Skip to main content
Log in

Dinitrogen fixation in the world's oceans

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

The surface water of themarine environment has traditionally beenviewed as a nitrogen (N) limited habitat, andthis has guided the development of conceptualbiogeochemical models focusing largely on thereservoir of nitrate as the critical source ofN to sustain primary productivity. However,selected groups of Bacteria, includingcyanobacteria, and Archaea canutilize dinitrogen (N2) as an alternativeN source. In the marine environment, thesemicroorganisms can have profound effects on netcommunity production processes and can impactthe coupling of C-N-P cycles as well as the netoceanic sequestration of atmospheric carbondioxide. As one component of an integrated ‘Nitrogen Transport and Transformations’ project, we have begun to re-assess ourunderstanding of (1) the biotic sources andrates of N2 fixation in the world'soceans, (2) the major controls on rates ofoceanic N2 fixation, (3) the significanceof this N2 fixation for the global carboncycle and (4) the role of human activities inthe alteration of oceanic N2 fixation. Preliminary results indicate that rates ofN2 fixation, especially in subtropical andtropical open ocean habitats, have a major rolein the global marine N budget. Iron (Fe)bioavailability appears to be an importantcontrol and is, therefore, critical inextrapolation to global rates of N2fixation. Anthropogenic perturbations mayalter N2 fixation in coastal environmentsthrough habitat destruction and eutrophication,and open ocean N2 fixation may be enhancedby warming and increased stratification of theupper water column. Global anthropogenic andclimatic changes may also affect N2fixation rates, for example by altering dustinputs (i.e. Fe) or by expansion ofsubtropical boundaries. Some recent estimatesof global ocean N2 fixation are in therange of 100–200 Tg N (1–2 × 1014 g N)yr−1, but have large uncertainties. Theseestimates are nearly an order of magnitudegreater than historical, pre-1980 estimates,but approach modern estimates of oceanicdenitrification.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alldredge AL & Silver MW (1982) Abundance and production rates of floating diatom mats (Rhizosolenia castracanei and R. imbricata var. shrubsolei) in the Eastern Pacific Ocean. Mar. Biol. 66: 83–88

    Google Scholar 

  • Altabet MA (1988) 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

    Google Scholar 

  • Beget JE (1996) Tephrochronology and paleoclimatology of the last interglacial-glacial cycle recorded in Alaskan loess deposits. Quat. Int. 34-36: 121–126

    Google Scholar 

  • Benson DR (1985) Consumption of atmospheric nitrogen. In: Leadbetter ER & Poindexter JS (Eds) Bacteria in Nature, Volume 1: Bacterial Activities in Perspective (pp 155–198). Plenum Press, New York

    Google Scholar 

  • Bergman B & Carpenter EJ (1991) Nitrogenase confined to randomly distributed trichomes in the marine cyanobacterium Trichodesmium thiebautii. J. Phycol. 27: 158–165

    Google Scholar 

  • Bergman B, Siddiqui PJA, Carpenter EJ & Peschek GA (1993) Cytochrome oxidase: subcellular distrivution and relationship to nitrogenase expression in the nonheterocystous cyanobacterium Trichodemium thiebautii. Appl. Environ. Microbiol. 59: 3239–3244

    Google Scholar 

  • Bergman B, Gallon JR, Rai AN & Stal LJ (1997) N2 fixation by non-heterocystous cyanobacteria. FEMS Microbiol. Rev. 19: 139–185

    Google Scholar 

  • Bishop PE, Jarlenski DML & Hetherington DR (1980) Evidence for an alternative nitrogen fixation system in Azotobacter vinelandii. Proc. Natl. Acad. Sci. USA 77: 7342–7346

    Google Scholar 

  • Bishop PE & Premakumar R (1992) Alternative nitrogen fixation systems. In: Stacey G, Burris RH & Evans HJ (Eds) Biological Nitrogen Fixation (pp 736–762). Chapman and Hall, New York

