DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Simple Plant and Microbial Exudates Destabilize Mineral-Associated Organic Matter via Multiple Pathways

Abstract

Most mineral-associated organic matter (MAOM) is protected against microbial attack, thereby contributing to longterm carbon storage in soils. However, the extent to which reactive compounds released by plants and microbes may destabilize MAOM and so enhance microbial access, as well as the underlying mechanisms, remain unclear. Here, we tested the ability of functionally distinct model exudates (ligands, reductants, and simple sugars) to promote microbial utilization of monomeric MAOM, bound via outer-sphere complexes to common iron and aluminum (hydr)oxide minerals. The strong ligand oxalic acid induced rapid MAOM mineralization, coinciding with greater sorption to and dissolution of minerals, suggestive of direct MAOM mobilization mechanisms. In contrast, the simple sugar glucose caused slower MAOM mineralization, but stimulated microbial activity and metabolite production, indicating an indirect microbially-mediated mechanism. Catechol, acting as reductant, promoted both mechanisms. While MAOM on ferrihydrite showed the greatest vulnerability to both direct and indirect mechanisms, MAOM on other (hydr)oxides was more susceptible to direct mechanisms. These findings suggest that MAOM persistence, and thus longterm carbon storage within a given soil, is not just a function of mineral reactivity but also depends on the capacity of plant roots and associated microbes to produce reactive compounds capable of triggering specific destabilizationmore » mechanisms.« less

Authors:
 [1];  [2];  [3]; ORCiD logo [4];  [5]; ORCiD logo [1]
  1. Stockbridge School of Agriculture and School of Earth & Sustainability, University of Massachusetts, Amherst, Massachusetts 01003, United States
  2. Stockbridge School of Agriculture and School of Earth & Sustainability, University of Massachusetts, Amherst, Massachusetts 01003, United States, Department of Biology, Lund University, 223 62 Lund, Sweden
  3. Department of Geosciences, University of Massachusetts, Amherst, Massachusetts 01003, United States
  4. Department of Environmental Science, University of Arizona, Tucson, Arizona 85719, United States
  5. The Ecosystems Center, Marine Biological Laboratory, Woods Hole, Massachusetts 02543, United States
Publication Date:
Research Org.:
Marine Biological Laboratory, Woods Hole, MA (United States); Univ. of Massachusetts, Amherst, MA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1777582
Alternate Identifier(s):
OSTI ID: 1774962
Grant/Contract Number:  
SC0019142; SC0019477
Resource Type:
Published Article
Journal Name:
Environmental Science and Technology
Additional Journal Information:
Journal Name: Environmental Science and Technology Journal Volume: 55 Journal Issue: 5; Journal ID: ISSN 0013-936X
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; Mineral-associated organic matter; root exudates; soil carbon; iron minerals; aluminum minerals; ligands; microbial mineralization; carbohydrates; mineralization; dissolution; aromatic compounds; minerals

Citation Formats

Li, Hui, Bölscher, Tobias, Winnick, Matthew, Tfaily, Malak M., Cardon, Zoe G., and Keiluweit, Marco. Simple Plant and Microbial Exudates Destabilize Mineral-Associated Organic Matter via Multiple Pathways. United States: N. p., 2021. Web. doi:10.1021/acs.est.0c04592.
Li, Hui, Bölscher, Tobias, Winnick, Matthew, Tfaily, Malak M., Cardon, Zoe G., & Keiluweit, Marco. Simple Plant and Microbial Exudates Destabilize Mineral-Associated Organic Matter via Multiple Pathways. United States. https://doi.org/10.1021/acs.est.0c04592
Li, Hui, Bölscher, Tobias, Winnick, Matthew, Tfaily, Malak M., Cardon, Zoe G., and Keiluweit, Marco. Mon . "Simple Plant and Microbial Exudates Destabilize Mineral-Associated Organic Matter via Multiple Pathways". United States. https://doi.org/10.1021/acs.est.0c04592.
@article{osti_1777582,
title = {Simple Plant and Microbial Exudates Destabilize Mineral-Associated Organic Matter via Multiple Pathways},
author = {Li, Hui and Bölscher, Tobias and Winnick, Matthew and Tfaily, Malak M. and Cardon, Zoe G. and Keiluweit, Marco},
abstractNote = {Most mineral-associated organic matter (MAOM) is protected against microbial attack, thereby contributing to longterm carbon storage in soils. However, the extent to which reactive compounds released by plants and microbes may destabilize MAOM and so enhance microbial access, as well as the underlying mechanisms, remain unclear. Here, we tested the ability of functionally distinct model exudates (ligands, reductants, and simple sugars) to promote microbial utilization of monomeric MAOM, bound via outer-sphere complexes to common iron and aluminum (hydr)oxide minerals. The strong ligand oxalic acid induced rapid MAOM mineralization, coinciding with greater sorption to and dissolution of minerals, suggestive of direct MAOM mobilization mechanisms. In contrast, the simple sugar glucose caused slower MAOM mineralization, but stimulated microbial activity and metabolite production, indicating an indirect microbially-mediated mechanism. Catechol, acting as reductant, promoted both mechanisms. While MAOM on ferrihydrite showed the greatest vulnerability to both direct and indirect mechanisms, MAOM on other (hydr)oxides was more susceptible to direct mechanisms. These findings suggest that MAOM persistence, and thus longterm carbon storage within a given soil, is not just a function of mineral reactivity but also depends on the capacity of plant roots and associated microbes to produce reactive compounds capable of triggering specific destabilization mechanisms.},
doi = {10.1021/acs.est.0c04592},
journal = {Environmental Science and Technology},
number = 5,
volume = 55,
place = {United States},
year = {Mon Feb 15 00:00:00 EST 2021},
month = {Mon Feb 15 00:00:00 EST 2021}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1021/acs.est.0c04592

