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

Nature Ecology & Evolution volume 2, pages 1588–1596 (2018)Cite this article

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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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Authors and Affiliations

  1. Pacific Northwest National Laboratory, Environmental Molecular Sciences Laboratory, Richland, WA, USA

    Petr Čapek

  2. Department of Physical Geography, Stockholm University, Stockholm, Sweden

    Stefano Manzoni, Gustaf Hugelius & Juri Palmtag

  3. Bolin Centre for Climate Research, Stockholm University, Stockholm, Sweden

    Stefano Manzoni, Birgit Wild, Gustaf Hugelius & Juri Palmtag

  4. Department of Ecosystem Biology, University of South Bohemia, České Budějovice, Czech Republic

    Eva Kaštovská, Kateřina Diáková, Jiří Bárta & Hana Šantrůčková

  5. Department of Environmental Science and Analytical Chemistry, Stockholm University, Stockholm, Sweden

    Birgit Wild

  6. Department of Microbiology and Ecosystem Science, University of Vienna, Vienna, Austria

    Jörg Schnecker & Andreas Richter

  7. Department of Environmental and Biological Sciences, University of Eastern Finland, Kuopio, Finland

    Christina Biasi & Pertti J. Martikainen

  8. Department of Ecogenomics and Systems Biology, University of Vienna, Vienna, Austria

    Ricardo Jorge Eloy Alves & Christa Schleper

  9. Institute of Soil Science, Leibniz Universität Hannover, Hannover, Germany

    Georg Guggenberger, Norman Gentsch & Olga Shibistova

  10. Soil Science and Soil Protection, Martin Luther University Halle-Wittenberg, Halle, Germany

    Robert Mikutta

  11. Institute of Microbiology, University of Greifswald, Greifswald, Germany

    Tim Urich

  12. Institute for Applied Systems Analysis, Ecosystems Services and Management Program, IIASA, Laxenburg, Austria

    Andreas Richter

Authors
  1. Petr Čapek
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  2. Stefano Manzoni
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  3. Eva Kaštovská
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  4. Birgit Wild
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  5. Kateřina Diáková
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  6. Jiří Bárta
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  7. Jörg Schnecker
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  8. Christina Biasi
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  9. Pertti J. Martikainen
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  10. Ricardo Jorge Eloy Alves
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  11. Georg Guggenberger
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  12. Norman Gentsch
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  13. Gustaf Hugelius
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  14. Juri Palmtag
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  15. Robert Mikutta
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  16. Olga Shibistova
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  17. Tim Urich
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  18. Christa Schleper
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  19. Andreas Richter
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  20. Hana Šantrůčková
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Contributions

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.

Corresponding author

Correspondence to Petr Čapek.

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The authors declare no competing interests.

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Supplementary information

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).

Reporting Summary

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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  • DOI: https://doi.org/10.1038/s41559-018-0662-8

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