    Google Scholar 

  • Borstad GA, Gower JFR & Carpenter EJ (1992) Development of algorithms for remote sensing of Trichodesmium blooms. In: Carpenter EJ, Capone DG & Rueter JG (Eds) Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs (pp 193–210). Kluwer Academic Publishers, The Netherlands

    Google Scholar 

  • Brandes JA, Devol AH, Yoshinari T, Jayakumar DA & Naqvi SWA (1998) Isotopic composition of nitrate in the central Arabian Sea and eastern tropical North Pacific: A tracer for mixing and nitrogen cycles. Limnol. Oceanogr. 43: 1680–1689

    Google Scholar 

  • Broughton WJ & Pühler A (Eds) (1986) Nitrogen Fixation, Volume 4: Molecular Biology. Clarendon Press, Oxford

    Google Scholar 

  • Bryceson I & Fay P (1981) Nitrogen fixation in Oscillatoria (Trichodesmium) erythraea in relation to bundle formation and trichome differentiation. Mar. Biol. 61: 159–166

    Google Scholar 

  • Burns RC & Hardy RWF (1975) Nitrogen fixation in bacteria and higher plants. Springer-Verlag, New York

    Google Scholar 

  • Burris RH (1991) Nitrogenases. J. Biol. Chem. 266: 9339–9342

    Google Scholar 

  • Capone DG (1988) Benthic nitrogen fixation. In: Blackburn H & Sorensen J (Eds) Nitrogen Cycling in Coastal Marine Environments (pp 85–123). John Wiley, New York

    Google Scholar 

  • Capone DG & Carpenter EJ (1982) Nitrogen fixation in the marine environment. Science 217: 1140–1142

    Google Scholar 

  • Capone DG & Carpenter EJ (1999) Nitrogen fixation by marine cyanobacteria: Historical and global perspectives. Bull. Inst. Oceanogr. Monaco 19: 235–256

    Google Scholar 

  • Capone DG, Ferrier MD & Carpenter EJ (1994) Cycling and release of glutamate and glutamine in colonies of the marine planktonic cyanobacterium, Trichodesmium thiebautii. Appl. Environ. Microbiol. 60: 3989–3995

    Google Scholar 

  • Capone DG, O'Neil JM, Zehr J & Carpenter EJ (1990) Basis for diel variation in nitrogenase activity in the marine planktonic cyanobacterium Trichodesmium thiebautii. Appl. Environ. Microbiol. 56: 3532–3536

    Google Scholar 

  • Capone DG, Zehr JP, Paerl HW, Bergman B & Carpenter EJ (1997) Trichodesmium a globally significant marine cyanobacterium. Science 276: 1221–1229

    Google Scholar 

  • Carpenter EJ (1972) Nitrogen fixation by a blue-green epiphyte on pelagic Sargassum. Science 178: 1207–1209

    Google Scholar 

  • Carpenter EJ (1983) Nitrogen fixation by marine Oscillatoria (Trichodesmium) in the world's oceans. In: Carpenter EJ & Capone DG (Eds) Nitrogen in the Marine Environment (pp 65–103). Academic Press, New York

    Google Scholar 

  • Carpenter EJ, Bergman B, Dawson R, Siddiqui PJA, Soderback E & Capone DG (1992) Glutamine synthetase and nitrogen cycling in colonies of the marine diazotrophic cyanobacterium, Trichodesmium spp. Appl. Environ. Microbiol. 58: 3122–3129

    Google Scholar 

  • Carpenter EJ & Capone DG (1992) Nitrogen fixation in Trichodesmium blooms. In: Carpenter EJ, Capone DG & Rueter J (Eds) Marine Pelagic Cyanobacteria: Trichodesmium and Other Diazotrophs (pp 211–217). Kluwer Academic Publishers, The Netherlands

    Google Scholar 

  • Carpenter EJ, Chang J, Cottrell M, Schubauer J, Paerl HW, Bebout BM & Capone DG (1990) Re-evaluation of nitrogenase oxygen-protective mechanisms in the planktonic marine cyanobacterium Trichodesmium. Mar. Ecol. Prog. Ser. 65: 151–158

    Google Scholar 

  • Carpenter EJ & Culliney JL (1975) Nitrogen fixation in marine shipworms. Science 187: 551–552

    Google Scholar 

  • Carpenter EJ, Harvey HR, Fry B & Capone DG (1997) Biogeochemical tracers of the marine cyanobacterium Trichodesmium. Deep-Sea Res. 44: 27–38

    Google Scholar 

  • Carpenter EJ, O'Neil JM, Dawson R, Capone DG, Siddiqui PJA, Roenneberg T & Bergman B (1993) The tropical diazotrophic phytoplankter Trichodesmium: biological characteristics of two common species. Mar. Ecol. Prog. Ser. 95: 295–304

    Google Scholar 

  • Carpenter EJ & Price CC, IV (1976) Marine Oscillatoria (Trichodesmium): Explanation for aerobic nitrogen fixation without heterocysts. Science 191: 1278–1280

    Google Scholar 

  • Carpenter EJ & Roenneberg T (1995) The marine planktonic cyanobacteria Trichodesmium spp.: photosynthetic rate measurements in the SW Atlantic Ocean. Mar. Ecol. Prog. Ser. 118: 267–273

    Google Scholar 

  • Carpenter EJ & Romans, K (1991) Major role of the cyanobacterium Trichodesmium in nutrient cycling in the North Atlantic Ocean. Science 254: 1356–1358

    Google Scholar 

  • Checkley DM Jr & Miller CA (1989) Nitrogen isotope fractionation by oceanic zooplankton. Deep-Sea Res. 36: 1449–1456

    Google Scholar 

  • Codispoti L (1989) Phosphorus versus nitrogen limitation of new and export production. In: Berger WH, Smetacek VS & Wefer G (Eds) Productivity in the Ocean: Present and Past (pp 377–394). John Wiley & Sons, New York

    Google Scholar 

  • Cole JJ, Lane JM, Marino R & Howarth RW (1993) Molybdenum assimilation by cyanobacteria and phytoplankton in freshwater and salt water. Limnol. Oceanogr. 38: 25–35

    Google Scholar 

  • Cragin JH, Herron MM, Langway Jr. CC & Klouda G (1997) Interhemispheric comparison of changes in the composition of atmospheric precipitation during the late Cenozoic era. In: Dunbar MJ (Ed) Polar Oceans, Proceedings of the Polar Oceans Conference (pp 617–641). Arctic Institute of North America, Calgary, Alberta

    Google Scholar 

  • Cullen JJ, Franks PJS, Karl DM & Longhurst A (2001) Physical influences on marine ecosystem dynamics. In: Robinson AR, McCarthy JJ & Rothschild BJ (Eds) The Sea, vol. 12, in press

  • Davey A & Marchant HJ (1983) Seasonal variation in nitrogen fixation by Nostoc commune Vaucher at the Vestfold Hills, Antarctica. Phycologia 22: 337–385

    Google Scholar 

  • Dean DR, Bolin JT & Zheng L (1993) Nitrogenase metalloclusters: Structures, organization, and synthesis. J. Bact. 175: 6737–6744

    Google Scholar 

  • Delwiche CC (1970) The nitrogen cycle. Sci. Amer. 223: 137–146

    Google Scholar 

  • Delwiche C & Likens G (1977) Global chemical cycles and their alteration by man. Dahlem Konferenzen, Berlin

    Google Scholar 

  • Deutsch CA, Gruber NP, Key RM, Sarmiento JL & Ganachaud A (2001) Denitrification and N2 fixation in the Pacific Ocean. Global Biogeochem. Cycles 15: 483–506

    Google Scholar 

  • Dickey TD (1991) The emergence of concurrent high-resolution physical and bio-optical measurements in the upper ocean and their applications. Rev. Geophys. 29: 383–413

    Google Scholar 

  • Dore JE, Popp BN, Karl DM & Sansone FJ (1998) A large source of atmospheric nitrous oxide from subtropical North Pacific surface waters. Nature 396: 63–66

    Google Scholar 

  • Duarte CM (1992) Nutrient concentration of aquatic plants: Patterns across species. Limnol. Oceanogr. 37: 882–889

    Google Scholar 

  • Dugdale RC & Goering JJ (1967) Uptake of new and regenerated forms of nitrogen in primary Productivity. Limnol. Oceanogr. 12: 196–206

    Google Scholar 

  • Dugdale RC, Menzel DW & Ryther JH (1961) Nitrogen fixation in the Sargasso Sea. Deep-Sea Res. 7: 298–300

    Google Scholar 

  • Dupouy C (1992) Discoloured waters in the Melanesian archipelago (New Caledonia and Vanuatu). The value of the NIMBUS-7 Coastal Zone Colour Scanner observations. In: Carpenter EJ, Capone DG & Rueter JG (Eds) Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs (pp 177–191) Kluwer Academic Publishers, The Netherlands

    Google Scholar 

  • Dupouy C, Neveux J, Subramaniam A, Mulholland MR, Montoya JP, Campbell L, Carpenter EJ & Capone DG (2000) Satellite captures Trichodesmium blooms in the southwestern tropical Pacific. Eos 81: 13, 15, 16

    Google Scholar 

  • Dupouy C, Petit M & Dandonneau Y (1988) Satellite detected cyanobacteria bloom in the southwestern tropical Pacific. Int. J. Remote Sens. 9: 389–396

    Google Scholar 

  • Falkowski PG (1997) Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387: 272–275

    Google Scholar 

  • Fallik E, Chan Y-K & Robson RL (1991) Detection of alternative nitrogenases in aerobic gram-negative nitrogen-fixing bacteria. J Bact. 173: 365–371

    Google Scholar 

  • Fanning KA (1989) Influence of atmospheric pollution on nutrient limitation in the ocean. Nature 339: 460–463

    Google Scholar 

  • Fanning KA (1992) Nutrient provinces in the sea: Concentration ratios, reaction rate ratios, and ideal covariation. J. Geophys. Res. 97: 5693–5712

    Google Scholar 

  • Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol. Rev. 546: 340–373

    Google Scholar 

  • Fogg GE (1974) Nitrogen fixation. In: Stewart WDP (Ed) Algal Physiology and Biochemistry (pp 560–582). Blackwell, Oxford

    Google Scholar 

  • Fogg GE (1982) Nitrogen cycling in sea waters. Phil. Trans. R. Soc. London 296: 299–576

    Google Scholar 

  • Fredriksson C & Bergman B (1997) Ultrastructural characterization of cells specialized for nitrogen fixation in a non-heterocystous cyanobcterium, Trichodesmium. Protoplasma 197: 76–85

    Google Scholar 

  • Gallon JR (1981) The oxygen sensitivity of nitrogenase: a problem for biochemists and microorganisms. Trends Biochem. Sci. 6: 19–23

    Google Scholar 

  • Gallon JR (1992) Reconciling the incompatible: N2 fixation and O2. Tansley review No.144. New Phytol. 122: 571–609

    Google Scholar 

  • Gallon JR & Stal LJ (1992) N2 fixation in non-heterocystous cyanobacteria: An overview. In: Carpenter EJ, Capone DG & Rueter JG (Eds) Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs (pp 115–139). Kluwer Academic Publishers, The Netherlands

    Google Scholar 

  • Galloway JN, Schlesinger WH, Levy II H, Michaels A & Schnoor JL (1995) Nitrogen fixation: Anthropogenic enhancement-environmental response. Global Biogeochem. Cycles 9: 235–252

    Google Scholar 

  • Gledhill M & Berg CMGVd (1994) Determination of complexation of iron(III) with natural organic complexing ligands in sewater using cathodic stripping voltammetry. Mar. Chem. 47: 41

