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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Karl, D. et al. Dinitrogen fixation in the world's oceans. Biogeochemistry 57, 47–98 (2002)
Falkowski, P. G., Barber, R. T. & Smetacek, V. Biogeochemical controls and feedbacks on ocean primary production. Science 281, 200–206 (1998)
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)
Altabet, M. A. Constraints on oceanic N balance/imbalance from sedimentary 15N records. Biogeosciences 4, 75–86 (2007)
Mahaffey, C., Michaels, A. F. & Capone, D. G. The conundrum of marine N2 fixation. Am. J. Sci. 305, 546–595 (2005)
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)
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)
Mohr, W., Grosskopf, T., Wallace, D. W. R. & LaRoche, J. Methodological underestimation of oceanic nitrogen fixation rates. PLoS ONE 5, e12583 (2010)
Behrenfeld, M. J. & Falkowski, P. G. Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol. Oceanogr. 42, 1–20 (1997)
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)
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)
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)
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)
Duce, R. A. et al. Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science 320, 893–897 (2008)
Gruber, N. & Galloway, J. N. An Earth-system perspective of the global nitrogen cycle. Nature 451, 293–296 (2008)
Gruber, N. & Sarmiento, J. L. Global patterns of marine nitrogen fixation and denitrification. Glob. Biogeochem. Cycles 11, 235–266 (1997)
Zehr, J. P. et al. Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 412, 635–638 (2001)
Zehr, J. P. et al. Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II. Science 322, 1110–1112 (2008)
Moisander, P. H. et al. Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain. Science 327, 1512–1514 (2010)
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)
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)
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)
Fernandez, C., Farias, L. & Ulloa, O. Nitrogen fixation in denitrified marine waters. PLoS ONE 6, e20539 (2011)
Farnelid, H. et al. Nitrogenase gene amplicons from global marine surface waters are dominated by genes of non-cyanobacteria. PLoS ONE 6, e19223 (2011)
Halm, H. et al. Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre. ISME J. 6, 1238–1249 (2012)
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)
Moore, C. M. et al. Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability. Nature Geosci. 2, 867–871 (2009)
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)
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.
The authors declare no competing financial interests.
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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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