Mineral protection of soil carbon counteracted by root exudates [Root exudates counteract mineral control on soil carbon turnover]

Keiluweit, Marco; Bougoure, Jeremy J.; Nico, Peter S.; Pett-Ridge, Jennifer; Weber, Peter K.; Kleber, Markus

doi:10.1038/nclimate2580

Title: Mineral protection of soil carbon counteracted by root exudates [Root exudates counteract mineral control on soil carbon turnover]

Journal Article · Mon Mar 30 00:00:00 EDT 2015 · Nature Climate Change

DOI:https://doi.org/10.1038/nclimate2580· OSTI ID:1313557

Keiluweit, Marco ^[1]; Bougoure, Jeremy J. ^[2]; Nico, Peter S. ^[3]; Pett-Ridge, Jennifer ^[4]; Weber, Peter K. ^[4]; Kleber, Markus ^[5]

Oregon State Univ., Corvallis, OR (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States); Univ. of Western Australia, Western Australia (Australia)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Oregon State Univ., Corvallis, OR (United States); Leibnitz-Zentrum fur Agrarlandschaftsforschung (ZALF), Muncheberg (Germany)

Multiple lines of existing evidence suggest that climate change enhances root exudation of organic compounds into soils. Recent experimental studies show that increased exudate inputs may cause a net loss of soil carbon. This stimulation of microbial carbon mineralization ('priming') is commonly rationalized by the assumption that exudates provide a readily bioavailable supply of energy for the decomposition of native soil carbon (co-metabolism). Here we show that an alternate mechanism can cause carbon loss of equal or greater magnitude. We find that a common root exudate, oxalic acid, promotes carbon loss by liberating organic compounds from protective associations with minerals. By enhancing microbial access to previously mineral-protected compounds, this indirect mechanism accelerated carbon loss more than simply increasing the supply of energetically more favourable substrates. Our results provide insights into the coupled biotic-abiotic mechanisms underlying the 'priming' phenomenon and challenge the assumption that mineral-associated carbon is protected from microbial cycling over millennial timescales.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC52-07NA27344; AC02-05CH11231

