Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Nitrification by plants that also fix nitrogen

Nature volume 430, pages 98–101 (2004)Cite this article

Abstract

Nitrification is a key stage in the nitrogen cycle; it enables the transformation of nitrogen into an oxidized, inorganic state1,2. The availability of nitrates produced by this process often limits primary productivity and is an important determinant in plant community ecology and biodiversity3,4,5,6. Chemoautotrophic prokaryotes are recognized as the main facilitators of this process7, although heterotrophic nitrification by fungi may be significant under certain conditions8. However, there has been neither biochemical nor ecological evidence to support nitrification by photoautotrophic plants. Here we show how certain legumes that accumulate the toxin, 3-nitropropionic acid, generate oxidized inorganic nitrogen in their shoots, which is returned to the soil in their litter. In nitrogen-fixing populations this ‘new’ nitrate and nitrite can be derived from the assimilation of nitrogen gas. Normally, the transformation of elemental nitrogen from the atmosphere into a fixed oxidized form (as nitrate) is represented in the nitrogen cycle as a multiphasic process involving several different organisms. We show how this can occur in a single photoautotrophic organism, representing a previously undescribed feature of this biogeochemical cycle.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Nitrogen assimilation and photoautotrophic nitrification in legumes.

Similar content being viewed by others

References

  1. Focht, D. D. & Verstraete, W. Biochemical ecology of nitrification and denitrification. Adv. Microb. Ecol. 1, 135–214 (1977)

    Article  CAS  Google Scholar 

  2. Sprent, J. I. The Ecology of the Nitrogen Cycle (Cambridge Univ. Press, Cambridge, 1987)

    Google Scholar 

  3. Chapin, F. S. The mineral nutrition of wild plants. Annu. Rev. Ecol. Syst. 11, 233–260 (1980)

    Article  CAS  Google Scholar 

  4. Berendse, F. Interspecific competition and niche differentiation between Plantago lanceolata and Anthoxanthum odoratum in a natural hayfield. J. Ecol. 78, 413–427 (1983)

    Article  Google Scholar 

  5. Verhoeven, J. T. A., Koerselman, W. & Meuleman, A. F. M. Nitrogen or phosphorus-limited growth in herbaceous, wet vegetation: relations with atmospheric inputs and management regimes. Trends Ecol. Evol. 11, 494–497 (1996)

    Article  CAS  Google Scholar 

  6. Wedin, D. A. & Tilman, D. Influence of nitrogen loading and species composition on carbon balance of grasslands. Science 274, 1720–1721 (1996)

    Article  ADS  CAS  Google Scholar 

  7. Macdonald, R. M. in Nitrification (ed. Prosser, J. I.) 1–16 (IRL, Oxford, 1986)

    Google Scholar 

  8. Killham, K. in Nitrification (ed. Prosser, J. I.) 117–126 (IRL, Oxford, 1986)

    Google Scholar 

  9. Gustine, D. L. Aliphatic nitrocompounds in Crown Vetch: A review. Crop Sci. 19, 197–203 (1979)

    Article  Google Scholar 

  10. Williams, M. C. & Barneby, R. C. The occurrence of nitro-toxins in North American Astragalus (Fabaceae). Brittonia 29, 310–326 (1977)

    Article  CAS  Google Scholar 

  11. Williams, M. C. & Barneby, R. C. The occurrence of nitro-toxins in old world and South American Astragalus (Fabaceae). Brittonia 29, 327–331 (1977)

    Article  CAS  Google Scholar 

  12. Williams, M. C. Nitrocompounds in Indigofera species. Agron. J. 73, 434–436 (1981)

    Article  CAS  Google Scholar 

  13. Williams, M. C. Toxic nitro compounds in Lotus. Agron. J. 75, 520–522 (1983)

    Article  CAS  Google Scholar 

  14. Salem, M. A., Williams, M., Wainwright, S. J. & Hipkin, C. R. Nitroaliphatic compounds in Hippocrepis comosa and other legumes in the European flora. Phytochemistry 40, 89–91 (1995)

    Article  CAS  Google Scholar 

  15. Simpson, D. J., Wainwright, S. J. & Hipkin, C. R. Presence of 3-nitropropionic acid in widely distributed pasture legumes in Britain. Vet. Rec. 145, 169–171 (1999)

    Article  CAS  Google Scholar 

  16. Alston, T. A., Porter, D. J. T. & Bright, H. J. Enzyme inhibition by nitro and nitroso compounds. Acc. Chem. Res. 16, 418–424 (1983)

    Article  CAS  Google Scholar 

  17. Hipkin, C. R., Salem, M. A., Simpson, D. & Wainwright, S. J. 3-nitropropionic acid oxidase from horseshoe vetch (Hippocrepis comosa): a novel plant enzyme. Biochem. J. 340, 491–495 (1999)

