = {Mon Mar 14 00:00:00 EDT 2016},
month = {Mon Mar 14 00:00:00 EDT 2016}
}

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Works referenced in this record:

Environmental proteomics: A long march in the pedosphere
journal, February 2014


New insights into enzymes in the environment
journal, November 2013


Extracellular enzymes in terrestrial, freshwater, and marine environments: perspectives on system variability and common research needs
journal, September 2013


Soil enzymes in a changing environment: Current knowledge and future directions
journal, March 2013


Environmental Proteomics: a Paradigm Shift in Characterizing Microbial Activities at the Molecular Level
journal, March 2009

  • Keller, M.; Hettich, R.
  • Microbiology and Molecular Biology Reviews, Vol. 73, Issue 1
  • DOI: 10.1128/MMBR.00028-08

Microbial metaproteomics: identifying the repertoire of proteins that microorganisms use to compete and cooperate in complex environmental communities
journal, June 2012

  • Hettich, Robert L.; Sharma, Ritin; Chourey, Karuna
  • Current Opinion in Microbiology, Vol. 15, Issue 3
  • DOI: 10.1016/j.mib.2012.04.008

The Potential of Metagenomic Approaches for Understanding Soil Microbial Processes
journal, January 2014

  • Myrold, David D.; Zeglin, Lydia H.; Jansson, Janet K.
  • Soil Science Society of America Journal, Vol. 78, Issue 1
  • DOI: 10.2136/sssaj2013.07.0287dgs

My voyage of discovery to proteins in flatland …and beyond
journal, January 2008


Adsorption of Insecticidal Cry1Ab Protein to Humic Substances. 2. Influence of Humic and Fulvic Acid Charge and Polarity Characteristics
journal, August 2012

  • Tomaszewski, Jeanne E.; Madliger, Michael; Pedersen, Joel A.
  • Environmental Science & Technology
  • DOI: 10.1021/es302248u

The oxidative environment and protein damage
journal, January 2005


Reactivity Differences of Combined and Free Amino Acids: Quantifying the Relationship between Three-Dimensional Protein Structure and Singlet Oxygen Reaction Rates
journal, December 2013

  • Lundeen, Rachel A.; McNeill, Kristopher
  • Environmental Science & Technology, Vol. 47, Issue 24
  • DOI: 10.1021/es404236c

Oxidative modification of a proline-rich gliadin peptide
journal, December 2013


Lipid Peroxidation and Protein Oxidation in Azotobacter Vinelandii Exposed to Mercury, Silver, Crude oil, and Fenton Reagent
journal, October 1999


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

Adsorption and Oxidation of Phenolic Compounds by Iron and Manganese Oxides1
journal, January 1987


Pathogenic prion protein is degraded by a manganese oxide mineral found in soils
journal, January 2009

  • Russo, F.; Johnson, C. J.; Johnson, C. J.
  • Journal of General Virology, Vol. 90, Issue 1
  • DOI: 10.1099/vir.0.003251-0

Soil Mineralogy with Environmental Applications
book, January 2002


Soils Reveal Widespread Manganese Enrichment from Industrial Inputs
journal, January 2011

  • Herndon, Elizabeth M.; Jin, Lixin; Brantley, Susan L.
  • Environmental Science & Technology, Vol. 45, Issue 1
  • DOI: 10.1021/es102001w

Spectroscopic (XANES/XRF) characterization of contaminant manganese cycling in a temperate watershed
journal, August 2014

  • Herndon, Elizabeth M.; Martínez, Carmen E.; Brantley, Susan L.
  • Biogeochemistry, Vol. 121, Issue 3
  • DOI: 10.1007/s10533-014-0018-7

Movement of manganese contamination through the Critical Zone
journal, June 2011


The Adsorption and Reactions of Enzymes and Proteins on Kaolinite. I
journal, February 1954

  • McLaren, A. Douglas
  • The Journal of Physical Chemistry, Vol. 58, Issue 2
  • DOI: 10.1021/j150512a008

Hydrolysis of cellobiose by β-glucosidase in the presence of soil minerals – Interactions at solid–liquid interfaces and effects on enzyme activity levels
journal, December 2010


Adsorption of proteins and nucleic acids on clay minerals and their interactions: A review
journal, August 2013


A novel, highly stable fold of the immunoglobulin binding domain of streptococcal protein G
journal, August 1991


Multidimensional NMR Spectroscopy for Protein Characterization and Assignment inside Cells
journal, August 2005

  • Reardon, Patrick N.; Spicer, Leonard D.
  • Journal of the American Chemical Society, Vol. 127, Issue 31
  • DOI: 10.1021/ja053145k

Ultrahigh resolution protein structures using NMR chemical shift tensors
journal, October 2011

  • Wylie, B. J.; Sperling, L. J.; Nieuwkoop, A. J.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 41
  • DOI: 10.1073/pnas.1103728108

Generalized Reconstruction of n -D NMR Spectra from Multiple Projections:  Application to the 5-D HACACONH Spectrum of Protein G B1 Domain
journal, January 2004

  • Coggins, Brian E.; Venters, Ronald A.; Zhou, Pei
  • Journal of the American Chemical Society, Vol. 126, Issue 4
  • DOI: 10.1021/ja039430q

Protein Identification and Analysis Tools on the ExPASy Server
book, January 2005