OSTI ID:: 1313557

Alternate ID(s):: OSTI ID: 1512149

Report Number(s):: LLNL-JRNL-644153

Journal Information:: Nature Climate Change, Vol. 5, Issue 6; ISSN 1758-678X

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Intra-Annual Variation in Soil C, N and Nutrients Pools after Prescribed Fire in a Mississippi Longleaf Pine (Pinus palustris Mill.) Plantation Butnor, John R.; Johnsen, Kurt H.; Maier, Christopher A. Forests, Vol. 11, Issue 2 https://doi.org/10.3390/f11020181	journal	February 2020
Effect of Cover Crop on Carbon Distribution in Size and Density Separated Soil Aggregates Schaefer, Michael V.; Bogie, Nathaniel A.; Rath, Daniel Soil Systems, Vol. 4, Issue 1 https://doi.org/10.3390/soilsystems4010006	journal	January 2020
Direct uptake of organically derived carbon by grass roots and allocation in leaves and phytoliths: ¹³ C labeling evidence Alexandre, Anne; Balesdent, Jérôme; Cazevieille, Patrick Biogeosciences, Vol. 13, Issue 5 https://doi.org/10.5194/bg-13-1693-2016	journal	January 2016
High organic inputs explain shallow and deep SOC storage in a long-term agroforestry system – combining experimental and modeling approaches Cardinael, Rémi; Guenet, Bertrand; Chevallier, Tiphaine Biogeosciences, Vol. 15, Issue 1 https://doi.org/10.5194/bg-15-297-2018	journal	January 2018
Gone or just out of sight? The apparent disappearance of aromatic litter components in soils Klotzbücher, Thimo; Kalbitz, Karsten; Cerli, Chiara SOIL, Vol. 2, Issue 3 https://doi.org/10.5194/soil-2-325-2016	journal	January 2016
Citrate and malonate increase microbial activity and alter microbial community composition in uncontaminated and diesel-contaminated soil microcosms Martin, Belinda C.; George, Suman J.; Price, Charles A. SOIL, Vol. 2, Issue 3 https://doi.org/10.5194/soil-2-487-2016	journal	January 2016
Effects of altered dry season length and plant inputs on soluble soil carbon Homyak, Peter M.; Blankinship, Joseph C.; Slessarev, Eric W. Ecology, Vol. 99, Issue 10 https://doi.org/10.1002/ecy.2473	journal	August 2018
Impacts of an invasive grass on soil organic matter pools vary across a tree-mycorrhizal gradient Craig, Matthew E.; Lovko, Nadia; Flory, S. Luke Biogeochemistry, Vol. 144, Issue 2 https://doi.org/10.1007/s10533-019-00577-2	journal	June 2019
Interactive effects on organic matter processing from soils to the ocean: are priming effects relevant in aquatic ecosystems? Bengtsson, Mia M.; Attermeyer, Katrin; Catalán, Núria Hydrobiologia, Vol. 822, Issue 1 https://doi.org/10.1007/s10750-018-3672-2	journal	June 2018
Ecological role of bacterial inoculants and their potential impact on soil microbial diversity Ambrosini, Adriana; de Souza, Rocheli; Passaglia, Luciane M. P. Plant and Soil, Vol. 400, Issue 1-2 https://doi.org/10.1007/s11104-015-2727-7	journal	November 2015
More replenishment than priming loss of soil organic carbon with additional carbon input Liang, Junyi; Zhou, Zhenghu; Huo, Changfu Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05667-7	journal	August 2018
Global subsoil organic carbon turnover times dominantly controlled by soil properties rather than climate Luo, Zhongkui; Wang, Guocheng; Wang, Enli Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11597-9	journal	August 2019
Root exudate metabolomes change under drought and show limited capacity for recovery Gargallo-Garriga, Albert; Preece, Catherine; Sardans, Jordi Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-30150-0	journal	August 2018
Sampling roots to capture plant and soil functions Freschet, Grégoire T.; Roumet, Catherine Functional Ecology, Vol. 31, Issue 8 https://doi.org/10.1111/1365-2435.12883	journal	June 2017
Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome Pérez‐Izquierdo, Leticia; Zabal‐Aguirre, Mario; González‐Martínez, Santiago C. Journal of Ecology, Vol. 107, Issue 4 https://doi.org/10.1111/1365-2745.13202	journal	February 2019
Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes Tedersoo, Leho; Bahram, Mohammad Biological Reviews, Vol. 94, Issue 5 https://doi.org/10.1111/brv.12538	journal	May 2019
Microbial mechanisms of carbon priming effects revealed during the interaction of crop residue and nutrient inputs in contrasting soils Fang, Yunying; Nazaries, Loïc; Singh, Brajesh K. Global Change Biology, Vol. 24, Issue 7 https://doi.org/10.1111/gcb.14154	journal	April 2018
Molecular and Microscopic Insights into the Formation of soil Organic Matter in a red pine Rhizosphere Keller, C. Kent; Dohnalkova, A.; Tfaily, Malak M. GSA Annual Meeting in Seattle, Washington, USA - 2017, Geological Society of America Abstracts with Programs https://doi.org/10.1130/abs/2017am-307345	conference	January 2017
Effects of Organic Amendments on the Transformation of Fe (Oxyhydr)Oxides and Soil Organic Carbon Storage Wen, Yongli; Xiao, Jian; Goodman, Bernard A. Frontiers in Earth Science, Vol. 7 https://doi.org/10.3389/feart.2019.00257	journal	October 2019
Dynamics of deep soil carbon – insights from 14 C time series across a climatic gradient van der Voort, Tessa Sophia; Mannu, Utsav; Hagedorn, Frank Biogeosciences, Vol. 16, Issue 16 https://doi.org/10.5194/bg-16-3233-2019	journal	January 2019
Soil CO₂ efflux in an old-growth southern conifer forests (Agathis australis) – magnitude, components, and controls Schwendenmann, Luitgard; Macinnis-Ng, Cate SOIL https://doi.org/10.5194/soil-2016-21	posted_content	April 2016
Constraining carbon and nutrient flows in soil with ecological stoichiometry Buchkowski, Robert; Shaw, Alanna; Sihi, Debjani Zenodo https://doi.org/10.5281/zenodo.3464584	text	January 2019
Molecular and Microscopic Insights into the Formation of Soil Organic Matter in a Red Pine Rhizosphere Dohnalkova, Alice; Tfaily, Malak; Smith, A. Soils, Vol. 1, Issue 1 https://doi.org/10.3390/soils1010004	journal	August 2017
Scientists’ warning to humanity: microorganisms and climate change Cavicchioli, Ricardo; Ripple, William J.; Timmis, Kenneth N. ETH Zurich https://doi.org/10.3929/ethz-b-000350779	text	January 2019
Elevated moisture stimulates carbon loss from mineral soils by releasing protected organic matter Huang, Wenjuan; Hall, Steven J. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01998-z	journal	November 2017
High organic inputs explain shallow and deep SOC storage in a long-term agroforestry system – Combining experimental and modeling approaches. Cardinael, Rémi; Guenet, Bertrand; Chevallier, Tiphaine Biogeosciences https://doi.org/10.5194/bg-2017-125	posted_content	April 2017
Gone or just out of sight? The apparent disappearance of aromatic litter components in soils Klotzbücher, T.; Kalbitz, K.; Cerli, C. SOIL https://doi.org/10.5194/soil-2015-79	posted_content	January 2016
Effect of ground water level on the release of carbon, nitrogen and phosphorus during decomposition of Carex. cinerascens Kükenth in the typical seasonal floodplain in dry season Zhang, Quanjun; Zhang, Guangshuai; Yu, Xiubo Journal of Freshwater Ecology, Vol. 34, Issue 1 https://doi.org/10.1080/02705060.2019.1584128	journal	January 2019
Soil CO ₂ efflux in an old-growth southern conifer forest ( Agathis australis ) – magnitude, components and controls Schwendenmann, Luitgard; Macinnis-Ng, Cate SOIL, Vol. 2, Issue 3 https://doi.org/10.5194/soil-2-403-2016	journal	January 2016
Constraining carbon and nutrient flows in soil with ecological stoichiometry Buchkowski, Robert; Shaw, Alanna; Sihi, Debjani Zenodo https://doi.org/10.5281/zenodo.3464585	text	January 2019
Spatial Heterogeneity of SOM Concentrations Associated with White-rot Versus Brown-rot Wood Decay Bai, Zhen; Ma, Qiang; Dai, Yucheng Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-14181-7	journal	October 2017
Differential effects of conifer and broadleaf litter inputs on soil organic carbon chemical composition through altered soil microbial community composition Wang, Hui; Liu, Shi-Rong; Wang, Jing-Xin Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep27097	journal	June 2016
Optimizing rice plant photosynthate allocation reduces N2O emissions from paddy fields Jiang, Yu; Huang, Xiaomin; Zhang, Xin Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep29333	journal	July 2016
Microbial respiration, but not biomass, responded linearly to increasing light fraction organic matter input: Consequences for carbon sequestration Rui, Yichao; Murphy, Daniel V.; Wang, Xiaoli Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep35496	journal	October 2016