skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Plant roots stimulate the decomposition of complex, but not simple, soil carbon

Abstract

Roots release carbon into soil and can alleviate energy limitation of microbial organic matter decomposition. We know little about the effects of roots on microbial decomposition of different organic matter substrates, despite the importance for soil carbon stocks and turnover. Through implementing root-microbe interactions, the Carbon, Organisms, Rhizosphere, and Protection in the Soil Environment (CORPSE) model was previously shown to represent dynamics of total soil carbon in temperate forest field experiments. However, the model permits alternative hypotheses concerning microbial-substrate affinity. We investigated how root inputs affect decomposition of soil organic carbon (SOC) with variable decomposability. We simulated SOC stocks in CORPSE and compared microbial degradation of two substrates types with varying root-microbe interactions under two alternative hypotheses that varied in microbial-substrate affinity. We compared our modeled hypotheses to a forest field experiment where we quantified decomposition of isotopically-labeled starch and leaf tissues in soils with manipulated root access to microbes. Here, we tested the hypothesis that decomposition of leaves would be more sensitive to root inputs than decomposition of starch, corresponding to the alternative model hypothesis. In the field study, leaf decomposition increased with root density while starch decomposition was unchanged by root density. Microbial biomass and enzyme activity consistentlymore » increased with root inputs in CORPSE and the field study. Our field experiment supported the CORPSE simulations with high microbial-substrate affinity. Roots stimulated microbial growth and enzyme production, which increased degradation of more complex substrates such as leaf tissues. Substrates that were easily decomposed, such as starch, may already be degrading at a maximum rate in the absence of rhizosphere influence because their decomposition rate was unchanged by root inputs. We found that the degree to which roots stimulate microbial decomposition depends on the substrate being decomposed, and that root-microbe interactions influenced SOC stocks in both our model and field experiment. Environmental changes that alter root-microbe interactions could, therefore, alter soil C stocks and biogeochemical cycling, and models of these interactions should incorporate differential influence of rhizosphere inputs on different substrates.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2];  [3];  [4]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. Univ. of Tennessee, Knoxville, TN (United States)
  4. Univ. of Vermont, Burlington, VT (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1609047
Alternate Identifier(s):
OSTI ID: 1582681
Grant/Contract Number:  
AC05-00OR22725; SC0010562
Resource Type:
Accepted Manuscript
Journal Name:
Functional Ecology
Additional Journal Information:
Journal Volume: 34; Journal Issue: 4; Journal ID: ISSN 0269-8463
Publisher:
British Ecological Society; Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; broadleaf boreal forest; ecosystem model; extracellular enzymes; plant-microbe interaction; soil carbon; soil organic matter; stable isotopes

Citation Formats

Moore, Jessica, Sulman, Benjamin, Mayes, Melanie A., Patterson, Courtney M., and Classen, Aimee T. Plant roots stimulate the decomposition of complex, but not simple, soil carbon. United States: N. p., 2019. Web. https://doi.org/10.1111/1365-2435.13510.
Moore, Jessica, Sulman, Benjamin, Mayes, Melanie A., Patterson, Courtney M., & Classen, Aimee T. Plant roots stimulate the decomposition of complex, but not simple, soil carbon. United States. https://doi.org/10.1111/1365-2435.13510
Moore, Jessica, Sulman, Benjamin, Mayes, Melanie A., Patterson, Courtney M., and Classen, Aimee T. Thu . "Plant roots stimulate the decomposition of complex, but not simple, soil carbon". United States. https://doi.org/10.1111/1365-2435.13510. https://www.osti.gov/servlets/purl/1609047.
@article{osti_1609047,
title = {Plant roots stimulate the decomposition of complex, but not simple, soil carbon},
author = {Moore, Jessica and Sulman, Benjamin and Mayes, Melanie A. and Patterson, Courtney M. and Classen, Aimee T.},
abstractNote = {Roots release carbon into soil and can alleviate energy limitation of microbial organic matter decomposition. We know little about the effects of roots on microbial decomposition of different organic matter substrates, despite the importance for soil carbon stocks and turnover. Through implementing root-microbe interactions, the Carbon, Organisms, Rhizosphere, and Protection in the Soil Environment (CORPSE) model was previously shown to represent dynamics of total soil carbon in temperate forest field experiments. However, the model permits alternative hypotheses concerning microbial-substrate affinity. We investigated how root inputs affect decomposition of soil organic carbon (SOC) with variable decomposability. We simulated SOC stocks in CORPSE and compared microbial degradation of two substrates types with varying root-microbe interactions under two alternative hypotheses that varied in microbial-substrate affinity. We compared our modeled hypotheses to a forest field experiment where we quantified decomposition of isotopically-labeled starch and leaf tissues in soils with manipulated root access to microbes. Here, we tested the hypothesis that decomposition of leaves would be more sensitive to root inputs than decomposition of starch, corresponding to the alternative model hypothesis. In the field study, leaf decomposition increased with root density while starch decomposition was unchanged by root density. Microbial biomass and enzyme activity consistently increased with root inputs in CORPSE and the field study. Our field experiment supported the CORPSE simulations with high microbial-substrate affinity. Roots stimulated microbial growth and enzyme production, which increased degradation of more complex substrates such as leaf tissues. Substrates that were easily decomposed, such as starch, may already be degrading at a maximum rate in the absence of rhizosphere influence because their decomposition rate was unchanged by root inputs. We found that the degree to which roots stimulate microbial decomposition depends on the substrate being decomposed, and that root-microbe interactions influenced SOC stocks in both our model and field experiment. Environmental changes that alter root-microbe interactions could, therefore, alter soil C stocks and biogeochemical cycling, and models of these interactions should incorporate differential influence of rhizosphere inputs on different substrates.},
doi = {10.1111/1365-2435.13510},
journal = {Functional Ecology},
number = 4,
volume = 34,
place = {United States},
year = {2019},
month = {12}
}