Save / Share:

Works referenced in this record:

Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?
journal, January 2018


Sugars in soil and sweets for microorganisms: Review of origin, content, composition and fate
journal, November 2015


Nitrogen acquisition from mineral‐associated proteins by an ectomycorrhizal fungus
journal, May 2020


Root exudate composition of grass and forb species in natural grasslands
journal, July 2020


Mineral protection of soil carbon counteracted by root exudates
journal, March 2015

  • Keiluweit, Marco; Bougoure, Jeremy J.; Nico, Peter S.
  • Nature Climate Change, Vol. 5, Issue 6
  • DOI: 10.1038/nclimate2580

Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
journal, March 2018


Roles of different types of oxalate surface complexes in dissolution process of ferrihydrite aggregates
journal, February 2018


Reductive dissolution of goethite by phenolic reductants
journal, May 1989


Biodegradation of forest floor organic matter bound to minerals via different binding mechanisms
journal, May 2007

  • Mikutta, Robert; Mikutta, Christian; Kalbitz, Karsten
  • Geochimica et Cosmochimica Acta, Vol. 71, Issue 10
  • DOI: 10.1016/j.gca.2007.03.002

The Iron Oxides
book, July 2003


Review of mechanisms and quantification of priming effects
journal, October 2000


Priming effect of some organic additions to 14C-labelled soil
journal, January 1989


Sorptive stabilization of organic matter in soils by hydrous iron oxides
journal, January 2007


Adsorption on Hydrous Oxides i. Oxalate and Benzoate on Goethite
journal, March 1977


Synthetic iron (hydr)oxide-glucose associations in subsurface soil: Effects on decomposability of mineral associated carbon
journal, February 2018


Mechanisms of dissolution of iron oxides in aqueous oxalic acid solutions
journal, September 1996


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

Ionization and Fragmentation of Humic Substances in Electrospray Ionization Fourier Transform-Ion Cyclotron Resonance Mass Spectrometry
journal, September 2002

  • Stenson, Alexandra C.; Landing, William M.; Marshall, Alan G.
  • Analytical Chemistry, Vol. 74, Issue 17
  • DOI: 10.1021/ac020019f

High-Resolution Fourier Transform Ion Cyclotron Resonance Mass Spectrometry of Humic and Fulvic Acids:  Improvements and Comparisons
journal, January 2002

  • Kujawinski, Elizabeth B.; Hatcher, Patrick G.; Freitas, Michael A.
  • Analytical Chemistry, Vol. 74, Issue 2
  • DOI: 10.1021/ac0108313

Isotopic compositions of the elements 2013 (IUPAC Technical Report)
journal, March 2016

  • Meija, Juris; Coplen, Tyler B.; Berglund, Michael
  • Pure and Applied Chemistry, Vol. 88, Issue 3
  • DOI: 10.1515/pac-2015-0503

What do we know about soil carbon destabilization?
journal, July 2019

  • Bailey, Vanessa L.; Pries, Caitlin Hicks; Lajtha, Kate
  • Environmental Research Letters, Vol. 14, Issue 8
  • DOI: 10.1088/1748-9326/ab2c11

A mechanism of aluminium toxicity to soil bacteria and possible ecological implications
journal, April 1995


Biodegradation of ferrihydrite-associated organic matter
journal, January 2014


Adsorption of Organic Matter at Mineral/Water Interfaces. 2. Outer-Sphere Adsorption of Maleate and Implications for Dissolution Processes
journal, June 2004

  • Johnson, Stephen B.; Yoon, Tae Hyun; Kocar, Benjamin D.
  • Langmuir, Vol. 20, Issue 12
  • DOI: 10.1021/la036288y

Bio-based production of organic acids with Corynebacterium glutamicum: Organic acid production with Corynebacterium glutamicum
journal, December 2012