    Article  CAS  Google Scholar 

  18. Dijkstra, P. et al. Nitrogen stable isotope composition of leaves and roots of plants growing in a forest and a meadow. Isotopes Environ. Health Stud. 39, 29–39 (2003)

    Article  CAS  Google Scholar 

  19. Baxter, R. L. et al. Fungal biosynthesis of 3-nitropropionic acid. J. Chem. Soc. Perkin Trans. 1, 2495–2501 (1992)

    Article  Google Scholar 

  20. Rehder, H. & Schäfer, A. Nutrient turnover studies in alpine ecosystems. IV. Communities of the Central Alps and comparative survey. Oecologia 34, 309–327 (1978)

    Article  ADS  CAS  Google Scholar 

  21. Pastor, J., Stillwell, M. A. & Tilman, D. Nitrogen mineralization and nitrification in four Minnesota old fields. Oecologia 71, 481–485 (1987)

    Article  ADS  CAS  Google Scholar 

  22. Morecroft, M. D., Marrs, R. M. & Woodward, F. I. Altitudinal and seasonal trends in soil nitrogen mineralization rate in the Scottish Highlands. J. Ecol. 80, 49–56 (1992)

    Article  Google Scholar 

  23. Shearer, G. & Kohl, D. H. N2-fixation in field settings: Estimations based on natural 15N abundance. Aust. J. Plant Physiol. 13, 699–756 (1986)

    CAS  Google Scholar 

  24. Arnon, D. I. & Hoagland, D. R. Crop production in artificial culture solutions and in soils, with special reference to factors influencing yield and absorption of inorganic nutrients. Soil Sci. 50, 463–483 (1940)

    CAS  Google Scholar 

  25. Matsumoto, H., Unrau, A. M., Hylin, J. W. & Temple, B. Spectrophotometric determination of 3-nitropropionic acid in biological extracts. Anal. Chem. 33, 1442–1444 (1961)

    Article  CAS  Google Scholar 

  26. Everest, S. A., Hipkin, C. R. & Syrett, P. J. The effect of phosphate and flavin adenine dinucleotide on nitrate reductase activity of some unicellular marine algae. J. Exp. Mar. Biol. Ecol. 76, 263–275 (1984)

    Article  CAS  Google Scholar 

  27. Parsons, T. R., Maita, Y. & Lalli, C. M. A Manual of Chemical and Biological Methods for Seawater Analysis (Pergamon, Oxford, 1984)

    Google Scholar 

Download references

Acknowledgements

We thank R. Williams, D. Knight, R. Jones and K. Flynn for their assistance. M.A.S. thanks the Libyan government for financial support. The following botanic gardens supplied seed: Akureyri, Iceland; Bayreuth, Germany; Bern, Switzerland; Bonn, Germany; Bordeaux, France; Bratislava, Slovakia; Caen, France; Cambridge, UK; Dresden, Germany; Firenze, Italy; Halle, Germany; Hamburg, Germany; Innsbruck, Austria; Jenna, Germany; L'Aquila, Italy; Latte, Italy; Leicester, UK; Leipsig, Germany; Lisbon, Portugal; Oldenburg, Germany; Oxford, UK; Padova, Italy; Rouen, France; Sienna, Italy; Strasbourg, France; and Urbino, Italy.

Author information

Author notes

  1. Deborah J. Simpson

    Present address: Cardiff School of Biosciences, Cardiff University, Cardiff, CF10 3TL, UK

  2. Mansour A. Salem

    Present address: Faculty of Engineering and Technology, Sebha University, Sebha, Libya

  3. Charles R. Hipkin and Deborah J. Simpson: These authors contributed equally to this work.

Authors and Affiliations

  1. School of Biological Sciences, University of Wales Swansea, Institute of Environmental Sustainability, SA2 8PP, Swansea, UK

    Charles R. Hipkin, Deborah J. Simpson, Stephen J. Wainwright & Mansour A. Salem

Authors
  1. Charles R. Hipkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Deborah J. Simpson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephen J. Wainwright
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mansour A. Salem
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Charles R. Hipkin.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Notes

Contains information about the production of 3-nitropropionic acid, nitrate and nitrite by axenic cultures of horseshoe vetch, including a photograph of a seedling growing in sterile culture. (DOC 38 kb)

Supplementary Table 1

The proportions of nitrate and nitrite in fresh leaves, senescing leaves and litter of 3NPA-containing species. (DOC 25 kb)

Supplementary Table 2

The amino acid contents of horseshoe vetch and white clover, in water culture and natural populations. (DOC 21 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hipkin, C., Simpson, D., Wainwright, S. et al. Nitrification by plants that also fix nitrogen. Nature 430, 98–101 (2004). https://doi.org/10.1038/nature02635

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02635

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing