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Title: Interactions among roots, mycorrhizas and free-living microbial communities differentially impact soil carbon processes

Abstract

1. Plant roots, their associated microbial community and free-living soil microbes interact to regulate the movement of carbon from the soil to the atmosphere, one of the most important and least understood fluxes of terrestrial carbon. Our inadequate understanding of how plant–microbial interactions alter soil carbon decomposition may lead to poor model predictions of terrestrial carbon feedbacks to the atmosphere. 2. Roots, mycorrhizal fungi and free-living soil microbes can alter soil carbon decomposition through exudation of carbon into soil. Exudates of simple carbon compounds can increase microbial activity because microbes are typically carbon limited. When both roots and mycorrhizal fungi are present in the soil, they may additively increase carbon decomposition. However, when mycorrhizas are isolated from roots, they may limit soil carbon decomposition by competing with free-living decomposers for resources. 3. We manipulated the access of roots and mycorrhizal fungi to soil in situ in a temperate mixed deciduous forest. We added 13C-labelled substrate to trace metabolized carbon in respiration and measured carbon-degrading microbial extracellular enzyme activity and soil carbon pools. We used our data in a mechanistic soil carbon decomposition model to simulate and compare the effects of root and mycorrhizal fungal presence on soil carbon dynamics overmore » longer time periods. 4. Contrary to what we predicted, root and mycorrhizal biomass did not interact to additively increase microbial activity and soil carbon degradation. The metabolism of 13C-labelled starch was highest when root biomass was high and mycorrhizal biomass was low. These results suggest that mycorrhizas may negatively interact with the free-living microbial community to influence soil carbon dynamics, a hypothesis supported by our enzyme results. Our steady-state model simulations suggested that root presence increased mineral-associated and particulate organic carbon pools, while mycorrhizal fungal presence had a greater influence on particulate than mineral-associated organic carbon pools. 5. Synthesis. Our results suggest that the activity of enzymes involved in organic matter decomposition was contingent upon root–mycorrhizal–microbial interactions. Using our experimental data in a decomposition simulation model, we show that root–mycorrhizal–microbial interactions may have longer- term legacy effects on soil carbon sequestration. Overall, our study suggests that roots stimulate microbial activity in the short term, but contribute to soil carbon storage over longer periods of time.« less

Authors:
 [1];  [1];  [1];  [2];  [2];  [3]
+ Show Author Affiliations
  1. 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); Univ. of Copenhagen, Kobenhavn O (Denmark)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1326499
Alternate Identifier(s):
OSTI ID: 1400939; OSTI ID: 1501382
Grant/Contract Number:  
AC05-00OR22725; SC0010562
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Ecology
Additional Journal Information:
Journal Volume: 103; Journal Issue: 6; Journal ID: ISSN 0022-0477
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; decomposition; extracellular enzyme activity; forest; nutrient cycling; plant-microbe interactions; plant-soil (below-ground) interactions; rhizosphere; simulation model; stable isotope

Citation Formats

Moore, Jessica A. M., Jiang, Jiang, Patterson, Courtney M., Mayes, Melanie A., Wang, Gangsheng, and Classen, Aimée T. Interactions among roots, mycorrhizas and free-living microbial communities differentially impact soil carbon processes. United States: N. p., 2015. Web. doi:10.1111/1365-2745.12484.
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Moore, Jessica A. M., Jiang, Jiang, Patterson, Courtney M., Mayes, Melanie A., Wang, Gangsheng, & Classen, Aimée T. Interactions among roots, mycorrhizas and free-living microbial communities differentially impact soil carbon processes. United States. https://doi.org/10.1111/1365-2745.12484
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Moore, Jessica A. M., Jiang, Jiang, Patterson, Courtney M., Mayes, Melanie A., Wang, Gangsheng, and Classen, Aimée T. Tue . "Interactions among roots, mycorrhizas and free-living microbial communities differentially impact soil carbon processes". United States. https://doi.org/10.1111/1365-2745.12484. https://www.osti.gov/servlets/purl/1326499.
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@article{osti_1326499,
title = {Interactions among roots, mycorrhizas and free-living microbial communities differentially impact soil carbon processes},
author = {Moore, Jessica A. M. and Jiang, Jiang and Patterson, Courtney M. and Mayes, Melanie A. and Wang, Gangsheng and Classen, Aimée T.},
abstractNote = {1. Plant roots, their associated microbial community and free-living soil microbes interact to regulate the movement of carbon from the soil to the atmosphere, one of the most important and least understood fluxes of terrestrial carbon. Our inadequate understanding of how plant–microbial interactions alter soil carbon decomposition may lead to poor model predictions of terrestrial carbon feedbacks to the atmosphere. 2. Roots, mycorrhizal fungi and free-living soil microbes can alter soil carbon decomposition through exudation of carbon into soil. Exudates of simple carbon compounds can increase microbial activity because microbes are typically carbon limited. When both roots and mycorrhizal fungi are present in the soil, they may additively increase carbon decomposition. However, when mycorrhizas are isolated from roots, they may limit soil carbon decomposition by competing with free-living decomposers for resources. 3. We manipulated the access of roots and mycorrhizal fungi to soil in situ in a temperate mixed deciduous forest. We added 13C-labelled substrate to trace metabolized carbon in respiration and measured carbon-degrading microbial extracellular enzyme activity and soil carbon pools. We used our data in a mechanistic soil carbon decomposition model to simulate and compare the effects of root and mycorrhizal fungal presence on soil carbon dynamics over longer time periods. 4. Contrary to what we predicted, root and mycorrhizal biomass did not interact to additively increase microbial activity and soil carbon degradation. The metabolism of 13C-labelled starch was highest when root biomass was high and mycorrhizal biomass was low. These results suggest that mycorrhizas may negatively interact with the free-living microbial community to influence soil carbon dynamics, a hypothesis supported by our enzyme results. Our steady-state model simulations suggested that root presence increased mineral-associated and particulate organic carbon pools, while mycorrhizal fungal presence had a greater influence on particulate than mineral-associated organic carbon pools. 5. Synthesis. Our results suggest that the activity of enzymes involved in organic matter decomposition was contingent upon root–mycorrhizal–microbial interactions. Using our experimental data in a decomposition simulation model, we show that root–mycorrhizal–microbial interactions may have longer- term legacy effects on soil carbon sequestration. Overall, our study suggests that roots stimulate microbial activity in the short term, but contribute to soil carbon storage over longer periods of time.},
doi = {10.1111/1365-2745.12484},
journal = {Journal of Ecology},
number = 6,
volume = 103,
place = {United States},
year = {Tue Oct 20 00:00:00 EDT 2015},
month = {Tue Oct 20 00:00:00 EDT 2015}
}
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Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/1365-2745.12484
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Cited by: 49 works
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Figures / Tables:

Fig. 1 Fig. 1: Conceptual diagram illustrating hypothetical outcomes of root–mycorrhizal–microbial interactions. Our experimental mesocosms target three distinct and naturally occurring types of soil communities: communities with roots (dark coloured) and mycorrhizal fungi (light coloured) (+roots +myc), without roots ( –roots +myc) and without either ( –roots –myc). We examined the responsemore » of soil respiration (arrows, size indicates magnitude of flux), enzyme activity (boxes, + indicates greater magnitude of activity) and storage of soil organic carbon (SOC; darker shading of soil indicates higher magnitude of pool size) to root–mycorrhizal–microbial interactions. We predicted that decomposition processes would be greatest when roots and mycorrhizal fungi are present due to exudates stimulating microbial activity and that those processes would be reduced when roots or mycorrhizal fungi were absent from the soil community. We also predicted that SOC pools would be inversely related to decomposition processes: when decomposition was expected to be high, we would expect SOC pools to be low.« less
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dataset, October 2015

  • Moore, Jessica A. M.; Jiang, Jiang; Patterson, Courtney M.
  • Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1111/1365-2745.12484, 1 CSV file (6.974 Kb)
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    Works referencing / citing this record:

    Drivers of C cycling in three arctic-alpine plant communities
    text, January 2019

    Effects of global change factors and living roots on root litter decomposition in a Qinghai-Tibet alpine meadow
    journal, November 2019

    Plant roots increase both decomposition and stable organic matter formation in boreal forest soil
    journal, September 2019

    • Adamczyk, Bartosz; Sietiö, Outi-Maaria; Straková, Petra
    • Nature Communications, Vol. 10, Issue 1
    • DOI: 10.1038/s41467-019-11993-1

    Plant roots stimulate the decomposition of complex, but not simple, soil carbon
    journal, April 2020

    • Moore, Jessica A. M.; Sulman, Benjamin N.; Mayes, Melanie A.
    • Functional Ecology, Vol. 34, Issue 4
    • DOI: 10.1111/1365-2435.13510

    Contribution of plant litter and soil variables to organic carbon pools following tropical forest development after slash‐and‐burn agriculture
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    • Wang, Shaojun; Chen, Minkun; Cao, Run
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    Data from: Interactions among roots, mycorrhizae and free-living microbial communities differentially impact soil carbon processes
    dataset, October 2015

    • Moore, Jessica A. M.; Jiang, Jiang; Patterson, Courtney M.
    • Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1111/1365-2745.12484, 1 CSV file (6.974 Kb)
    • DOI: 10.5061/dryad.pb271

    Drivers of C cycling in three arctic-alpine plant communities
    text, January 2020

    Drivers of C cycling in three arctic-alpine plant communities
    journal, January 2019

    • Sørensen, Mia Vedel; Graae, Bente Jessen; Classen, Aimee
    • Arctic, Antarctic, and Alpine Research, Vol. 51, Issue 1
    • DOI: 10.1080/15230430.2019.1592649

    Data from: Interactions among roots, mycorrhizae and free-living microbial communities differentially impact soil carbon processes
    dataset, October 2015

    • Moore, Jessica A. M.; Jiang, Jiang; Patterson, Courtney M.
    • Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1111/1365-2745.12484, 1 CSV file (6.974 Kb)
    • DOI: 10.5061/dryad.pb271

    Plant roots increase both decomposition and stable organic matter formation in boreal forest soil
    journal, September 2019

    • Adamczyk, Bartosz; Sietiö, Outi-Maaria; Straková, Petra
    • Nature Communications, Vol. 10, Issue 1
    • DOI: 10.1038/s41467-019-11993-1

    Effects of global change factors and living roots on root litter decomposition in a Qinghai-Tibet alpine meadow
    journal, November 2019

    Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks
    journal, August 2019

    • Revillini, Daniel; Wilson, Gail W. T.; Miller, R. Michael
    • Frontiers in Plant Science, Vol. 10
    • DOI: 10.3389/fpls.2019.01018
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