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Grassland responses to elevated CO2 determined by plant–microbe competition for phosphorus

Nature Geoscience volume 16, pages 704–709 (2023)Cite this article

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Abstract

Rising atmospheric CO2 has stimulated plant productivity, with terrestrial ecosystems currently absorbing nearly one-third of anthropogenic CO2 emissions. Increases in photosynthesis can subsequently lead to increased carbon (C) storage in plants and soil. However, there is growing evidence that nitrogen (N) availability constrains elevated CO2 (eCO2) responses, yet we know much less about the role of phosphorus (P) limitation on productivity under eCO2. This is important because P-limited ecosystems are globally widespread, and the biogeochemical cycles of N and P differ fundamentally. In the Peak District National Park of northern England, we conducted a free-air CO2 enrichment (FACE) experiment for three years on two contrasting P-limited grasslands under long-term nutrient manipulation. Here we show that competition between plants and microbes for P can determine plant productivity responses to eCO2. In a limestone grassland, aboveground productivity increased (16%) and microbial biomass P remained unchanged, whereas in an acidic grassland, aboveground productivity and P uptake declined (11% and 20%, respectively), but P immobilization into microbial biomass increased (36%). Our results demonstrate that strong competition with microbes can cause plant P uptake to decline under eCO2, with implications for the future productivity of P-limited ecosystems in response to climate change.

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Fig. 1: Contrasting aboveground shoot productivity responses to CO2.
Fig. 2: Relationship between bicarbonate-extractable total P, as determined by inductively coupled plasma-optical emission spectroscopy, and aboveground biomass.
Fig. 3: Contrasting ratio on a log scale of AGBP to MBP.

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Data availability

Data used to produce this paper are available via the EIDC data repository https://doi.org/10.5285/35921c93-2d9e-4e35-8de5-adbfc37641b4.

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Acknowledgements

This work was funded by the Natural Environment Research Council (grant number NE/N0100086/1 to I.P.H. and NE/N010132/1 to G.K.P.) as part of the Phosphorus Limitation And ecosystem responses to Carbon dioxide Enrichment (PLACE) project. We thank Natural England for access to their Wardlow SSSI, S. Taylor (Natural England) for help with monolith extraction and transport and the Peak Park authority for permission to establish the miniFACE experiment within the Peak District National Park. We are grateful to G. McClean for work in establishing the experiment and C. Hook, I. Johnson and E. Paton for P analyses. For the purpose of open access, the author(s) has applied a Creative Commons Attribution (CC BY) licence (where permitted by UKRI, ‘Open Government Licence’ or ‘Creative Commons Attribution No-derivatives (CC BY-ND) licence’ may be stated instead) to any Author Accepted Manuscript version arising.

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Authors and Affiliations

  1. Plants Photosynthesis and Soil, School of Biosciences, University of Sheffield, Sheffield, UK

    J. Ben Keane, Christopher R. Taylor, Jonathan R. Leake & Gareth K. Phoenix

  2. Department of Environment and Geography, University of York, York, UK

    J. Ben Keane

  3. Geography, Faculty of Environment, Science and Economy, University of Exeter, Exeter, UK

    Iain P. Hartley

  4. Soil and Ecosystem Ecology, Earth and Environmental Sciences, University of Manchester, Manchester, UK

    Christopher R. Taylor

  5. Soil Chemistry, Wageningen University, Wageningen, the Netherlands

    Marcel R. Hoosbeek

  6. Istituto Di Biometeorologia–Consiglio Nazionale Delle Ricerche, Sede centrale, Florence, Italy

    Franco Miglietta

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Contributions

I.P.H., G.K.P., J.B.K., J.R.L. and M.R.H. designed the eCO2 experiment. G.K.P., I.P.H., F.M., J.B.K. and C.R.T. installed the FACE system and the mesocosms. J.B.K. and C.R.T. oversaw the operation and maintenance of the experiment. Lab analyses were undertaken by J.B.K. and C.R.T., and J.B.K. performed the data analyses. J.B.K., G.K.P. and I.P.H. wrote the original draft of the manuscript, and all authors contributed to subsequent revisions.

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Correspondence to J. Ben Keane.

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Nature Geoscience thanks Benjamin Turner and Carlo Calfapietra for their contribution to the peer review of this work. Primary Handling Editor: Xujia Jiang, in collaboration with the Nature Geoscience team.

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Extended data

Extended Data Fig. 1 Contrasting aboveground productivity responses to CO2.

Grasslands were exposed to ambient (a- dark green bars and filled circles) or elevated CO2 at 600 ppm (e-light green bars and filled circles), in acidic, (left hand column) and limestone grasslands, (right hand column). Data show means (± SE) in time series (n = 5) and cumulative productivity (n = 5) over the study period. Vertical arrows denote the start of CO2 fumigation.

Extended Data Fig. 2 Soil microbial biomass P (MBP) responses to CO2.

Grasslands were exposed to ambient (a- dark green bars and filled circles) or elevated CO2 at 600 ppm (e-light green bars and filled circles), in acidic, (left hand column) and limestone grasslands, (right hand column). Data show means (± SE) in time series (n = 5) and overall mean MBP (n = 5) over the study period. Vertical arrows denote start of CO2 fumigation.

Extended Data Table 1 Bulk density of two grassland soils under long-term nutrient treatments
Full size table

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Ben Keane, J., Hartley, I.P., Taylor, C.R. et al. Grassland responses to elevated CO2 determined by plant–microbe competition for phosphorus. Nat. Geosci. 16, 704–709 (2023). https://doi.org/10.1038/s41561-023-01225-z

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