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Temperature sensitivity of woody nitrogen fixation across species and growing temperatures

Nature Plants volume 8, pages 209–216 (2022)Cite this article

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Abstract

The future of the land carbon sink depends on the availability of nitrogen (N)1,2 and, specifically, on symbiotic N fixation3,4,5,6,7,8, which can rapidly alleviate N limitation. The temperature response of symbiotic N fixation has been hypothesized to explain the global distribution of N-fixing trees9,10 and is a key part of some terrestrial biosphere models (TBMs)3,7,8, yet there are few data to constrain the temperature response of symbiotic N fixation. Here we show that optimal temperatures for N fixation in four tree symbioses are in the range 29.0–36.9 °C, well above the 25.2 °C optimum currently used by TBMs. The shape of the response to temperature is also markedly different to the function used by TBMs (asymmetric rather than symmetric). We also show that N fixation acclimates to growing temperature (hence its range of optimal temperatures), particularly in our two tropical symbioses. Surprisingly, optimal temperatures were 5.2 °C higher for N fixation than for photosynthesis, suggesting that plant carbon and N gain are decoupled with respect to temperature. These findings may help explain why N-fixing tree abundance is highest where annual maximum temperatures are >35 °C (ref. 10) and why N-fixing symbioses evolved during a warm period in the Earth’s history11,12. Everything else being equal, our findings indicate that climate warming will probably increase N fixation, even in tropical ecosystems, in direct contrast to past projections8.

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Fig. 1: Temperature response of N fixation in four tree species (columns) grown under a range of growing temperatures (rows).
Fig. 2: Optimal temperatures for woody N fixation are 3.9–11.7 °C higher than previously estimated by Houlton et al.9 and 1.8–7.3 °C higher than net photosynthesis.
Fig. 3: Optimal temperatures and rates at low and high temperatures show thermal acclimation of N fixation and photosynthesis.
Fig. 4: Prolonged exposure to high temperatures causes reduction in N fixation at a predictable rate.

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Data availability

Data generated during this study are available on GitHub (https://github.com/tbytnero/Bytnerowicz-Akana-Griffin-Menge-N-fix-Temp; ref. 50).

Code availability

The R code with which data were analysed and figures created is available on GitHub (https://github.com/tbytnero/Bytnerowicz-Akana-Griffin-Menge-N-fix-Temp; ref. 50).

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Acknowledgements

We thank D. Tufts for assistance with the culture and preservation of bacteria, and the numerous friends at Columbia’s E3B department and Lamont-Doherty Earth Observatory who watered and fertilized plants. This publication was developed under STAR Fellowship Assistance Agreement no. FP91781501–0 awarded by the US Environmental Protection Agency (EPA) to T.A.B. Support was given by the Stengl-Wyer Scholars Program awarded by the University of Texas at Austin to T.A.B., by the National Science Foundation (NSF) Graduate Research Fellowship Program (no. DGE-2036197) to P.R.A. and by an NSF grant (no. DEB‐1457650) to D.N.L.M. This publication has not been formally reviewed by EPA. The views expressed in this publication are solely those of the authors, and EPA does not endorse any products or commercial services mentioned herein.

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Authors and Affiliations

  1. Department of Ecology, Evolution and Environmental Biology, Columbia University, New York, NY, USA

    Thomas A. Bytnerowicz, Palani R. Akana, Kevin L. Griffin & Duncan N. L. Menge

  2. Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA

    Thomas A. Bytnerowicz

  3. Department of Earth and Environmental Sciences, Columbia University, Palisades, NY, USA

    Kevin L. Griffin

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Contributions

T.A.B., K.L.G. and D.N.L.M. conceived of the project. T.A.B. and P.R.A. collected data. T.A.B. conducted analyses and wrote the initial draft. All authors contributed to writing.

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Correspondence to Thomas A. Bytnerowicz.

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Nature Plants thanks Yingping Wang and the other, anonymous, reviewers for their contribution to the peer review of this work.

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Supplementary text, Tables 1–14 and Figs. 1–17.

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Bytnerowicz, T.A., Akana, P.R., Griffin, K.L. et al. Temperature sensitivity of woody nitrogen fixation across species and growing temperatures. Nat. Plants 8, 209–216 (2022). https://doi.org/10.1038/s41477-021-01090-x

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