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Mineral protection of soil carbon counteracted by root exudates

Abstract

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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Figure 1: Proposed mechanisms for the exudate-induced acceleration of the microbial mineralization of native carbon (‘priming effects’) in the rhizosphere.
Figure 2: Exudate effects on artificial rhizosphere soil.
Figure 3: Exudate-induced effects on total soil C and protective mineral phases.
Figure 4: Exudate effect on metal–organic associations in the pore water.

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Acknowledgements

The authors thank A.L.D. Kilcoyne (ALS beamline 5.3.2.2), S.Y. Liu and M. Ahmed (ALS beamline 9.0.2) for their support. M.Keiluweit was supported by a Lawrence Scholar Fellowship awarded through Lawrence Livermore National Laboratory (LLNL). M.Kleber acknowledges support through Research Agreement No. 2014–1918 with the Institute of Soil Landscape Research, Leibniz-Center for Agricultural Landscape Research (ZALF), Müncheberg, Germany. This work was performed under the auspices of the US Department of Energy by LLNL under Contract DE-AC52-07NA27344. Funding was provided by LLNL LDRD ‘Microbes and Minerals: Imaging C Stabilization’ and a US DOE Genomics Science program award SA-DOE-29318 to J.P-R. The work of P.S.N. is supported by LBNL award No. IC006762 as sub-award from LLNL and DOE-BER Sustainable Systems SFA. The Advanced Light Source is supported by the Director, Office of Science, Office of Basic Energy Sciences, of the US DOE under Contract No. DE-AC02-05CH11231.

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M.Keiluweit performed microcosm set-up, laboratory analyses, synchrotron analyses, data analysis and wrote the manuscript. J.J.B. was responsible for DNA/RNA extractions and data processing. J.J.B. and P.K.W. conducted NanoSIMS analyses. M.Kleber., J.P-R., P.K.W. and P.S.N. supervised the project. All authors discussed the results and contributed to the manuscript.

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Correspondence to Marco Keiluweit.

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Keiluweit, M., Bougoure, J., Nico, P. et al. Mineral protection of soil carbon counteracted by root exudates. Nature Clim Change 5, 588–595 (2015). https://doi.org/10.1038/nclimate2580

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