Roots selectively decompose litter to mine nitrogen and build new soil carbon

Ridgeway, Joanna; Kane, Jennifer; Morrissey, Ember; Starcher, Hayden; Brzostek, Edward

doi:10.1111/ele.14331

Title: Roots selectively decompose litter to mine nitrogen and build new soil carbon

Journal Article · 27 October 2023 · Ecology Letters

DOI: https://doi.org/10.1111/ele.14331 · OSTI ID:2203982

^[1]; Kane, Jennifer ^[2];

^[2]; Starcher, Hayden ^[3]; Brzostek, Edward ^[1]

Department of Biology West Virginia University Morgantown West Virginia USA, Center for Advanced Bioenergy and Bioproducts Innovation University of Illinois at Urbana‐Champaign Urbana Illinois USA
Division of Plant and Soil Sciences West Virginia University Morgantown West Virginia USA
Department of Biology West Virginia University Morgantown West Virginia USA

Abstract Plant–microbe interactions in the rhizosphere shape carbon and nitrogen cycling in soil organic matter (SOM). However, there is conflicting evidence on whether these interactions lead to a net loss or increase of SOM. In part, this conflict is driven by uncertainty in how living roots and microbes alter SOM formation or loss in the field. To address these uncertainties, we traced the fate of isotopically labelled litter into SOM using root and fungal ingrowth cores incubated in a Miscanthus x giganteus field. Roots stimulated litter decomposition, but balanced this loss by transferring carbon into aggregate associated SOM. Further, roots selectively mobilized nitrogen from litter without additional carbon release. Overall, our findings suggest that roots mine litter nitrogen and protect soil carbon.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0018420

OSTI ID:: 2203982

Alternate ID(s):: OSTI ID: 2204334; OSTI ID: 2283110

Journal Information:: Ecology Letters, Journal Name: Ecology Letters Journal Issue: 1 Vol. 27; ISSN 1461-023X

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (48)