    Google Scholar 

  • Glibert PM & Bronk DA (1994) Release of dissolved organic nitrogen by marine diazotrophic cyanobacteria, Trichodesmium spp. Appl. Environ. Microbiol. 60: 3996–4000

    Google Scholar 

  • Gordon N, Angel DL, Neori A, Kress N & Kimor B (1994) Heterotrophic dinoflagellates with symbiotic cyanobacteria and nitrogen limitation in the Gulf of Aqaba. Mar. Ecol. Prog. Ser. 107: 83–88

    Google Scholar 

  • Gruber N & Sarmiento JL (1997) Global patterns of marine nitrogen fixation and denitrification. Global Biogeochem. Cycles 11: 235–266

    Google Scholar 

  • Guerinot ML & Colwell RR (1985) Enumeration, isolation, and characterization of N2-fixing bacteria from seawater. Appl Environ. Microbiol. 50: 350–355

    Google Scholar 

  • Guerinot ML & Patriquin DG (1981) The association of N2-fixing bacteria with sea urchins. Mar. Biol. 62: 197–207

    Google Scholar 

  • Guerinot ML, West PA, Lee JV & Colwell RR (1982) Vibrio diazotrophicus sp. nov., a marine nitrogen-fixing bacterium. Int. J. Syst. Bact. 32: 350–357

    Google Scholar 

  • Hanson RB (1977) Pelagic Sargassum community metabolism: Carbon and nitrogen. J. Exp. Mar. Biol. Ecol. 29: 107–118

    Google Scholar 

  • Haxo FT, Lewin RA, Lee KW & Li M-R (1987) Fine structure and pigments of Oscillatoria (Trichodesmium) aff. Thiebautii (Cyanophyta) in culture. Phycologia 26: 443–456

    Google Scholar 

  • Hecky RE, Campbell P & Hendzel LL (1993) The stoichiometry of carbon, nitrogen, and phosphorus in particulate matter of lakes and oceans. Limnol. Oceanogr. 38: 709–724

    Google Scholar 

  • Hood RR, Michaels AF & Capone DG (2000) Answers sought to the enigma of marine nitrogen fixation. Eos, Trans. Amer. Geophys. Un. 81: 133, 138, 139

    Google Scholar 

  • Howard JB & Rees DC (1996) Structural basis of biological nitrogen fixation. Chem. Rev. 96: 2965–2982

    Google Scholar 

  • Howarth RW, Chan F & Marino R (1999) Do top-down and bottom-up controls interact to exclude nitrogen-fixing cyanobacteria from the plankton of estuaries: explorations with a simulation model. Biogeochem. 46: 203–231

    Google Scholar 

  • Howarth RW & Cole JJ (1985) Molybdenum availability, nitrogen limitation and phytoplankton growth in natural waters. Science 229: 653–655

    Google Scholar 

  • Howarth RW, Marino R, Lane J & Cole JJ (1988) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 2. Biogeochemical controls. Limnol. Oceanogr. 33: 688–701

    Google Scholar 

  • Husar RB, Prospero JM & Stowe LL (1997) Characterization of tropospheric aerosols over the oceans with the NOAA advanced very high resolution radiometer optical thickness operational product. J. Geophys. Res. 102: 16889–16909

    Google Scholar 

  • Janson S, Bergman B, Carpenter EJ, Giovannoni SJ & Vergin K (1999a) Genetic analysis of natural populations of the marine diazotrophic cyanobacterium Trichodesmium. FEMS Microbiol. Ecol. 30: 57–65

    Google Scholar 

  • Janson S, Carpenter EJ & Bergman B (1994) Compartmentalization of nitrogenase in a nonheterocystous cyanobacterium Trichodesmium contortum. FEMS Microbiol. Lett. 118: 9–14

    Google Scholar 

  • Janson S, Siddiqui PJA, Walsby AE, Romans K, Carpenter EJ & Bergman B (1995) Cytomorphological characterization of the planktonic diazotrophic cyanobacteria Trichodesmium spp. from the Indian Ocean and Caribbean and Sargasso Seas. J. Phycol. 31: 463–477

