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Doubling of marine dinitrogen-fixation rates based on direct measurements

Nature volume 488, pages 361–364 (2012)Cite this article

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Abstract

Biological dinitrogen fixation provides the largest input of nitrogen to the oceans, therefore exerting important control on the ocean's nitrogen inventory and primary productivity1,2,3. Nitrogen-isotope data from ocean sediments suggest that the marine-nitrogen inventory has been balanced for the past 3,000 years (ref. 4). Producing a balanced marine-nitrogen budget based on direct measurements has proved difficult, however, with nitrogen loss exceeding the gain from dinitrogen fixation by approximately 200 Tg N yr−1 (refs 5, 6). Here we present data from the Atlantic Ocean and show that the most widely used method of measuring oceanic N2-fixation rates7 underestimates the contribution of N2-fixing microorganisms (diazotrophs) relative to a newly developed method8. Using molecular techniques to quantify the abundance of specific clades of diazotrophs in parallel with rates of 15N2 incorporation into particulate organic matter, we suggest that the difference between N2-fixation rates measured with the established method7 and those measured with the new method8 can be related to the composition of the diazotrophic community. Our data show that in areas dominated by Trichodesmium, the established method underestimates N2-fixation rates by an average of 62%. We also find that the newly developed method yields N2-fixation rates more than six times higher than those from the established method when unicellular, symbiotic cyanobacteria and γ-proteobacteria dominate the diazotrophic community. On the basis of average areal rates measured over the Atlantic Ocean, we calculated basin-wide N2-fixation rates of 14 ± 1 Tg N yr−1 and 24 ±1 Tg N yr−1 for the established and new methods, respectively. If our findings can be extrapolated to other ocean basins, this suggests that the global marine N2-fixation rate derived from direct measurements may increase from 103 ± 8 Tg N yr−1 to 177 ± 8 Tg N yr−1, and that the contribution of N2 fixers other than Trichodesmium is much more significant than was previously thought.

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Figure 1: Sampling sites and sea surface temperature.
Figure 2: Comparison between bubble-addition and dissolution methods.
Figure 3: Mixed-layer inventory of N 2 -fixation rates in the tropical and equatorial Atlantic Ocean.
Figure 4: Relative abundance of various phylotypes of diazotrophic bacteria from the same stations as the N 2 -fixation rate measurements, estimated with TaqMan nifH gene assays.

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Acknowledgements

We thank G. Klockgether and T. Max for mass-spectrometry measurements. We thank S. Fehsenfeld for helping with sampling and H. Nurlaeli for experimental work on Nodularia. We also thank the captain and crew of RV Meteor and RV Polarstern, as well as the chief scientists, P. Brandt and A. Macke. We thank D. Desai for statistical analyses. This work is a contribution of the Sonderforschungsbereich 754 ‘Climate — Biogeochemistry Interactions in the Tropical Ocean’, which is supported by the Deutsche Forschungsgemeinschaft. We thank the Max Planck Gesellschaft for financial support. We thank the Bundesministerium für Bildung und Forschung (BMBF) for financial support through the SOPRAN II (Surface Ocean Processes in the Anthropocene) project, grant number 03F0611A.

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Author notes

  1. Wiebke Mohr & Julie LaRoche

    Present address: Present addresses: Harvard University, Department of Earth and Planetary Sciences, 20 Oxford Street, Cambridge, Massachusetts 02138, USA (W.M.); Department of Biology, Dalhousie University, 1355 Oxford Street, PO Box 1500, Halifax, Nova Scotia B3H 4R2, Canada (J.L.R.).,

  2. Tobias Großkopf and Wiebke Mohr: These authors contributed equally to this work.

Authors and Affiliations

  1. Helmholtz Centre for Ocean Research Kiel (GEOMAR), Düsternbrooker Weg 20, 24105 Kiel, Germany,

    Tobias Großkopf, Wiebke Mohr, Tina Baustian, Harald Schunck, Diana Gill & Julie LaRoche

  2. Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany,

    Marcel M. M. Kuypers & Gaute Lavik

  3. Institute for General Microbiology, Christian-Albrechts University Kiel, Am Botanischen Garten 1–9, 24118 Kiel, Germany,

    Ruth A. Schmitz

  4. Oceanography Department, Dalhousie University, 1355 Oxford Street, PO Box 15000, Halifax, Nova Scotia, B3H 4R2, Canada,

    Douglas W. R. Wallace

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Contributions

W.M. designed the dissolution method. T.G., T.B., H.S. and D.G. collected samples and performed nifH gene quantification. M.M.M.K. and G.L. did the measurements on the mass spectrometer. T.G. wrote the manuscript with W.M. and J.L.R.. M.M.M.K., G.L., R.A.S., D.W.R.W., J.L.R., W.M. and T.G. designed the experiments and analysed the data.

Corresponding authors

Correspondence to Tobias Großkopf or Julie LaRoche.

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The authors declare no competing financial interests.

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This file contains Supplementary Materials, Methods and Data, Supplementary Tables 1-5, Supplementary Figures 1-8 and additional refernces. (PDF 767 kb)

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Großkopf, T., Mohr, W., Baustian, T. et al. Doubling of marine dinitrogen-fixation rates based on direct measurements. Nature 488, 361–364 (2012). https://doi.org/10.1038/nature11338

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