Plant litter traits control microbial decomposition and drive soil carbon stabilization Ridgeway, Joanna R.; Morrissey, Ember M.; Brzostek, Edward R. Soil Biology and Biochemistry, Vol. 175 https://doi.org/10.1016/j.soilbio.2022.108857	journal	December 2022
Substrate supply, fine roots, and temperature control proteolytic enzyme activity in temperate forest soils Brzostek, Edward R.; Finzi, Adrien C. Ecology, Vol. 92, Issue 4 https://doi.org/10.1890/10-1803.1	journal	April 2011
Decomposition of particulate organic matter is more sensitive to temperature than the mineral associated organic matter Benbi, D. K.; Boparai, A. K.; Brar, Kiranvir Soil Biology and Biochemistry, Vol. 70 https://doi.org/10.1016/j.soilbio.2013.12.032	journal	March 2014
Meeting US biofuel goals with less land: the potential of Miscanthus Heaton, Emily A.; Dohleman, Frank G.; Long, Stephen P. Global Change Biology, Vol. 14, Issue 9, 2000-2014 https://doi.org/10.1111/j.1365‐2486.2008.01662.x	journal	August 2008
Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? Fernandez, Christopher W.; Kennedy, Peter G. New Phytologist, Vol. 209, Issue 4 https://doi.org/10.1111/nph.13648	journal	September 2015
Nitrogen limitation of decomposition and decay: How can it occur? Averill, Colin; Waring, Bonnie Global Change Biology, Vol. 24, Issue 4 https://doi.org/10.1111/gcb.13980	journal	December 2017
Bioenergy crop Miscanthus x giganteus acts as an ecosystem engineer to increase bacterial diversity and soil organic matter on marginal land Kane, Jennifer L.; Schartiger, Ronald G.; Daniels, Natalie Kruse Soil Biology and Biochemistry, Vol. 186 https://doi.org/10.1016/j.soilbio.2023.109178	journal	November 2023
Soil Structure and Organic Matter Six, J.; Paustian, K.; Elliott, E. T. Soil Science Society of America Journal, Vol. 64, Issue 2 https://doi.org/10.2136/sssaj2000.642681x	journal	January 2000
Anaerobic microsites have an unaccounted role in soil carbon stabilization Keiluweit, Marco; Wanzek, Tom; Kleber, Markus Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01406-6	journal	November 2017
Soil structure and management: a review Bronick, C. J.; Lal, R. Geoderma, Vol. 124, Issue 1-2 https://doi.org/10.1016/j.geoderma.2004.03.005	journal	January 2005
Persulfate Digestion and Simultaneous Colorimetric Analysis of Carbon and Nitrogen in Soil Extracts Doyle, Allen; Weintraub, Michael N.; Schimel, Joshua P. Soil Science Society of America Journal, Vol. 68, Issue 2 https://doi.org/10.2136/sssaj2004.6690	journal	March 2004
Patterns in root traits of woody species hosting arbuscular and ectomycorrhizas: implications for the evolution of belowground strategies Comas, Louise H.; Callahan, Hilary S.; Midford, Peter E. Ecology and Evolution, Vol. 4, Issue 15 https://doi.org/10.1002/ece3.1147	journal	July 2014
Nutrient requirements of Miscanthus x giganteus: Conclusions from a review of published studies Cadoux, Stéphane; Riche, Andrew B.; Yates, Nicola E. Biomass and Bioenergy, Vol. 38 https://doi.org/10.1016/j.biombioe.2011.01.015	journal	March 2012
Managing for soil carbon sequestration: Let’s get realistic Schlesinger, William H.; Amundson, Ronald Global Change Biology, Vol. 25, Issue 2 https://doi.org/10.1111/gcb.14478	journal	November 2018
Altered plant carbon partitioning enhanced forest ecosystem carbon storage after 25 years of nitrogen additions Eastman, Brooke A.; Adams, Mary B.; Brzostek, Edward R. New Phytologist, Vol. 230, Issue 4 https://doi.org/10.1111/nph.17256	journal	March 2021
Modeling the carbon cost of plant nitrogen acquisition: Mycorrhizal trade-offs and multipath resistance uptake improve predictions of retranslocation: Carbon cost of mycorrhizae Brzostek, Edward R.; Fisher, Joshua B.; Phillips, Richard P. Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 8 https://doi.org/10.1002/2014JG002660	journal	August 2014
An Evaluation of Techniques for Measuring Vesicular Arbuscular Mycorrhizal Infection in Roots Giovannetti, M.; Mosse, B. New Phytologist, Vol. 84, Issue 3 https://doi.org/10.1111/j.1469-8137.1980.tb04556.x	journal	March 1980