    Google Scholar 

  • Janson S, Wouters J, Bergman B & Carpenter EJ (1999b) Host specificity in the Richeliadiatom symbiosis by hetR gene sequence analysis. Environ. Microbiol. 1: 431–438

    Google Scholar 

  • Johnson KJ, Gordon RM & Coale KH (1997) What controls dissolved iron concentrations in the world ocean? Mar. Chem. 57: 181

    Google Scholar 

  • Joussaume S (1993) Paleoclimatic tracers: An investigation using an atmospheric general circulation model under ice age conditions - 1. Desert dust. J. Geophys. Res. 98: 2767–2805

    Google Scholar 

  • Kana TM (1993) Rapid oxygen cycling in Trichodesmium thiebautii. Limnol. Oceanogr. 38: 18–24

    Google Scholar 

  • Karl DM (1999) A sea of change: Biogeochemical variability in the North Pacific subtropical gyre. Ecosystems 2: 181–214

    Google Scholar 

  • Karl DM (2000) A new source of 'new' nitrogen in the sea. Trends in Microbiol. 8: 301 (Comment section)

    Google Scholar 

  • Karl DM, Björkman KM, Dore JE, Fujieki L, Hebel DV, Houlihan T, Letelier RM & Tupas LM (2001) Ecological nitrogen-to-phosphorus stoichiometry at Station ALOHA. Deep-Sea Res. II48: 1529–1566

    Google Scholar 

  • Karl DM, Letelier R, Hebel DV, Bird DF & Winn CD (1992) Trichodesmium blooms and new nitrogen in the north Pacific gyre. In: Carpenter EJ, Capone DG & Rueter JG (Eds) Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs (pp 219–237). Kluwer Academic Publishers, The Netherlands

    Google Scholar 

  • Karl D, Letelier R, Tupas L, Dore J, Christian J & Hebel D (1997) The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature388: 533–538

    Google Scholar 

  • Karl DM & Tien G (1997) Temporal variability in dissolved phosphorus concentrations in the subtropical North Pacific Ocean. Mar. Chem. 56: 77–96

    Google Scholar 

  • Keene WC & Savoie DL (1998) The pH of deliquesced sea-salt aerosol in polluted marine air. Geophys. Res. Lett. 25: 2181–2184

    Google Scholar 

  • Kim J & Rees DC (1994) Nitrogenase and biological nitrogen fixation. Biochem. 33: 389–397

    Google Scholar 

  • Kirshtein JD, Zehr JP & Paerl HW(1993) Determination of N2 fixation potential in the marine environment: application of the polymerase chain reaction. Mar. Ecol. Prog. Ser. 95: 305–309

    Google Scholar 

  • Kuchler DA & Jupp DLB (1988) Shuttle photograph captures massive phytoplankton bloom in the Great Barrier Reef. Int. J. Remote Sensing 9: 1299–1301

    Google Scholar 

  • Letelier RM & Karl DM (1996) Role of Trichodesmium spp. in the productivity of the subtropical North Pacific Ocean. Mar. Ecol. Prog. Ser. 133: 263–273

    Google Scholar 

  • Letelier RM & Karl DM (1998) Trichodesmium spp. physiology and nutrient fluxes in the North Pacific subtropical gyre. Aquat. Microb. Ecol. 15: 265–276

    Google Scholar 

  • LeTraon PY (1990) A method for optimal analysis of fields with spatially variable mean. J. Geophys. Res. 95: 13543–13547

    Google Scholar 

  • Li WKW, Glover HE & Morris I (1980) Physiology of carbon assimilation by Oscillatoria thiebautii in the Caribbean Sea. Limnol. Oceanogr. 25: 447–456

    Google Scholar 

  • Lin S, Henze S, Lundgren P, Bergman B & Carpenter EJ (1999) Whole-cell immunolocalization of nitrogenase in marine diazotrophic cyanobacteria, Trichodesmium spp. Appl. Environ. Microbiol. 64: 3052–3064