  • Wieschalka, Stefan; Blombach, Bastian; Bott, Michael
  • Microbial Biotechnology, Vol. 6, Issue 2
  • DOI: 10.1111/1751-7915.12013

Changes of Redox and pH Conditions in a Flooded Soil Amended with Glucose and Nitrate under Laboratory Conditions
journal, January 1992

  • Glinski, Jan; Stahr, Karl; Stepniewska, Zofia
  • Zeitschrift für Pflanzenernährung und Bodenkunde, Vol. 155, Issue 1
  • DOI: 10.1002/jpln.19921550104

The contentious nature of soil organic matter
journal, November 2015


Selective Sorption of Dissolved Organic Carbon Compounds by Temperate Soils
journal, November 2012


Graphical Method for Analysis of Ultrahigh-Resolution Broadband Mass Spectra of Natural Organic Matter, the Van Krevelen Diagram
journal, October 2003

  • Kim, Sunghwan; Kramer, Robert W.; Hatcher, Patrick G.
  • Analytical Chemistry, Vol. 75, Issue 20
  • DOI: 10.1021/ac034415p

Microbial lipid and amino sugar responses to long-term simulated global environmental changes in a California annual grassland
journal, May 2015

  • Liang, Chao; Gutknecht, Jessica L. M.; Balser, Teri C.
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00385

Extracellular Enzyme Activity and Its Implications for Organic Matter Cycling in Northern Chinese Marginal Seas
journal, September 2019


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


Adsorption mechanisms of glucose in aqueous goethite suspensions
journal, January 2011

  • Olsson, Rickard; Giesler, Reiner; Persson, Per
  • Journal of Colloid and Interface Science, Vol. 353, Issue 1
  • DOI: 10.1016/j.jcis.2010.09.023

Root Exudation of Primary Metabolites: Mechanisms and Their Roles in Plant Responses to Environmental Stimuli
journal, February 2019

  • Canarini, Alberto; Kaiser, Christina; Merchant, Andrew
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.00157

Mobilization of ferrihydrite-associated organic carbon during Fe reduction: Adsorption versus coprecipitation
journal, January 2019


Extent and nature of organic coverage of soil mineral surfaces assessed by a gas sorption approach
journal, February 2009


Dissolution of iron oxide using oxalic acid
journal, July 2007


A simple and efficient method for the solid-phase extraction of dissolved organic matter (SPE-DOM) from seawater: SPE-DOM from seawater
journal, June 2008

  • Dittmar, Thorsten; Koch, Boris; Hertkorn, Norbert
  • Limnology and Oceanography: Methods, Vol. 6, Issue 6
  • DOI: 10.4319/lom.2008.6.230

Mineral–Organic Associations: Formation, Properties, and Relevance in Soil Environments
book, December 2014


Carbon loss from northern circumpolar permafrost soils amplified by rhizosphere priming
journal, July 2020


Synthesis and modeling perspectives of rhizosphere priming
journal, August 2013

  • Cheng, Weixin; Parton, William J.; Gonzalez-Meler, Miquel A.
  • New Phytologist, Vol. 201, Issue 1
  • DOI: 10.1111/nph.12440

Sorptive stabilization of organic matter by amorphous Al hydroxide
journal, March 2010

  • Schneider, M. P. W.; Scheel, T.; Mikutta, R.
  • Geochimica et Cosmochimica Acta, Vol. 74, Issue 5
  • DOI: 10.1016/j.gca.2009.12.017

Changes in water extractable organic matter during incubation of forest floor material in the presence of quartz, goethite and gibbsite surfaces
journal, August 2011

  • Heckman, Katherine; Vazquez-Ortega, Angelica; Gao, Xiaodong
  • Geochimica et Cosmochimica Acta, Vol. 75, Issue 15
  • DOI: 10.1016/j.gca.2011.05.009

Microbial and abiotic controls on mineral-associated organic matter in soil profiles along an ecosystem gradient
journal, July 2019


SOM genesis: microbial biomass as a significant source
journal, October 2011

  • Miltner, Anja; Bombach, Petra; Schmidt-Brücken, Burkhard
  • Biogeochemistry, Vol. 111, Issue 1-3
  • DOI: 10.1007/s10533-011-9658-z

Root-driven weathering impacts on mineral-organic associations in deep soils over pedogenic time scales
journal, October 2019

  • Garcia Arredondo, Mariela; Lawrence, Corey R.; Schulz, Marjorie S.
  • Geochimica et Cosmochimica Acta, Vol. 263
  • DOI: 10.1016/j.gca.2019.07.030

Rhizosphere Effects on Decomposition
journal, January 2003

  • Cheng, Weixin; Johnson, Dale W.; Fu, Shenglei
  • Soil Science Society of America Journal, Vol. 67, Issue 5
  • DOI: 10.2136/sssaj2003.1418