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.

Convergent estimates of marine nitrogen fixation

Nature volume 566, pages 205–211 (2019)Cite this article

Subjects

Abstract

Uncertainty in the global patterns of marine nitrogen fixation limits our understanding of the response of the ocean’s nitrogen and carbon cycles to environmental change. The geographical distribution of and ecological controls on nitrogen fixation are difficult to constrain with limited in situ measurements. Here we present convergent estimates of nitrogen fixation from an inverse biogeochemical and a prognostic ocean model. Our results demonstrate strong spatial variability in the nitrogen-to-phosphorus ratio of exported organic matter that greatly increases the global nitrogen-fixation rate (because phytoplankton manage with less phosphorus when it is in short supply). We find that the input of newly fixed nitrogen from microbial fixation and external inputs (atmospheric deposition and river fluxes) accounts for up to 50 per cent of carbon export in subtropical gyres. We also find that nitrogen fixation and denitrification are spatially decoupled but that nevertheless nitrogen sources and sinks appear to be balanced over the past few decades. Moreover, we propose a role for top-down zooplankton grazing control in shaping the global patterns of nitrogen fixation. Our findings suggest that biological carbon export in the ocean is higher than expected and that stabilizing nitrogen-cycle feedbacks are weaker than previously thought.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

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

Fig. 1: Schematic representation of the P-cycle and N-cycle models.
Fig. 2: N:P ratio of exported organic material.
Fig. 3: Maps of the column-integrated sources and sinks of fixed nitrogen.
Fig. 4: Contribution of newly fixed N to export production of carbon.
Fig. 5: Prognostic model simulations of diazotrophs and N2 fixation.

Data availability

All other data used to constrain the inverse model are publicly available (see Supplementary Information). The particulate organic matter data used for the comparison between the N:P of suspended particulate organic matter with the inferred N:P of exported organic matter shown in Fig. 2 is from a previous publication59. The model output for generating all of the other figures is available upon request.

References

  1. Mohr, W. et al. Methodological underestimation of oceanic nitrogen fixation rates. PLoS ONE 5, e12583 (2010).

    Article  ADS  Google Scholar 

  2. Großkopf, T. et al. Doubling of marine dinitrogen-fixation rates based on direct measurements. Nature 488, 361–364 (2012).

    Article  ADS  Google Scholar 

  3. Dabundo, R. et al. The contamination of commercial 15N2 gas stocks with 15N-labeled nitrate and ammonium and consequences for nitrogen fixation measurements. PLoS ONE 9, e110335 (2014).

    Article  ADS  Google Scholar 

  4. Luo, Y. W. et al. Data-based assessment of environmental controls on global marine nitrogen fixation. Biogeosciences 11, 691–708 (2014).

    Article  ADS  Google Scholar 

  5. 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 

  6. Deutsch, C. et al. Denitrification and N2 fixation in the Pacific Ocean. Glob. Biogeochem. Cycles 15, 483–506 (2001).

    Article  ADS  CAS  Google Scholar 

  7. Deutsch, C. et al. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445, 163–167 (2007).

    Article  ADS  CAS  Google Scholar 

  8. Knapp, A. N. et al. Low rates of nitrogen fixation in eastern tropical South Pacific surface waters. Proc. Natl Acad. Sci. USA 113, 4398–4403 (2016).

    Article  ADS  CAS  Google Scholar 

  9. Bonnet, S. et al. Hot spot of N2 fixation in the western tropical South Pacific pleads for a spatial decoupling between N2 fixation and denitrification. Proc. Natl Acad. Sci. USA 114, E2800–E2801 (2017).

    Article  CAS  Google Scholar 

  10. Somes, C. J. & Oschlies, A. On the influence of “non-Redfield” dissolved organic nutrient dynamics on the spatial distribution of N2 fixation and the size of the marine fixed nitrogen inventory. Glob. Biogeochem. Cycles 29, 973–993 (2015).

    Article  ADS  CAS  Google Scholar 

  11. Letscher, R. T. & Moore, J. K. Preferential remineralization of dissolved organic phosphorus and non-Redfield DOM dynamics in the global ocean: impacts on marine productivity, nitrogen fixation, and carbon export. Glob. Biogeochem. Cycles 29, 325–340 (2015).

    Article  ADS  CAS  Google Scholar 

  12. Mills, M. M. & Arrigo, K. R. Magnitude of oceanic nitrogen fixation influenced by the nutrient uptake ratio of phytoplankton. Nat. Geosci. 3, 412–416 (2010).

    Article  ADS  CAS  Google Scholar 

  13. Weber, T. & Deutsch, C. Oceanic nitrogen reservoir regulated by plankton diversity and ocean circulation. Nature 489, 419–422 (2012).

    Article  ADS  CAS  Google Scholar 

  14. Landolfi, A. et al. A new perspective on environmental controls of marine nitrogen fixation. Geophys. Res. Lett. 42, 4482–4489 (2015).

    Article  ADS  CAS  Google Scholar 

  15. Weber, T. S. & Deutsch, C. Ocean nutrient ratios governed by plankton biogeography. Nature 467, 550–554 (2010).

    Article  ADS  CAS  Google Scholar 

  16. Teng, Y. C. et al. Global-scale variations of the ratios of carbon to phosphorus in exported marine organic matter. Nat. Geosci. 7, 895–898 (2014).

    Article  ADS  CAS  Google Scholar 

  17. Letscher, R. T. et al. Variable C:N:P stoichiometry of dissolved organic matter cycling in the Community Earth System Model. Biogeosciences 12, 209–221 (2015).

    Article  ADS  CAS  Google Scholar 

  18. Martiny, A. C. et al. Regional variation in the particulate organic carbon to nitrogen ratio in the surface ocean. Glob. Biogeochem. Cycles 27, 723–731 (2013).

    Article  CAS  Google Scholar 

  19. Martiny, A. C. et al. Strong latitudinal patterns in the elemental ratios of marine plankton and organic matter. Nat. Geosci. 6, 279–283 (2013).

    Article  ADS  CAS  Google Scholar 

  20. DeVries, T. & Primeau, F. W. Dynamically and observationally constrained estimates of water-mass distributions and ages in the global ocean. J. Phys. Oceanogr. 41, 2381–2401 (2011).

    Article  ADS  Google Scholar 

  21. Primeau, F. W., Holzer, M. & DeVries, T. Southern Ocean nutrient trapping and the efficiency of the biological pump. J. Geophys. Res. Oceans 118, 2547–2564 (2013).

    Article  ADS  CAS  Google Scholar 

  22. Garcia, H. E. et al. in World Ocean Atlas 2013 Vol. 4 Dissolved Inorganic Nutrients (Phosphate, Nitrate, Silicate) (eds Levitus, S. & Mishonov, A.) http://www.nodc.noaa.gov/OC5/indprod.html (NOAA Atlas NESDIS 76, US Government Printing Office, Washington DC, 2013).

  23. Galbraith, E. D. & Martiny, A. C. A simple nutrient-dependence mechanism for predicting the stoichiometry of marine ecosystems. Proc. Natl Acad. Sci. USA 112, 8199–8204 (2015).

    Article  ADS  CAS  Google Scholar 

  24. Loh, A. N. & Bauer, J. E. Distribution, partitioning and fluxes of dissolved and particulate organic C, N and P in the eastern North Pacific and Southern Oceans. Deep Sea Res. I 47, 2287–2316 (2000).

    Article  CAS  Google Scholar 

  25. Primeau, F. W. & Holzer, M. The ocean’s memory of the atmosphere: residence-time and ventilation-rate distributions of water masses. J. Phys. Oceanogr. 36, 1439–1456 (2006).

    Article  ADS  Google Scholar 

  26. DeVries, T., Primeau, F. & Deutsch, C. The sequestration efficiency of the biological pump. Geophys. Res. Lett. 39, L13601 (2012).

    Article  ADS  Google Scholar 

  27. Marconi, D. et al. Tropical dominance of N2 fixation in the north Atlantic Ocean. Glob. Biogeochem. Cycles 31, 1608–1623 (2017).

    Article  ADS  CAS  Google Scholar 

  28. Tyrrell, T. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400, 525–531 (1999).

    Article  ADS  CAS  Google Scholar 

  29. Blais, M. et al. Nitrogen fixation and identification of potential diazotrophs in the Canadian Arctic. Glob. Biogeochem. Cycles 26, GB3022 (2012).

    Article  ADS  Google Scholar 

  30. Bianchi, D. et al. Global niche of marine anaerobic metabolisms expanded by particle microenvironments. Nat. Geosci. 11, 263–268 (2018).

    Article  ADS  CAS  Google Scholar 

  31. Eugster, O. & Gruber, N. A probabilistic estimate of global marine N-fixation and denitrification. Glob. Biogeochem. Cycles 26, GB4013 (2012).

    Article  ADS  Google Scholar 

  32. Moore, J. K. & Doney, S. C. Iron availability limits the ocean nitrogen inventory stabilizing feedbacks between marine denitrification and nitrogen fixation. Glob. Biogeochem. Cycles 21, GB2001 (2007).

    Article  ADS  Google Scholar 

  33. Wu, J. F. et al. Phosphate depletion in the western North Atlantic. Ocean Sci. 289, 759–762 (2000).

    CAS  Google Scholar 

  34. Sañudo-Wilhelmy, S. A. et al. Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature 411, 66–69 (2001).

    Article  Google Scholar 

  35. Mills, M. M. et al. Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429, 292–294 (2004).

    Article  Google Scholar 

  36. Altabet, M. Variations in nitrogen isotopic composition between sinking and suspended particles: implications for nitrogen cycling and particle transformation in the open ocean. Deep Sea Res. I 35, 535–554 (1988).

    Article  ADS  CAS  Google Scholar 

  37. Karl, D. et al. The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388, 533–538 (1997).

    Article  ADS  CAS  Google Scholar 

  38. Brandes, J. A. & Devol, A. H. A global marine-fixed nitrogen isotopic budget: implications for Holocene nitrogen cycling. Glob. Biogeochem. Cycles 16, 67-1–67-14 (2002).

    Article  Google Scholar 

  39. DeVries, T. et al. Marine denitrification rates determined from a global 3-D inverse model. Biogeosciences 10, 2481–2496 (2013).

    Article  ADS  CAS  Google Scholar 

  40. Lamarque, J.-F. et al. Historical (1850–2000) gridded anthropogenic and biomass burning emissions of reactive gases and aerosols: methodology and application. Atmos. Chem. Phys. 10, 7017–7039 (2010).

    Article  ADS  CAS  Google Scholar 

  41. Yang, S. & Gruber, N. The anthropogenic perturbation of the marine nitrogen cycle by atmospheric deposition: nitrogen cycle feedbacks and the 15N Haber–Bosch effect. Glob. Biogeochem. Cycles 30, 1418–1440 (2016).

    Article  ADS  CAS  Google Scholar 

  42. Somes, C. J. et al. Limited impact of atmospheric nitrogen deposition on marine productivity due to biogeochemical feedbacks in a global ocean model. Geophys. Res. Lett. 43, 4500–4509 (2016).

    Article  ADS  CAS  Google Scholar 

  43. Somes, C. J., Schmittner, A. & Altabet, M. A. Nitrogen isotope simulations show the importance of atmospheric iron deposition for nitrogen fixation across the Pacific Ocean. Geophys. Res. Lett. 37, L23605 (2010).

    Article  ADS  Google Scholar 

  44. Ward, B. A. et al. Iron, phosphorus, and nitrogen supply ratios define the biogeography of nitrogen fixation. Limnol. Oceanogr. 58, 2059–2075 (2013).

    Article  ADS  CAS  Google Scholar 

  45. Edwards, K. F. et al. Light and growth in marine phytoplankton: allometric, taxonomic, and environmental variation. Limnol. Oceanogr. 60, 540–552 (2015).

    Article  ADS  Google Scholar 

  46. Fu, F.-X. et al. Differing responses of marine N2 fixers to warming and consequences for future diazotroph community structure. Aquat. Microb. Ecol. 72, 33–46 (2014).

    Article  Google Scholar 

  47. Landolfi, A. et al. Overlooked runaway feedback in the marine nitrogen cycle: the vicious cycle. Biogeosciences 10, 1351–1363 (2013).

    Article  ADS  CAS  Google Scholar 

  48. O’Neil, J. M. & Roman, M. R. Ingestion of the cyanobacterium Trichodesmium spp. by pelagic harpacticoid copepods Macrosetella, Miracia and Oculosetella. Hydrobiologia 292/293, 235–240 (1994).

