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Assimilation of upwelled nitrate by small eukaryotes in the Sargasso Sea

Nature Geoscience volume 4, pages 717–722 (2011)Cite this article

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Abstract

Phytoplankton growth is potentially limited by the scarcity of biologically available forms of nitrogen such as nitrate and ammonium. In the subtropical ocean gyres, water column stratification impedes the upward flux of nitrate to surface waters. Phytoplankton in these waters are assumed to rely largely on ammonium and other forms of nitrogen recycled during the breakdown of organic matter. Here, we use flow cytometry to separate prokaryotic and eukaryotic phytoplankton collected from Sargasso Sea surface waters in the summers of 2008 and 2009, and to analyse their respective nitrogen isotope ratios. We show that prokaryotes have a uniformly low ratio of 15N to 14N, δ15N, consistent with their reliance on recycled nitrogen. In contrast, small eukaryotic phytoplankton, less than 30 μm in size, have a higher and more variable δ15N, with a mean value similar to that of nitrate in underlying Subtropical Mode Water. For the summertime Sargasso Sea, we estimate that small eukaryotes obtain more than half of their nitrogen from upwelled nitrate. In addition, our data support the view that sinking material derives largely from eukaryotic, not prokaryotic, phytoplankton biomass.

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Figure 1: Important forms of nitrogen in the Sargasso Sea.
Figure 2: Abundances and nitrogen isotope ratios of populations sorted by flow cytometry.
Figure 3: Changes to our view of Sargasso Sea nitrogen cycling.

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References

  1. Dugdale, R. C. & Goering, J. J. Uptake of new and regenerated forms of nitrogen in primary production. Limnol. Oceanogr. 12, 196–206 (1967).

    Article  Google Scholar 

  2. Eppley, R. W. & Peterson, B. J. Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282, 677–680 (1979).

    Article  Google Scholar 

  3. Menzel, D. W. & Ryther, J. H. The annual cycle of primary production in the Sargasso Sea off Bermuda. Deep-Sea Res. 6, 351–367 (1960).

    Google Scholar 

  4. Lipschultz, F. A time-series assessment of the nitrogen cycle at BATS. Deep-Sea Res. II 48, 1897–1924 (2001).

    Article  Google Scholar 

  5. Steinberg, D. K. et al. Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): A decade-scale look at ocean biology and biogeochemistry. Deep-Sea Res. II 48, 1405–1447 (2001).

    Article  Google Scholar 

  6. Chisholm, S. W. et al. novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334, 340–343 (1988).

    Article  Google Scholar 

  7. Waterbury, J. B., Watson, S., Guillard, R. R. L. & Brand, L. E. Widespread occurrence of a unicellular, marine, planktonic, cyanobacterium. Nature 277, 293–294 (1979).

    Article  Google Scholar 

  8. DuRand, M. D., Olson, R. J. & Chisholm, S. W. Phytoplankton population dynamics at the Bermuda Atlantic Time-series station in the Sargasso Sea. Deep-Sea Res. II 48, 1983–2003 (2001).

    Article  Google Scholar 

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

    Article  Google Scholar 

  10. Altabet, M. A. A time-series study of the vertical structure of nitrogen and particle dynamics in the Sargasso Sea. Limnol. Oceanogr. 34, 1185–1201 (1989).

    Article  Google Scholar 

  11. Knapp, A. N., Sigman, D. M. & Lipschultz, F. N isotopic composition of dissolved organic nitrogen and nitrate at the Bermuda Atlantic Time-series Study site. Glob. Biogeochem. Cycles 19, 1–15 (2005).

    Article  Google Scholar 

  12. Saino, T. & Hattori, A. Geographical variation of the water column distribution of suspended particulate organic nitrogen and its 15N natural abundance in the Pacific and its marginal seas. Deep-Sea Res. I 34, 807–827 (1987).

    Article  Google Scholar 

  13. Carpenter, E. J., Harvey, H. R., Fry, B. & Capone, D. G. Biogeochemical tracers of the marine cyanobacterium Trichodesmium. Deep-Sea Res. I 44, 27–38 (1997).

    Article  Google Scholar 

  14. Minagawa, M. & Wada, E. Nitrogen isotope ratios of red tide organisms in the East China Sea—a characterization of biological nitrogen-fixation. Mar. Chem. 19, 245–259 (1986).

    Article  Google Scholar 

  15. Checkley, D. M. Jr & Miller, C. A. Nitrogen isotope fractionation by oceanic zooplankton. Deep-Sea Res. 36, 1449–1456 (1989).

    Article  Google Scholar 

  16. Montoya, J. P., Carpenter, E. J. & Capone, D. G. Nitrogen fixation and nitrogen isotope abundances in zooplankton of the oligotrophic North Atlantic. Limnol. Oceanogr. 47, 1617–1628 (2002).

    Article  Google Scholar 

  17. Rau, G. H., Teyssie, J. L., Rassoulzadegan, F. & Fowler, S. W. 13C/12C and 15N/14N variations among size-fractionated marine particles—implications for their origin and trophic relationships. Mar. Ecol.-Prog. Ser. 59, 33–38 (1990).

