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.
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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.
Mohr, W. et al. Methodological underestimation of oceanic nitrogen fixation rates. PLoS ONE 5, e12583 (2010).
Großkopf, T. et al. Doubling of marine dinitrogen-fixation rates based on direct measurements. Nature 488, 361–364 (2012).
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).
Luo, Y. W. et al. Data-based assessment of environmental controls on global marine nitrogen fixation. Biogeosciences 11, 691–708 (2014).
Gruber, N. & Sarmiento, J. L. Global patterns of marine nitrogen fixation and denitrification. Glob. Biogeochem. Cycles 11, 235–266 (1997).
Deutsch, C. et al. Denitrification and N2 fixation in the Pacific Ocean. Glob. Biogeochem. Cycles 15, 483–506 (2001).
Deutsch, C. et al. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445, 163–167 (2007).
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).
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).
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).
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).
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).
Weber, T. & Deutsch, C. Oceanic nitrogen reservoir regulated by plankton diversity and ocean circulation. Nature 489, 419–422 (2012).
Landolfi, A. et al. A new perspective on environmental controls of marine nitrogen fixation. Geophys. Res. Lett. 42, 4482–4489 (2015).
Weber, T. S. & Deutsch, C. Ocean nutrient ratios governed by plankton biogeography. Nature 467, 550–554 (2010).
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).
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).
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).
Martiny, A. C. et al. Strong latitudinal patterns in the elemental ratios of marine plankton and organic matter. Nat. Geosci. 6, 279–283 (2013).
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).
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).
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).
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).
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).
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).
DeVries, T., Primeau, F. & Deutsch, C. The sequestration efficiency of the biological pump. Geophys. Res. Lett. 39, L13601 (2012).
Marconi, D. et al. Tropical dominance of N2 fixation in the north Atlantic Ocean. Glob. Biogeochem. Cycles 31, 1608–1623 (2017).
Tyrrell, T. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400, 525–531 (1999).
Blais, M. et al. Nitrogen fixation and identification of potential diazotrophs in the Canadian Arctic. Glob. Biogeochem. Cycles 26, GB3022 (2012).
Bianchi, D. et al. Global niche of marine anaerobic metabolisms expanded by particle microenvironments. Nat. Geosci. 11, 263–268 (2018).
Eugster, O. & Gruber, N. A probabilistic estimate of global marine N-fixation and denitrification. Glob. Biogeochem. Cycles 26, GB4013 (2012).
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).
Wu, J. F. et al. Phosphate depletion in the western North Atlantic. Ocean Sci. 289, 759–762 (2000).
Sañudo-Wilhelmy, S. A. et al. Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature 411, 66–69 (2001).
Mills, M. M. et al. Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429, 292–294 (2004).
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).
Karl, D. et al. The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388, 533–538 (1997).
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).
DeVries, T. et al. Marine denitrification rates determined from a global 3-D inverse model. Biogeosciences 10, 2481–2496 (2013).
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).
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).
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).
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).
Ward, B. A. et al. Iron, phosphorus, and nitrogen supply ratios define the biogeography of nitrogen fixation. Limnol. Oceanogr. 58, 2059–2075 (2013).
Edwards, K. F. et al. Light and growth in marine phytoplankton: allometric, taxonomic, and environmental variation. Limnol. Oceanogr. 60, 540–552 (2015).
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).
Landolfi, A. et al. Overlooked runaway feedback in the marine nitrogen cycle: the vicious cycle. Biogeosciences 10, 1351–1363 (2013).
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).
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).
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).
Seitzinger, S. et al. Global river nutrient export: a scenario analysis of past and future trends. Glob. Biogeochem. Cycles 24, GB0A08 (2010).
Westberry, T. et al. Carbon-based primary productivity modeling with vertically resolved photoacclimation. Glob. Biogeochem. Cycles 22, GB2024 (2008).
Ocean Productivity http://www.science.oregonstate.edu/ocean.productivity/index.php (2008).
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).
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).
Moore, C. M. et al. Processes and patterns of oceanic nutrient limitation. Nat. Geosci. 6, 701–710 (2013).
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).
Moore, J. K. et al. Sustained climate warming drives declining marine biological productivity. Science 359, 1139–1143 (2018).
Martiny, A. C. et al. Concentrations and ratios of particulate organic carbon, nitrogen, and phosphorus in the global ocean. Sci. Data 1, 140048 (2014).
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).
Nature thanks K. Casciotti, N. Gruber and C. Somes for their contribution to the peer review of this work.
The authors declare no competing interests.
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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
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