    Article  Google Scholar 

  49. Hunt, B. P. et al. Contribution and pathways of diazotroph-derived nitrogen to zooplankton during the VAHINE mesocosm experiment in the oligotrophic New Caledonia lagoon. Biogeosciences 13, 3131–3145 (2016).

    Article  ADS  Google Scholar 

  50. Getzlaff, J. & Dietze, H. Effects of increased isopycnal diffusivity mimicking the unresolved equatorial intermediate current system in an Earth system climate model. Geophys. Res. Lett. 40, 2166–2170 (2013).

    Article  ADS  Google Scholar 

  51. Seitzinger, S. et al. Global river nutrient export: a scenario analysis of past and future trends. Glob. Biogeochem. Cycles 24, GB0A08 (2010).

    Google Scholar 

  52. Westberry, T. et al. Carbon-based primary productivity modeling with vertically resolved photoacclimation. Glob. Biogeochem. Cycles 22, GB2024 (2008).

    Article  ADS  Google Scholar 

  53. Ocean Productivity http://www.science.oregonstate.edu/ocean.productivity/index.php (2008).

  54. Bohlen, L., Dale, A. W. & Wallmann, K. Simple transfer functions for calculating benthic fixed nitrogen losses and C:N:P regeneration ratios in global biogeochemical models. Glob. Biogeochem. Cycles 26, GB3029 (2012).

    Article  ADS  Google Scholar 

  55. Moore, J. K., Doney, S. C. & Lindsay, K. Upper ocean ecosystem dynamics and iron cycling in a global three-dimensional model. Glob. Biogeochem. Cycles 18, GB4028 (2004).

    Article  ADS  Google Scholar 

  56. Moore, C. M. et al. Processes and patterns of oceanic nutrient limitation. Nat. Geosci. 6, 701–710 (2013).

    Article  ADS  CAS  Google Scholar 

  57. Moore, J. K. et al. Marine ecosystem dynamics and biogeochemical cycling in the Community Earth System Model [CESM1 (BGC)]: comparison of the 1990s with the 2090s under the RCP4. 5 and RCP8. 5 scenarios. J. Clim. 26, 9291–9312 (2013).

    Article  ADS  Google Scholar 

  58. Moore, J. K. et al. Sustained climate warming drives declining marine biological productivity. Science 359, 1139–1143 (2018).

    Article  ADS  CAS  Google Scholar 

  59. Martiny, A. C. et al. Concentrations and ratios of particulate organic carbon, nitrogen, and phosphorus in the global ocean. Sci. Data 1, 140048 (2014).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Science Foundation (grant OCE 1436922 awarded to F.W.P.). F.W.P., J.K.M. and W.-L.W. also acknowledge support from the US Department of Energy Office of Biological and Environmental Research (grants DE-SC0007206, DE-SC0012550 and DE-SC0016539) and the RUBISCO-SFA (grant PC13115 to J.K.M.) and A.C.M. acknowledges financial support from the National Science Foundation (grants OCE-1046297 and OCE-1559002). We also acknowledge support from the National Science Foundation (grant OCE-1848576).

Reviewer information

Nature thanks K. Casciotti, N. Gruber and C. Somes for their contribution to the peer review of this work.

Author information

Authors and Affiliations

  1. Department of Earth System Science, University of California Irvine, Irvine, CA, USA

    Wei-Lei Wang, J. Keith Moore, Adam C. Martiny & François W. Primeau

  2. Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA, USA

    Adam C. Martiny

Authors
  1. Wei-Lei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Keith Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adam C. Martiny
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. François W. Primeau
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the design of the study. W.-L.W. and F.W.P. built the inverse model and analysed its results. J.K.M. performed the CESM simulations and analysed its output. F.W.P., W.-L.W. and J.K.M. wrote the manuscript. All authors participated in the discussion of the results and commented on the manuscript.

Corresponding author

Correspondence to François W. Primeau.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

This file contains the Supplementary Materials, Supplementary Figures S1-S21 and Supplementary Tables S1-S8.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, WL., Moore, J.K., Martiny, A.C. et al. Convergent estimates of marine nitrogen fixation. Nature 566, 205–211 (2019). https://doi.org/10.1038/s41586-019-0911-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41586-019-0911-2

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