Works referenced in this record:

Gross Nitrogen Dynamics in the Mycorrhizosphere of an Organic Forest Soil
journal, November 2015


Stoichiometry constrains microbial response to root exudation- insights from a model and a field experiment in a temperate forest
journal, January 2013


The Vertical Distribution of soil Organic Carbon and its Relation to Climate and Vegetation
journal, April 2000


Microbial dormancy improves development and experimental validation of ecosystem model
journal, July 2014

  • Wang, Gangsheng; Jagadamma, Sindhu; Mayes, Melanie A.
  • The ISME Journal, Vol. 9, Issue 1
  • DOI: 10.1038/ismej.2014.120

Dual, differential isotope labeling shows the preferential movement of labile plant constituents into mineral-bonded soil organic matter
journal, March 2016

  • Haddix, Michelle L.; Paul, Eldor A.; Cotrufo, M. Francesca
  • Global Change Biology, Vol. 22, Issue 6
  • DOI: 10.1111/gcb.13237

Novel in-growth core system enables functional studies of grassland mycorrhizal mycelial networks
journal, December 2001


A potential loss of carbon associated with greater plant growth in the European Arctic
journal, June 2012

  • Hartley, Iain P.; Garnett, Mark H.; Sommerkorn, Martin
  • Nature Climate Change, Vol. 2, Issue 12
  • DOI: 10.1038/nclimate1575

Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO 2
journal, July 2012


Disruption of root carbon transport into forest humus stimulates fungal opportunists at the expense of mycorrhizal fungi
journal, March 2010

  • Lindahl, Björn D.; de Boer, Wietse; Finlay, Roger D.
  • The ISME Journal, Vol. 4, Issue 7
  • DOI: 10.1038/ismej.2010.19

Soil carbon pools and world life zones
journal, July 1982

  • Post, Wilfred M.; Emanuel, William R.; Zinke, Paul J.
  • Nature, Vol. 298, Issue 5870
  • DOI: 10.1038/298156a0

An extraction method for measuring soil microbial biomass C
journal, January 1987


Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming
journal, April 2013

  • Yin, Huajun; Li, Yufei; Xiao, Juan
  • Global Change Biology, Vol. 19, Issue 7
  • DOI: 10.1111/gcb.12161

Increased coniferous needle inputs accelerate decomposition of soil carbon in an old-growth forest
journal, October 2009


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

Review of root dynamics in forest ecosystems grouped by climate, climatic forest type and species
journal, July 1995

  • Vogt, Kristiina A.; Vogt, Daniel J.; Palmiotto, Peter A.
  • Plant and Soil, Vol. 187, Issue 2
  • DOI: 10.1007/BF00017088

Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review
journal, October 2008


Root litter decomposition slows with soil depth
journal, October 2018


Mycorrhizal type determines the magnitude and direction of root-induced changes in decomposition in a temperate forest
journal, January 2015

  • Brzostek, Edward R.; Dragoni, Danilo; Brown, Zachary A.
  • New Phytologist, Vol. 206, Issue 4
  • DOI: 10.1111/nph.13303

Priming effects: Interactions between living and dead organic matter
journal, September 2010


Integrating microbial physiology and physio-chemical principles in soils with the MIcrobial-MIneral Carbon Stabilization (MIMICS) model
journal, January 2014


