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Doubling of marine dinitrogen-fixation rates based on direct measurements

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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References

  1. Karl, D. et al. Dinitrogen fixation in the world's oceans. Biogeochemistry 57, 47–98 (2002)

    Article  Google Scholar 

  2. Falkowski, P. G., Barber, R. T. & Smetacek, V. Biogeochemical controls and feedbacks on ocean primary production. Science 281, 200–206 (1998)

    Article  CAS  Google Scholar 

  3. 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)

    Article  ADS  CAS  Google Scholar 

  4. Altabet, M. A. Constraints on oceanic N balance/imbalance from sedimentary 15N records. Biogeosciences 4, 75–86 (2007)

    Article  ADS  CAS  Google Scholar 

  5. Mahaffey, C., Michaels, A. F. & Capone, D. G. The conundrum of marine N2 fixation. Am. J. Sci. 305, 546–595 (2005)

    Article  ADS  CAS  Google Scholar 

  6. Codispoti, L. A. An oceanic fixed nitrogen sink exceeding 400 Tg N a−1 vs the concept of homeostasis in the fixed-nitrogen inventory. Biogeosciences 4, 233–253 (2007)

    Article  ADS  CAS  Google Scholar 

  7. Montoya, J. P., Voss, M., Kahler, P. & Capone, D. G. A simple, high-precision, high-sensitivity tracer assay for N2 fixation. Appl. Environ. Microbiol. 62, 986–993 (1996)

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Mohr, W., Grosskopf, T., Wallace, D. W. R. & LaRoche, J. Methodological underestimation of oceanic nitrogen fixation rates. PLoS ONE 5, e12583 (2010)

    Article  ADS  Google Scholar 

  9. Behrenfeld, M. J. & Falkowski, P. G. Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol. Oceanogr. 42, 1–20 (1997)

    Article  ADS  CAS  Google Scholar 

  10. 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)

    Article  ADS  CAS  Google Scholar 

  11. Mills, M. M., Ridame, C., Davey, M., La Roche, J. & Geider, R. J. Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429, 292–294 (2004)

    Article  ADS  CAS  Google Scholar 

  12. Moore, J. K., Doney, S. C., Lindsay, K., Mahowald, N. & Michaels, A. F. Nitrogen fixation amplifies the ocean biogeochemical response to decadal timescale variations in mineral dust deposition. Tellus B 58, 560–572 (2006)

    Article  ADS  Google Scholar 

  13. Naqvi, S. W. A. et al. Increased marine production of N2O due to intensifying anoxia on the Indian continental shelf. Nature 408, 346–349 (2000)

    Article  ADS  CAS  Google Scholar 

  14. Duce, R. A. et al. Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science 320, 893–897 (2008)

    Article  ADS  CAS  Google Scholar 

  15. Gruber, N. & Galloway, J. N. An Earth-system perspective of the global nitrogen cycle. Nature 451, 293–296 (2008)

    Article  ADS  CAS  Google Scholar 

  16. Gruber, N. & Sarmiento, J. L. Global patterns of marine nitrogen fixation and denitrification. Glob. Biogeochem. Cycles 11, 235–266 (1997)

    Article  ADS  CAS  Google Scholar 

  17. Zehr, J. P. et al. Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 412, 635–638 (2001)

    Article  ADS  CAS  Google Scholar 

  18. Zehr, J. P. et al. Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II. Science 322, 1110–1112 (2008)

    Article  ADS  CAS  Google Scholar 

  19. Moisander, P. H. et al. Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain. Science 327, 1512–1514 (2010)

    Article  ADS  CAS  Google Scholar 

  20. Langlois, R. J., LaRoche, J. & Raab, P. A. Diazotrophic diversity and distribution in the tropical and subtropical Atlantic Ocean. Appl. Environ. Microbiol. 71, 7910–7919 (2005)

    Article  CAS  Google Scholar 

  21. Langlois, R. J., Hummer, D. & LaRoche, J. Abundances and distributions of the dominant nifH phylotypes in the Northern Atlantic Ocean. Appl. Environ. Microbiol. 74, 1922–1931 (2008)

    Article  CAS  Google Scholar 

  22. Hamersley, M. R. et al. Nitrogen fixation within the water column associated with two hypoxic basins in the Southern California Bight. Aquat. Microb. Ecol. 63, 193–205 (2011)

    Article  Google Scholar 

  23. Fernandez, C., Farias, L. & Ulloa, O. Nitrogen fixation in denitrified marine waters. PLoS ONE 6, e20539 (2011)

    Article  ADS  CAS  Google Scholar 

  24. Farnelid, H. et al. Nitrogenase gene amplicons from global marine surface waters are dominated by genes of non-cyanobacteria. PLoS ONE 6, e19223 (2011)

    Article  ADS  CAS  Google Scholar 

  25. Halm, H. et al. Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre. ISME J. 6, 1238–1249 (2012)

    Article  CAS  Google Scholar 

  26. Luo, Y. W. et al. Database of diazotrophs in global ocean: abundances, biomass and nitrogen fixation rates. Earth Syst. Sci. Data Discuss. 5, 47–106 (2012)

    Article  ADS  Google Scholar 

  27. Moore, C. M. et al. Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability. Nature Geosci. 2, 867–871 (2009)

    Article  ADS  CAS  Google Scholar 

  28. Subramaniam, A. et al. Amazon River enhances diazotrophy and carbon sequestration in the tropical North Atlantic Ocean. Proc. Natl Acad. Sci. USA 105, 10460–10465 (2008)

    Article  ADS  CAS  Google Scholar 

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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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Authors

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.

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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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