A unifying framework for dinitrogen fixation in the terrestrial biosphere

Abstract

Dinitrogen (N2) fixation is widely recognized as an important process in controlling ecosystem responses to global environmental change, both today1 and in the past2; however, significant discrepancies exist between theory and observations of patterns of N2 fixation across major sectors of the land biosphere. A question remains as to why symbiotic N2-fixing plants are more abundant in vast areas of the tropics than in many of the mature forests that seem to be nitrogen-limited in the temperate and boreal zones3. Here we present a unifying framework for terrestrial N2 fixation that can explain the geographic occurrence of N2 fixers across diverse biomes and at the global scale. By examining trade-offs inherent in plant carbon, nitrogen and phosphorus capture, we find a clear advantage to symbiotic N2 fixers in phosphorus-limited tropical savannas and lowland tropical forests. The ability of N2 fixers to invest nitrogen into phosphorus acquisition seems vital to sustained N2 fixation in phosphorus-limited tropical ecosystems. In contrast, modern-day temperatures seem to constrain N2 fixation rates and N2-fixing species from mature forests in the high latitudes. We propose that an analysis that couples biogeochemical cycling and biophysical mechanisms is sufficient to explain the principal geographical patterns of symbiotic N2 fixation on land, thus providing a basis for predicting the response of nutrient-limited ecosystems to climate change and increasing atmospheric CO2.

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Figure 1: Temperature dependence of terrestrial nitrogenase activity.
Figure 2: Phosphatase enzyme rates in soils with and without N 2-fixing plants.
Figure 3: Model results for different hypotheses across terrestrial biomes at steady state.

References

  1. 1

    Hungate, B. A., Dukes, J. S., Shaw, M. R., Luo, Y. & Field, C. B. Nitrogen and climate change. Science 302, 1512–1513 (2003)

    Article  PubMed  Google Scholar 

  2. 2

    Falkowski, P. G. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387, 272–275 (1997)

    ADS  Article  Google Scholar 

  3. 3

    Crews, T. E. The presence of nitrogen fixing legumes in terrestrial communities: Evolutionary vs ecological considerations. Biogeochemistry 46, 233–246 (1999)

    Google Scholar 

  4. 4

    Redfield, A. C. The biological control of chemical factors in the environment. Am. Sci. 46, 205–221 (1958)

    Google Scholar 

  5. 5

    Deutsch, C., Sarmiento, J. L., Sigman, D. M., Gruber, N. & Dunne, J. P. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445, 163–167 (2007)

    ADS  Article  PubMed  Google Scholar 

  6. 6

    Schindler, D. W. Eutrophication and recovery in experimental lakes: implications for lake management. Science 184, 897–899 (1974)

    ADS  Article  PubMed  Google Scholar 

  7. 7

    Deutsch, C., Sigman, D. M., Thunell, R. C., Meckler, A. N. & Haug, G. H. Isotopic constraints on glacial/interglacial changes in the oceanic nitrogen budget. Glob. Biochem. Cycles 18 GB4012 (2004)

  8. 8

    Vitousek, P. M. & Howarth, R. W. Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13, 87–115 (1991)

    Article  Google Scholar 

  9. 9

    ter Steege, H. et al. Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443, 444–447 (2006)

    ADS  Article  PubMed  Google Scholar 

  10. 10

    Martinelli, L. A. et al. Nitrogen stable isotopic composition of leaves and soil: Tropical versus temperate forests. Biogeochemistry 46, 45–65 (1999)

    Google Scholar 

  11. 11

    Gutschick, V. P. Evolved strategies in nitrogen acquisition by plants. Am. Nat. 118, 607–637 (1981)

    Article  Google Scholar 

  12. 12

    Vitousek, P. M. & Field, C. B. Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochemistry 46, 179–202 (1999)

    Google Scholar 

  13. 13

    Rastetter, E. B. et al. Resource optimization and symbiotic nitrogen fixation. Ecosystems 4, 369–388 (2001)

    Article  Google Scholar 

  14. 14

    Dyhrman, S. T. et al. Phosphonate utilization by the globally important marine diazotroph Trichodesmium . Nature 439, 68–71 (2006)

    ADS  Article  PubMed  Google Scholar 

  15. 15

    Treseder, K. K. & Vitousek, P. M. Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82, 946–954 (2001)

    Article  Google Scholar 

  16. 16

    Duff, S. M. G., Sarath, G. & Plaxton, W. C. The role of acid phosphatases in plant phosphorus metabolism. Physiol. Plant. 90, 791–800 (1994)

    Article  Google Scholar 

  17. 17

    McGill, W. B. & Cole, C. V. Comparative aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26, 267–286 (1981)

    ADS  Article  Google Scholar 

  18. 18

    Olander, L. P. & Vitousek, P. M. Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49, 175–190 (2000)

    Article  Google Scholar 

  19. 19

    Vitousek, P. M. & Sanford, R. L. Nutrient cycling in moist tropical forest. Annu. Rev. Ecol. Syst. 17, 137–167 (1986)

    Article  Google Scholar 

  20. 20

    Ceuterick, F. et al. Effect of high pressure, detergents and phospholipase on the break in the Arrhenius plot of Azotobacter nitrogenase. Eur. J. Biochem. 87, 401–407 (1978)

    Article  PubMed  Google Scholar 

  21. 21

    Kamh, M., Abdou, M., Chude, V., Wiesler, F. & Horst, W. J. Mobilization of phosphorus contributes to positive rotational effects of leguminous cover crops on maize grown on soils from northern Nigeria. J. Plant Nutr. Soil Sci. 165, 566–572 (2002)