Climate-smart soils Paustian, Keith; Lehmann, Johannes; Ogle, Stephen Nature, Vol. 532, Issue 7597 https://doi.org/10.1038/nature17174	journal	April 2016
More Productive Than Maize in the Midwest: How Does Miscanthus Do It? Dohleman, Frank G.; Long, Stephen P. Plant Physiology, Vol. 150, Issue 4 https://doi.org/10.1104/pp.109.139162	journal	June 2009
Soil carbon storage informed by particulate and mineral-associated organic matter Cotrufo, M. Francesca; Ranalli, Maria Giovanna; Haddix, Michelle L. Nature Geoscience, Vol. 12, Issue 12 https://doi.org/10.1038/s41561‐019‐0484‐6	journal	November 2019
Rhizosphere priming effects on soil carbon and nitrogen mineralization Zhu, Biao; Gutknecht, Jessica L. M.; Herman, Donald J. Soil Biology and Biochemistry, Vol. 76 https://doi.org/10.1016/j.soilbio.2014.04.033	journal	September 2014
Soil Carbon Sequestration Impacts on Global Climate Change and Food Security Lal, R. Science, Vol. 304, Issue 5677 https://doi.org/10.1126/science.1097396	journal	June 2004
Microbial carbon limitation: The need for integrating microorganisms into our understanding of ecosystem carbon cycling Soong, Jennifer L.; Fuchslueger, Lucia; Marañon‐Jimenez, Sara Global Change Biology, Vol. 26, Issue 4 https://doi.org/10.1111/gcb.14962	journal	April 2020
Organo-mineral associations in temperate soils: Integrating biology, mineralogy, and organic matter chemistry Kögel-Knabner, Ingrid; Guggenberger, Georg; Kleber, Markus Journal of Plant Nutrition and Soil Science, Vol. 171, Issue 1 https://doi.org/10.1002/jpln.200700048	journal	February 2008
The role of root Exudates in Rhizosphere Interactions with Plants and Other Organisms Bais, Harsh P.; Weir, Tiffany L.; Perry, Laura G. Annual Review of Plant Biology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105159	journal	June 2006
Multiple models and experiments underscore large uncertainty in soil carbon dynamics Sulman, Benjamin N.; Moore, Jessica A. M.; Abramoff, Rose Biogeochemistry, Vol. 141, Issue 2 https://doi.org/10.1007/s10533-018-0509-z	journal	October 2018
The influence of organic and inorganic nutrient inputs on soil organic carbon functional groups content and maize yields Ndung'u, M.; Ngatia, L. W.; Onwonga, R. N. Heliyon, Vol. 7, Issue 8 https://doi.org/10.1016/j.heliyon.2021.e07881	journal	August 2021
Nutrient management and bioaugmentation interactively shape plant–microbe interactions in Miscanthus × giganteus Kane, Jennifer L.; Robinson, Marshall C.; Schartiger, Ronald G. GCB Bioenergy, Vol. 14, Issue 11 https://doi.org/10.1111/gcbb.13000	journal	September 2022
Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests Frey, S. D.; Ollinger, S.; Nadelhoffer, K. Biogeochemistry, Vol. 121, Issue 2 https://doi.org/10.1007/s10533-014-0004-0	journal	July 2014
Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees Chen, Weile; Koide, Roger T.; Adams, Thomas S. Proceedings of the National Academy of Sciences, Vol. 113, Issue 31 https://doi.org/10.1073/pnas.1601006113	journal	July 2016
Global soil organic carbon assessment Stockmann, Uta; Padarian, José; McBratney, Alex Global Food Security, Vol. 6 https://doi.org/10.1016/j.gfs.2015.07.001	journal	October 2015
Synthesis and modeling perspectives of rhizosphere priming Cheng, Weixin; Parton, William J.; Gonzalez-Meler, Miquel A. New Phytologist, Vol. 201, Issue 1 https://doi.org/10.1111/nph.12440	journal	August 2013
The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model Schimel, J. Soil Biology and Biochemistry, Vol. 35, Issue 4 https://doi.org/10.1016/S0038‐0717(03)00015‐4	journal	April 2003
Distinct bioenergetic signatures in particulate versus mineral-associated soil organic matter Williams, Elizabeth K.; Fogel, Marilyn L.; Berhe, Asmeret Asefaw Geoderma, Vol. 330 https://doi.org/10.1016/j.geoderma.2018.05.024	journal	November 2018
