A plant–microbe interaction framework explaining nutrient effects on primary production

Abstract

In most terrestrial ecosystems, plant growth is limited by nitrogen and phosphorus. Adding either nutrient to soil usually affects primary production, but their effects can be positive or negative. Here we provide a general stoichiometric framework for interpreting these contrasting effects. First, we identify nitrogen and phosphorus limitations on plants and soil microorganisms using their respective nitrogen to phosphorus critical ratios. Second, we use these ratios to show how soil microorganisms mediate the response of primary production to limiting and non-limiting nutrient addition along a wide gradient of soil nutrient availability. Using a meta-analysis of 51 factorial nitrogen–phosphorus fertilization experiments conducted across multiple ecosystems, we demonstrate that the response of primary production to nitrogen and phosphorus additions is accurately predicted by our stoichiometric framework. The only pattern that could not be predicted by our original framework suggests that nitrogen has not only a structural function in growing organisms, but also a key role in promoting plant and microbial nutrient acquisition. We conclude that this stoichiometric framework offers the most parsimonious way to interpret contrasting and, until now, unresolved responses of primary production to nutrient addition in terrestrial ecosystems.

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Fig. 1: Concept of nutrient limitation.
Fig. 2: Consequences of differential plant and microbial nutrient limitations.
Fig. 3: Correspondence between the theory and published data.

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Acknowledgements

This study was supported by the International Program CryoCARB (MSM 7E10073—CryoCARB, Austrian Science Fund (FWF): I370-B17, German Federal Ministry of Education and Research (03F0616A)), project no. GA17-15229S and the SoWa Research Infrastructure funded by MEYS CZ grants LM2015075 and EF16_013/0001782—SoWa Ecosystems Research. S.M. acknowledges support from the Swedish Research Councils, Formas (2015-468) and VR (2016-04146) and the Bolin Centre for Climate Research. J.B., T.U. and H.S. were also supported by Czech Science Foundation project no. 16-18453 S. G.H. acknowledges the Joint Partnership Initiative project COUP and the Swedish Research Council grant no. E0689701 and the project CryoN funded by Academy of Finland (no. 132045). P.C. would also like to thank TES program of the U.S. Department of Energy (DOE) Office of Science, Biological and Environmental Research (BER) for partial support at Pacific Northwest National Laboratory (PNNL). PNNL is operated by Battelle for DOE. X. Xu kindly shared his dataset on microbial biomass elemental composition. We also thank N. Hess and B. Bond-Lamberty for comments and language corrections to this manuscript.

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P.C. collected data for meta-analysis and wrote the manuscript. P.C., S.M. and H.S. developed the conceptual framework. Other co-authors conducted a thorough critical review of the manuscript and contributed to manuscript writing.

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Correspondence to Petr Čapek.

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Supplementary Table 1

List of studies used in the meta-analysis with corresponding variables extracted from each study (ecosystem type, measured plant characteristic, soil N/P and C/N ratio, microbial critical N/P and C/N ratio, plant critical N/P ratio and dominant plant–microbe relationship).

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Statistical meta-analysis

Step-by-step statistical meta-analysis with detailed additional information.

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Čapek, P., Manzoni, S., Kaštovská, E. et al. A plant–microbe interaction framework explaining nutrient effects on primary production. Nat Ecol Evol 2, 1588–1596 (2018). https://doi.org/10.1038/s41559-018-0662-8

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