    Google Scholar 

  • Lipschultz F & Owens NJ (1996) An assessment of nitrogen fixation as a source of nitrogen to the North Atlantic Ocean. Biogeochem. 35: 261–274

    Google Scholar 

  • Liu K-K, SuM-J, Hsueh C-R & Gong G-C (1996) The nitrogen isotopic composition of nitrate in the Kuroshio Water northwest of Taiwan: Evidence for nitrogen fixation as a source of isotopically light nitrate. Mar. Chem. 54: 273–292

    Google Scholar 

  • Liu T, An Z, Yuan B & Han J (1985) The loess-paleosol sequence in China and climatic history. Episodes8: 21–28

    Google Scholar 

  • Longhurst A (1998) Ecological Geography of the Sea. Academic Press, San Diego, California

    Google Scholar 

  • Longhurst AR & Harrison WG (1989) The biological pump: profiles of plankton production and consumption in the upper ocean. Prog. Oceanog. 22: 7–123

    Google Scholar 

  • Lundgren P, Soederbaeck E, Carpenter EJ & Bergman B (2000) Nitrogen fixation and nitrogenase in Katagnymene spp., a non-heterocystous marine cyanobacterium. Submitted to J. Phycol

  • Mague TH, Weare NM & Holm-Hansen O (1974) Nitrogen fixation in the North Pacific Ocean. Mar. Biol. 24: 109–119

  • Mahowald N, Kohfeld KE, Hansson M, Balkanski Y, Harrison SP, Prentice IC, Schulz M & Rodhe H (1999) Dust sources and deposition during the last glacial maximum and current climate: A comparison of model results with palaeodata from ice cores and marine sediments. J. Geophys. Res. in press

  • Martinez L, Silver MW, King JM & Alldredge AL (1983) Nitrogen fixation by floating diatom mats: A source of new nitrogen to oligotrophic ocean waters. Science221: 152–154

    Google Scholar 

  • McElroy MB (1976) Chemical processes in the solar system: a kinetic perspective. In: Herschbach D (Ed) MTP International Review of Science (pp 127–211). Buttersworth, London

    Google Scholar 

  • McElroy MB (1983) Marine biological controls on atmospheric CO2 climate. Nature302: 328–329

    Google Scholar 

  • Michaels AF, Bates NR, Buesseler KO, Carlson CA & Knap AH (1994) Carbon-cycle imbalances in the Sargasso Sea. Nature 372: 37–540

    Google Scholar 

  • Michaels AF, Karl DM & Capone D (2001) Redfield stoichiometry, new production and nitrogen fixation. Oceanography (Special JGOFS edition), in press

  • Michaels AF, Olson D, Sarmiento JL, Ammerman JW, Fanning K, Jahnke R, Knap AH, Lipschultz F & Prospero JM (1996) Inputs, losses and transformations of nitrogen and phosphorus in the pelagic North Atlantic Ocean. Biogeochem. 35: 181–226

    Google Scholar 

  • Mitsui A, Kumazawa S, Takahashi A, Ikemoto H, Cao S & Arai T (1986) Strategy by which nitrogen-fixing unicellular cyanobacteria grow photoautotrophically. Nature 323: 720–722

    Google Scholar 

  • Montoya JP, Voss M, Kaehler P & Capone DG (1996) A simple, high precision tracer assay for dinitrogen fixation. Appl. Environ. Microbiol. 62: 986–993

    Google Scholar 

  • Moore B, Whitley E & Webster TA (1921) Studies of photo-synthesis in marine algae - 1. Fixation of carbon and nitrogen from inorganic sources in sea water. 2. Increase of alkalinity of sea water as a measure of photo-synthesis. Proc. Roy. Soc. Lond. B 92: 51–58

    Google Scholar 

  • Mulholland MR, Ohki K & Capone DG (1999) Nitrogen utilization and metabolism relative to patterns of N2 fixation in cultures of Trichodesmium NIBB1067. J. Phycol. 35: 977–988