    Article  Google Scholar 

  22. 22

    Wang, Y. P., Houlton, B. Z. & Field, C. B. A model of biogeochemical cycles of carbon, nitrogen, and phosphorus including symbiotic nitrogen fixation and phosphatase production. Glob. Biogeochem. Cycles 21, GB1018 (2007)

    ADS  Article  Google Scholar 

  23. 23

    Bloom, A. J., Chapin, F. S. & Mooney, H. A. Resource limitation in plants—an economic analogy. Annu. Rev. Ecol. Syst. 16, 363–392 (1985)

    Article  Google Scholar 

  24. 24

    Lambers, H., Shane, M. W., Cramer, M. D., Pearse, S. J. & Veneklaas, E. J. Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann. Bot. 98, 693–713 (2006)

    Article  PubMed  PubMed Central  Google Scholar 

  25. 25

    Bormann, F. H. & Likens, G. E. Pattern and Process in a Forested Ecosystem (Springer, Berlin, 1979)

    Google Scholar 

  26. 26

    Houlton, B. Z. et al. Nitrogen dynamics in ice storm-damaged forest ecosystems: implications for nitrogen limitation theory. Ecosystems 6, 431–443 (2004)

    Article  Google Scholar 

  27. 27

    Cleveland, C. C. et al. Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Glob. Biogeochem. Cycles 13, 623–645 (1999)

    ADS  Article  Google Scholar 

  28. 28

    Chestnut, T. J., Zarin, D. J., McDowell, W. H. & Keller, M. A nitrogen budget for late-successional hillslope tabonuco forest, Puerto Rico Biogeochemistry 46, 85–108 (1999)

    Google Scholar 

  29. 29

    Pons, T. L., Perreijn, K., van Kessel, C. & Werger, M. J. A. Symbiotic nitrogen fixation in a tropical rainforest: 15N natural abundance measurements supported by experimental isotopic enrichment. New Phytol. 173, 154–167 (2007)

    Article  PubMed  Google Scholar 

  30. 30

    Sprent, J. I. & Raven, J. A. Evolution of nitrogen-fixing symbioses. Proc. Royal Society Edinburgh Section B-Biological Sciences 85, 215–237 (1985)

    Article  Google Scholar 

  31. 31

    Coxson, D. S. & Kershaw, K. A. Rehydration response of nitrogenase activity and carbon fixation in terrestrial Nostoc commune from Stipa–Bouteloa grassland. Can. J. Bot. 61, 2658–2668 (1983)

    Article  Google Scholar 

  32. 32

    Chapin, D. M., Bliss, L. C. & Bledsoe, L. J. Environmental regulation of nitrogen fixation in a high arctic lowland ecosystem. Can. J. Bot. 69, 2744–2755 (1991)

    Article  Google Scholar 

  33. 33

    Roper, M. M. Straw decomposition and nitrogenase activity (C2H2 reduction): Effects of soil moisture and temperature. Soil Biol. Biochem. 17, 65–71 (1985)

    Article  Google Scholar 

  34. 34

    Chan, Y.-K. Temperature response of an associative N2-fixing Pseudomonas species in pure culture. Can. J. Microbiol. 37, 715–718 (1991)

    Article  Google Scholar 

  35. 35

    Schomberg, H. H. & Weaver, R. W. Nodulation, nitrogen fixation, and early growth of arrowleaf clover in response to root temperature and starter nitrogen. Agron. J. 84, 1046–1050 (1992)

    Article  Google Scholar 

  36. 36

    Liengen, T. & Olsen, R. A. Seasonal and site-specific variations in nitrogen fixation in a high arctic area, Ny-Alesund, Spitsbergen. Can. J. Microbiol. 43, 759–769 (1997)

    Article  Google Scholar 

  37. 37

    Zou, X. M., Binkley, D. & Caldwell, B. A. Effects of dinitrogen fixing trees on phosphorus biogeochemical cycling in contrasting forests. Soil Sci. Soc. Am. J. 59, 1452–1458 (1995)

    ADS  Article  Google Scholar 

  38. 38

    Giardina, C. P., Huffman, S., Binkley, D. & Caldwell, B. A. Alders increase soil phosphorus availability in a Douglas-fir plantation. Can. J. Forest Res. 25, 1652–1657 (1995)

    Article  Google Scholar 

  39. 39

    Allison, S. D., Nielsen, C. & Hughes, R. F. Elevated enzyme activities in soils under the invasive nitrogen-fixing tree Falcataria moluccana . Soil Biol. Biochem. 38, 1537–1544 (2006)

    Article  Google Scholar 

  40. 40

    Caldwell, B. A. Effects of invasive scotch broom on soil properties in a Pacific coastal prairie soil. Appl. Soil Ecol. 32, 149–152 (2006)

    Article  Google Scholar 

  41. 41

    Nuruzzaman, M., Lambers, H., Bolland, M. D. A. & Veneklaas, E. J. Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant Soil 281, 109–120 (2006)

    Article  Google Scholar 

Download references

Acknowledgements

This work was funded by the National Science Foundation, CSIRO, the Australian Greenhouse Office, the David and Lucile Packard Foundation, and the US Department of Energy.

Author Contributions B.Z.H. wrote the initial manuscript. Y.P.W. and B.Z.H. performed the model simulations. All authors discussed the approach, organization and results, and developed and improved the manuscript.

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Correspondence to Benjamin Z. Houlton.

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The file contains Supplementary Notes and Supplementary Figures 1-2 with Legends, Supplementary Table 1 and additional references. (PDF 117 kb)

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Houlton, B., Wang, Y., Vitousek, P. et al. A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454, 327–330 (2008). https://doi.org/10.1038/nature07028

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