    Article  Google Scholar 

  18. Moore, L. R., Post, A. F., Rocap, G. & Chisholm, S. W. Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnol. Oceanogr. 47, 989–996 (2002).

    Article  Google Scholar 

  19. Hansell, D. A. & Carlson, C. A. Biogeochemistry of total organic carbon and nitrogen in the Sargasso Sea: Control by convective overturn. Deep-Sea Res. II 48, 1649–1667 (2001).

    Article  Google Scholar 

  20. Macko, S. A., Estep, M. L. F., Engel, M. H. & Hare, P. E. Kinetic fractionation of stable nitrogen isotopes during amino-acid transamination. Geochim. Cosmochim. Acta 50, 2143–2146 (1986).

    Article  Google Scholar 

  21. Silfer, J. A., Engel, M. H. & Macko, S. A. Kinetic fractionation of stable carbon and nitrogen isotopes during peptide-bond hydrolysis—experimental evidence and geochemical implications. Chem. Geol. 101, 211–221 (1992).

    Google Scholar 

  22. Knapp, A. N., Sigman, D. M., Lipschultz, F., Kustka, A. & Capone, D. G. Interbasin isotopic correspondence between upper-ocean bulk DON and subsurface nitrate and its implications for marine nitrogen cycling. Glob. Biogeochem. Cycles. (in the press).

  23. Zubkov, M. V., Fuchs, B. M., Tarran, G. A., Burkill, P. H. & Amann, R. High rate of uptake of organic nitrogen compounds by Prochlorococcus cyanobacteria as a key to their dominance in oligotrophic oceanic waters. Appl. Environ. Microbiol. 69, 1299–1304 (2003).

    Article  Google Scholar 

  24. Wawrik, B., Callaghan, A. V. & Bronk, D. A. Use of inorganic and organic nitrogen by Synechococcus spp. and diatoms on the West Florida shelf as measured using stable isotope probing. Appl. Environ. Microbiol. 75, 6662–6670 (2009).

    Article  Google Scholar 

  25. Lomas, M. W. & Lipschultz, F. Forming the primary nitrite maximum: Nitrifiers or phytoplankton. Limnol. Oceanogr. 51, 2453–2467 (2006).

    Article  Google Scholar 

  26. Hoch, M. P., Fogel, M. L. & Kirchman, D. L. Isotope fractionation associated with ammonium uptake by a marine bacterium. Limnol. Oceanogr. 37, 1447–1459 (1992).

    Article  Google Scholar 

  27. DiFiore, P. J., Sigman, D. M. & Dunbar, R. B. Upper ocean nitrogen fluxes in the Polar Antarctic Zone: Constraints from the nitrogen and oxygen isotopes of nitrate. Geochem. Geophys. Geosyst. 10, Q11016 (2009).

    Article  Google Scholar 

  28. Harrison, W. G., Harris, L. R. & Irwin, B. D. The kinetics of nitrogen utilization in the oceanic mixed layer: Nitrate and ammonium interactions at nanomolar concentrations. Limnol. Oceanogr. 41, 16–32 (1996).

    Article  Google Scholar 

  29. Granger, J., Sigman, D. M., Lehmann, M. F. & Tortell, P. D. Nitrogen and oxygen isotope fractionation during dissimilatory nitrate reduction by denitrifying bacteria. Limnol. Oceanogr. 53, 2533–2545 (2008).

    Article  Google Scholar 

  30. Villareal, T. A. et al. Upward transport of oceanic nitrate by migrating diatom mats. Nature 397, 423–425 (1999).

    Article  Google Scholar 

  31. Goericke, R. Response of phytoplankton community structure and taxon-specific growth rates to seasonally varying physical forcing in the Sargasso Sea off Bermuda. Limnol. Oceanogr. 43, 921–935 (1998).

    Article  Google Scholar 

  32. Cochlan, W. P. & Harrison, P. J. Inhibition of nitrate uptake by ammonium and urea in the eucaryotic picoflagellate Micromonas pusilla (Butcher) Manton et Parke. J. Exp. Mar. Biol. Ecol. 153, 143–152 (1991).

    Article  Google Scholar 

  33. McGillicuddy, D. J. Jr et al. Influence of mesoscale eddies on new production in the Sargasso Sea. Nature 394, 263–266 (1998).

    Article  Google Scholar 

  34. Johnson, K. S., Riser, S. C. & Karl, D. M. Nitrate supply from the deep to near-surface waters of the North Pacific subtropical gyre. Nature 465, 1062–1065 (2010).

    Article  Google Scholar 

  35. Katija, K. & Dabiri, J. O. A viscosity-enhanced mechanism for biogenic ocean mixing. Nature 460, 624–626 (2009).

    Article  Google Scholar 

  36. Jenkins, W. J. Studying subtropical thermocline ventilation and circulation using tritium and 3He. J. Geophys. Res. 103, 15817–15831 (1998).