Selective progressive response of soil microbial community to wild oat roots
journal, November 2008

  • DeAngelis, Kristen M.; Brodie, Eoin L.; DeSantis, Todd Z.
  • The ISME Journal, Vol. 3, Issue 2
  • DOI: 10.1038/ismej.2008.103

Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes
journal, March 2015

  • McCormack, M. Luke; Dickie, Ian A.; Eissenstat, David M.
  • New Phytologist, Vol. 207, Issue 3
  • DOI: 10.1111/nph.13363

Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest
journal, March 2013


Root exudates increase N availability by stimulating microbial turnover of fast-cycling N pools
journal, March 2017


Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles
journal, January 2015

  • Finzi, Adrien C.; Abramoff, Rose Z.; Spiller, Kimberly S.
  • Global Change Biology, Vol. 21, Issue 5
  • DOI: 10.1111/gcb.12816

Stored carbon partly fuels fine-root respiration but is not used for production of new fine roots
journal, May 2013

  • Lynch, Douglas J.; Matamala, Roser; Iversen, Colleen M.
  • New Phytologist, Vol. 199, Issue 2
  • DOI: 10.1111/nph.12290

Novel scanning procedure enabling the vectorization of entire rhizotron-grown root systems
journal, January 2013


Weaker soil carbon–climate feedbacks resulting from microbial and abiotic interactions
journal, November 2014


Interactions among roots, mycorrhizas and free-living microbial communities differentially impact soil carbon processes
journal, October 2015

  • Moore, Jessica A. M.; Jiang, Jiang; Patterson, Courtney M.
  • Journal of Ecology, Vol. 103, Issue 6, p. 1442-1453
  • DOI: 10.1111/1365-2745.12484

Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO2
journal, November 2014

  • Sulman, Benjamin N.; Phillips, Richard P.; Oishi, A. Christopher
  • Nature Climate Change, Vol. 4, Issue 12
  • DOI: 10.1038/nclimate2436

Quantifying global soil carbon losses in response to warming
journal, November 2016

  • Crowther, T. W.; Todd-Brown, K. E. O.; Rowe, C. W.
  • Nature, Vol. 540, Issue 7631
  • DOI: 10.1038/nature20150

Global estimates of boreal forest carbon stocks and flux
journal, May 2015


An Affinity–Effect Relationship for Microbial Communities in Plant–Soil Feedback Loops
journal, January 2014


Microbial Community Composition and Function Across an Arctic Tundra Landscape
journal, July 2006


SPRUCE Environmental Monitoring Data: 2010-2016
dataset, January 2016

  • Hanson, P.; Riggs, J.; Dorrance, C.
  • SPRUCE (Spruce and Peatland Responses Under Changing Environments)
  • DOI: 10.3334/CDIAC/spruce.001

Fungal Traits That Drive Ecosystem Dynamics on Land
journal, May 2015

  • Treseder, Kathleen K.; Lennon, Jay T.
  • Microbiology and Molecular Biology Reviews, Vol. 79, Issue 2
  • DOI: 10.1128/MMBR.00001-15

Applying population and community ecology theory to advance understanding of belowground biogeochemistry
journal, January 2017

  • Buchkowski, Robert W.; Bradford, Mark A.; Grandy, Andrew Stuart
  • Ecology Letters, Vol. 20, Issue 2
  • DOI: 10.1111/ele.12712

Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation
journal, February 2005

  • Rasse, Daniel P.; Rumpel, Cornelia; Dignac, Marie-France
  • Plant and Soil, Vol. 269, Issue 1-2
  • DOI: 10.1007/s11104-004-0907-y

Effects of selected root exudate components on soil bacterial communities: Root exudate components and soil microbial communities
journal, July 2011


Diverse Mycorrhizal Associations Enhance Terrestrial C Storage in a Global Model
journal, April 2019

  • Sulman, Benjamin N.; Shevliakova, Elena; Brzostek, Edward R.
  • Global Biogeochemical Cycles, Vol. 33, Issue 4
  • DOI: 10.1029/2018GB005973

Hydrologic Cycling of Mercury and Organic Carbon in a Forested Upland-Bog Watershed
journal, May 2001

  • Kolka, R. K.; Grigal, D. F.; Nater, E. A.
  • Soil Science Society of America Journal, Vol. 65, Issue 3
  • DOI: 10.2136/sssaj2001.653897x

Investigating drivers of microbial activity and respiration in a forested bog
journal, February 2020


Ectomycorrhizal colonization slows root decomposition: the post-mortem fungal legacy
journal, August 2006