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Microbial formation of stable soil carbon is more efficient from belowground than aboveground input

Abstract

The relative contributions of aboveground versus belowground plant carbon inputs to the stable soil organic carbon pool are the subject of much debate—with direct implications for how the carbon cycle is modelled and managed. The belowground rhizosphere pathway (that is, carbon exiting the living root) is theorized to form stable soil carbon more efficiently than the aboveground pathway. However, while several mechanisms have been invoked to explain this efficiency, few have been empirically tested or quantified. Here, we use soil microcosms with standardized carbon inputs to investigate three posited mechanisms that differentiate aboveground from belowground input pathways of dissolved organic carbon—through the microbial biomass—to the mineral-stabilized soil organic carbon pool: (1) the physical distance travelled, (2) the microbial abundance in the region in which a carbon compound enters (that is, rhizosphere versus bulk soil) and (3) the frequency and volume of carbon delivery (that is, infrequent ‘pulse’ versus frequent ‘drip’). We demonstrate that through the microbial formation pathway, belowground inputs form mineral-stabilized soil carbon more efficiently than aboveground inputs, partly due to the greater efficiency of formation by the rhizosphere microbial community relative to the bulk soil community. However, we show that because the bulk soil has greater capacity to form mineral-stabilized soil carbon due to its greater overall volume, the relative contributions of aboveground versus belowground carbon inputs depend strongly on the ratio of rhizosphere to bulk soil.

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Fig. 1: Proposed mechanisms favouring the efficiency of the belowground versus aboveground pathway in the DOC-microbial route to mineral stabilization.
Fig. 2: The formation of stable 13C-MASOC in a whole microcosm.
Fig. 3: The concentration of stable 13C-MASOC formed per gram of rhizosphere or bulk soil.
Fig. 4: Follow-up assay with field-isolated rhizosphere and bulk soil microbial communities.
Fig. 5: Projections of the relative importance of aboveground leachate DOC versus belowground root exudate DOC across a range of typical rhizosphere-to-bulk ratios.

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Data availability

Experimental data in support of these findings are available at https://github.com/NoahSokol/root-pathway-efficiency.

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Acknowledgements

We thank E. Iturbe for assistance with the figures, M. Keiluweit for input on microcosm design and J. Sanderman, D. Rasse and C. Chenu for discussion during the planning stages of the experiment. We also thank E. Karlsen-Ayala and C. Lombroso for assistance with laboratory work. Funding was provided to N.W.S. from the National Science and Engineering Research Council of Canada, the Yale Institute for Biospheric Studies and a Doctoral Dissertation Improvement Grant from the National Science Foundation.

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N.W.S. and M.A.B. conceived the project. N.W.S. designed and led the research and analysed the data. N.W.S. wrote the manuscript, with contributions from M.A.B.

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Correspondence to Noah W. Sokol.

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Sokol, N.W., Bradford, M.A. Microbial formation of stable soil carbon is more efficient from belowground than aboveground input. Nature Geosci 12, 46–53 (2019). https://doi.org/10.1038/s41561-018-0258-6

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