    Article  Google Scholar 

  37. Fenchel, T., King, G. M. & Blackburn, T. H. Bacterial Biogeochemistry: The Ecophysiology of Mineral Cycling (Elsevier Academic Press, 1998).

    Google Scholar 

  38. Ducklow, H. W., Purdie, D. A., Williams, P. J. L. & Davies, J. M. Bacterioplankton—a sink for carbon in a coastal marine plankton community. Science 232, 865–867 (1986).

    Article  Google Scholar 

  39. Altabet, M. A. & Small, L. F. Nitrogen isotopic ratios in fecal pellets produced by marine zooplankton. Geochim. Cosmochim. Acta 54, 155–163 (1990).

    Article  Google Scholar 

  40. Montoya, J. P., Wiebe, P. H. & McCarthy, J. J. Natural abundance of 15N in particulate nitrogen and zooplankton in the Gulf Stream region and warm-core ring 86a. Deep-Sea Res. I 39, S363–S392 (1992).

    Article  Google Scholar 

  41. Tamelander, T., Soreide, J. E., Hop, H. & Carroll, M. L. Fractionation of stable isotopes in the Arctic marine copepod Calanus glacialis: Effects on the isotopic composition of marine particulate organic matter. J. Exp. Mar. Biol. Ecol. 333, 231–240 (2006).

    Article  Google Scholar 

  42. Harbison, G. R. & McAlister, V. L. Filter-feeding rates and particle retention efficiencies of 3 species of Cyclosalpa (Tunicata, Thaliacea). Limnol. Oceanogr. 24, 875–892 (1979).

    Article  Google Scholar 

  43. Schnetzer, A. & Steinberg, D. K. Natural diets of vertically migrating zooplankton in the Sargasso Sea. Mar. Biol. 141, 403 (2002).

    Article  Google Scholar 

  44. Lomas, M. W. & Moran, S. B. Evidence for aggregation and export of cyanobacteria and nano-eukaryotes from the Sargasso Sea euphotic zone. Biogeosciences 8, 203–216 (2011).

    Article  Google Scholar 

  45. Michaels, A. F. & Silver, M. W. Primary production, sinking fluxes and the microbial food web. Deep-Sea Res. 35, 473–490 (1988).

    Article  Google Scholar 

  46. Richardson, T. L. & Jackson, G. A. Small phytoplankton and carbon export from the surface ocean. Science 315, 838–840 (2007).

    Article  Google Scholar 

  47. Casey, J. R. et al. Phytoplankton taxon-specific orthophosphate (Pi) and ATP utilization in the western subtropical North Atlantic. Aquat. Microbial. Ecol. 58, 31–44 (2009).

    Article  Google Scholar 

  48. Braman, R. S. & Hendrix, S. A. Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium(III) reduction with chemiluminescence detection. Anal. Chem. 61, 2715–2718 (1989).

    Article  Google Scholar 

  49. Sigman, D. M. et al. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal. Chem. 73, 4145–4153 (2001).

    Article  Google Scholar 

  50. Casciotti, K. L., Sigman, D. M., Hastings, M. G., Böhlke, J. K. & Hilkert, A. Measurement of the oxygen isotopic composition of nitrate in seawater and freshwater using the denitrifier method. Anal. Chem. 74, 4905–4912 (2002).

    Article  Google Scholar 

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Acknowledgements

We thank A. Babbin, S. Bell, J. Granger, A. Knapp, H. Ren and L. Treibergs, the staff of the Bermuda Institute of Ocean Sciences and the captain and crew of the R/V Atlantic Explorer. We also thank B. Plessen at GeoForschungsZentrum, Potsdam, for analysis of bulk PN samples from July 2008. N. Levine pointed us towards the possible impacts of Hurricane Bertha. This work was supported by the Charrock Foundation, by the Siebel Energy Grand Challenge of Princeton University, and by the US NSF through grants OCE-0752161 (M.W.L.), OCE-0452162 (B.B.W.) and OCE-0447570 (D.M.S.). This is BIOS contribution no. 2028.

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Authors and Affiliations

  1. Department of Geosciences, Princeton University, Guyot Hall, Princeton, New Jersey 08544, USA

    Sarah E. Fawcett, Bess B. Ward & Daniel M. Sigman

  2. Bermuda Institute of Ocean Sciences, St George’s GE01, Bermuda

    Michael W. Lomas

  3. School of Ocean and Earth Science and Technology, University of Hawaii, Honolulu, Hawaii 96822, USA

    John R. Casey

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  1. Sarah E. Fawcett
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M.W.L. and D.M.S. suggested the research area, S.E.F., M.W.L., B.B.W. and D.M.S. planned the project, S.E.F. and J.R.C. performed most of the work, and all authors wrote the paper, led by S.E.F.

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Correspondence to Sarah E. Fawcett.

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Fawcett, S., Lomas, M., Casey, J. et al. Assimilation of upwelled nitrate by small eukaryotes in the Sargasso Sea. Nature Geosci 4, 717–722 (2011). https://doi.org/10.1038/ngeo1265

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