  • Gasteiger, Elisabeth; Hoogland, Christine; Gattiker, Alexandre
  • The Proteomics Protocols Handbook
  • DOI: 10.1385/1-59259-890-0:571

Rapid Protein Global Fold Determination Using Ultrasparse Sampling, High-Dynamic Range Artifact Suppression, and Time-Shared NOESY
journal, September 2012

  • Coggins, Brian E.; Werner-Allen, Jonathan W.; Yan, Anthony
  • Journal of the American Chemical Society, Vol. 134, Issue 45
  • DOI: 10.1021/ja307445y

Structure of an HIV-1-neutralizing antibody target, the lipid-bound gp41 envelope membrane proximal region trimer
journal, January 2014

  • Reardon, P. N.; Sage, H.; Dennison, S. M.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 4
  • DOI: 10.1073/pnas.1309842111

NMRPipe: A multidimensional spectral processing system based on UNIX pipes
journal, November 1995

  • Delaglio, Frank; Grzesiek, Stephan; Vuister, GeertenW.
  • Journal of Biomolecular NMR, Vol. 6, Issue 3
  • DOI: 10.1007/BF00197809

Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa
journal, November 1987


NMR with Proteins and Nucleic Acids
journal, January 1986


Reaction mechanisms in the radiolysis of peptides, polypeptides, and proteins
journal, April 1987


Reductive Transformation of Birnessite by Aqueous Mn(II)
journal, August 2011

  • Elzinga, Evert J.
  • Environmental Science & Technology, Vol. 45, Issue 15
  • DOI: 10.1021/es2013038

The citric acid–MnIII,IVO2(birnessite) reaction. Electron transfer, complex formation, and autocatalytic feedback
journal, September 2006


Hydrolysis of an Organophosphate Ester by Manganese Dioxide
journal, February 2001

  • Baldwin, Darren S.; Beattie, James K.; Coleman, Lynette M.
  • Environmental Science & Technology, Vol. 35, Issue 4
  • DOI: 10.1021/es001309l

Phosphate Ester Hydrolysis Facilitated by Mineral Phases
journal, June 1995

  • Baldwin, Darren S.; Beattie, James K.; Coleman, Lynette M.
  • Environmental Science & Technology, Vol. 29, Issue 6
  • DOI: 10.1021/es00006a040

Redox Reactions between Mn(II) and Hexagonal Birnessite Change Its Layer Symmetry
journal, January 2016

  • Zhao, Huaiyan; Zhu, Mengqiang; Li, Wei
  • Environmental Science & Technology, Vol. 50, Issue 4
  • DOI: 10.1021/acs.est.5b04436

Transformations of Synthetic Birnessite as Affected by pH and Manganese Concentration
journal, January 1994


Polypeptide Adsorption on a Synthetic Montmorillonite: A Combined Solid-State NMR Spectroscopy, X-ray Diffraction, Thermal Analysis and N2 Adsorption Study
journal, April 2003

  • Gougeon, Régis D.; Soulard, Michel; Reinholdt, Marc
  • European Journal of Inorganic Chemistry, Vol. 2003, Issue 7
  • DOI: 10.1002/ejic.200390177

Soil mineral–organic matter–microbe interactions: Impacts on biogeochemical processes and biodiversity in soils
journal, November 2005


The chemical and functional characterization of soil N and its biotic components
journal, December 2009


Mineralization of Amino Acids and Evidence of Direct Assimilation of Organic Nitrogen
journal, May 1990


The direct or MIT route for nitrogen immobilization: A 15N mirror image study with leucine and glycine
journal, January 1997


Nitrogen Mineralization: Challenges of a Changing Paradigm
journal, March 2004

  • Schimel, Joshua P.; Bennett, Jennifer
  • Ecology, Vol. 85, Issue 3
  • DOI: 10.1890/03-8002

Controls on soil nitrogen cycling and microbial community composition across land use and incubation temperature
journal, March 2007


Vascular plant success in a warming Antarctic may be due to efficient nitrogen acquisition
journal, March 2011

  • Hill, Paul W.; Farrar, John; Roberts, Paula
  • Nature Climate Change, Vol. 1, Issue 1
  • DOI: 10.1038/nclimate1060

Characterization of the manganese oxide produced by pseudomonas putida strain MnB1
journal, July 2003


Works referencing / citing this record:

Fe(II) reduction of pyrolusite (β-MnO2) and secondary mineral evolution
journal, December 2017

  • Schaefer, Michael V.; Handler, Robert M.; Scherer, Michelle M.
  • Geochemical Transactions, Vol. 18, Issue 1
  • DOI: 10.1186/s12932-017-0045-0

Minerals in the rhizosphere: overlooked mediators of soil nitrogen availability to plants and microbes
journal, June 2018

  • Jilling, Andrea; Keiluweit, Marco; Contosta, Alexandra R.
  • Biogeochemistry, Vol. 139, Issue 2
  • DOI: 10.1007/s10533-018-0459-5

The laccase-like reactivity of manganese oxide nanomaterials for pollutant conversion: rate analysis and cyclic voltammetry
journal, August 2017


Carbohydrates protect protein against abiotic fragmentation by soil minerals
journal, January 2018

  • Reardon, Patrick N.; Walter, Eric D.; Marean-Reardon, Carrie L.
  • Scientific Reports, Vol. 8, Issue 1
  • DOI: 10.1038/s41598-017-19119-7