A rapid chloroform-fumigation extraction method for measuring soil microbial biomass carbon and nitrogen in flooded rice soils Witt, C.; Gaunt, J. L.; Galicia, C. C. Biology and Fertility of Soils, Vol. 30, Issue 5-6 https://doi.org/10.1007/s003740050030	journal	March 2000
The importance of anabolism in microbial control over soil carbon storage Liang, Chao; Schimel, Joshua P.; Jastrow, Julie D. Nature Microbiology, Vol. 2, Issue 8 https://doi.org/10.1038/nmicrobiol.2017.105	journal	July 2017
Conceptualizing soil organic matter into particulate and mineral‐associated forms to address global change in the 21st century Lavallee, Jocelyn M.; Soong, Jennifer L.; Cotrufo, M. Francesca Global Change Biology, Vol. 26, Issue 1 https://doi.org/10.1111/gcb.14859	journal	November 2019
Long‐term yields in annual and perennial bioenergy crops in the Midwestern United States Kantola, Ilsa B.; Masters, Michael D.; Blanc‐Betes, Elena GCB Bioenergy https://doi.org/10.1111/gcbb.12940	journal	April 2022
Plant- or microbial-derived? A review on the molecular composition of stabilized soil organic matter Angst, Gerrit; Mueller, Kevin E.; Nierop, Klaas G. J. Soil Biology and Biochemistry, Vol. 156 https://doi.org/10.1016/j.soilbio.2021.108189	journal	May 2021
Land use change to bioenergy: A meta-analysis of soil carbon and GHG emissions Harris, Z. M.; Spake, R.; Taylor, G. Biomass and Bioenergy, Vol. 82 https://doi.org/10.1016/j.biombioe.2015.05.008	journal	November 2015
Mineral protection of soil carbon counteracted by root exudates Keiluweit, Marco; Bougoure, Jeremy J.; Nico, Peter S. Nature Climate Change, Vol. 5, Issue 6 https://doi.org/10.1038/nclimate2580	journal	March 2015
The contentious nature of soil organic matter Lehmann, Johannes; Kleber, Markus Nature, Vol. 528, Issue 7580 https://doi.org/10.1038/nature16069	journal	November 2015
Effect of high soil C/N ratio and nitrogen limitation caused by the long-term combined organic-inorganic fertilization on the soil microbial community structure and its dominated SOC decomposition Cui, Jiwen; Zhu, Ruili; Wang, Xiya Journal of Environmental Management, Vol. 303 https://doi.org/10.1016/j.jenvman.2021.114155	journal	February 2022
Comparative Biogeochemical Cycles of Bioenergy Crops Reveal Nitrogen-Fixation and Low Greenhouse Gas Emissions in a Miscanthus × giganteus Agro-Ecosystem Davis, Sarah C.; Parton, William J.; Dohleman, Frank G. Ecosystems, Vol. 13, Issue 1 https://doi.org/10.1007/s10021‐009‐9306‐9	journal	December 2009
Priming mechanisms providing plants and microbes access to mineral-associated organic matter Jilling, Andrea; Keiluweit, Marco; Gutknecht, Jessica L. M. Soil Biology and Biochemistry, Vol. 158 https://doi.org/10.1016/j.soilbio.2021.108265	journal	July 2021
Soil carbon 4 per mille Minasny, Budiman; Malone, Brendan P.; McBratney, Alex B. Geoderma, Vol. 292 https://doi.org/10.1016/j.geoderma.2017.01.002	journal	April 2017
The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Cotrufo, M. Francesca; Wallenstein, Matthew D.; Boot, Claudia M. Global Change Biology, Vol. 19, Issue 4 https://doi.org/10.1111/gcb.12113	journal	February 2013
Isolating organic carbon fractions with varying turnover rates in temperate agricultural soils – A comprehensive method comparison Poeplau, Christopher; Don, Axel; Six, Johan Soil Biology and Biochemistry, Vol. 125 https://doi.org/10.1016/j.soilbio.2018.06.025	journal	October 2018

Similar Records

Plant litter traits control microbial decomposition and drive soil carbon stabilization

Journal Article · 2022 · Soil Biology and Biochemistry · OSTI ID:1894471

Ridgeway, Joanna; Morrissey, Ember; Brzostek, Edward

Missing links in the root-soil organic matter continuum

Journal Article · 2009 · New Phytologist · OSTI ID:1015681

O'Brien, Sarah L.; Iversen, Colleen M

Castanha et al. 2018: Hopland Lysimeter 13C-Labeled Root Litter Decomposition Study.

Dataset · 2022 · OSTI ID:1895464

Castanha, Cristina; Zhu, Biao; Hicks Pries, Caitlin; +2 more

Title: Roots selectively decompose litter to mine nitrogen and build new soil carbon

Citation Formats

References (48)

Similar Records

Related Subjects