    Google Scholar 

  • Niemi A (1979) Blue-green algal blooms and N:P ratios in the Baltic Sea. Acta Bot. Fenn. 110: 57–61

    Google Scholar 

  • Ohki K & Fujita Y (1982) Laboratory culture of the pelagic blue-green alga Trichodesmium thiebautii: Conditions for unialgal culture. Mar. Ecol. Prog. Ser. 7: 185–190

    Google Scholar 

  • Ohki K & Fujita Y (1988) Aerobic nitrogenase activity measured as acetylene reduction in the marine non-heterocystous cyanobacterium Trichodesmium spp. grown under artificial conditions. Mar. Biol. 98: 111–114

    Google Scholar 

  • Ohki K, Rueter JG & Fujita Y (1986) Cultures of the pelagic cyanophytes Trichodesmium erythraeum and T. thiebautii in synthetic medium. Mar. Biol. 91: 9–13

    Google Scholar 

  • Ohki K, Zehr JP, Falkowski PG & Fujita Y (1991) Regulation of nitrogen fixation by different nitrogen sources in the marine non-heterocystous cyanobacterium Trichodesmium sp. NIBB1067. Arch. Microbiol. 156: 335–337

    Google Scholar 

  • Owens NJP (1987) Natural variations in 15N in the marine environment. Adv. Mar. Biol. 24: 389–451

    Google Scholar 

  • Paerl HW (1994) Spatial segregation of CO2 fixation in Trichodesmium sp.: Linkage to N2 fixation potential. J. Phycol. 30: 790–799

    Google Scholar 

  • Paerl HW (2000) Physical-chemical constraints on cyanobacterial growth in the oceans. International Symposium on Marine Cyanobacteria and Related Organisms, Institut Oceanographique, Paris

    Google Scholar 

  • Paerl HW & Bebout BM (1988) Direct measurement of O2-depleted microzones in marine Oscillatoria: relation to N2 fixation. Science 241: 442–445

    Google Scholar 

  • Paerl HW, Bebout BM & Prufert LE (1989a) Bacterial associations with marine Oscillatoria sp. (Trichodesmium sp.) populations: Ecophysiological implications. J. Phycol. 25: 773–784

    Google Scholar 

  • Paerl HW & Bland PT (1982) Localized tetrazolium reduction in relation to N2 fixation, CO2 fixation, and H2 uptake in aquatic filamentous cyanobacteria. Appl. Environ. Microbiol. 43: 218–226

    Google Scholar 

  • Paerl HW, Crocker KM & Prufert LE (1987) Limitation of N2 fixation in coastal marine waters: relative importance of molybdenum, iron, phosphorus and organic matter availability. Limnol. Oceanogr. 32: 525–536

    Google Scholar 

  • Paerl HW & Pinckney JL (1996) A mini-review of microbial consortia: their roles in aquatic production and biogeochemical cycling. Microb. Ecol. 31: 225–247

    Google Scholar 

  • Paerl HW, Priscu JC & Brawner DL (1989b) Immunochemical localization of nitrogenase in marine Trichodesmium aggregates: Relationship to N2 fixation potential. Appl. Environ. Microbiol. 55: 2965–2975

    Google Scholar 

  • Paerl HW, Prufert-Bebout L & Guo C (1994) Iron-stimulated N2 fixation and growth in natural and cultured populations of the planktonic marine cyanobacterium Trichodesmium sp. Appl. Environ. Microbiol. 60: 1044–1047

    Google Scholar 

  • Paerl HW & Zehr JP (2000) Marine nitrogen fixation. In: Kirchman DL (Ed) Microbial Ecology of the Oceans (pp 387–426). Wiley-Liss

  • Paul EA (1978) Contribution of nitrogen fixation to ecosystem functioning and nitrogen fluxes on a global basis. Ecol. Bull. 26: 282–293

    Google Scholar 

  • Paulsen DM, Paerl HW & Bishop PE (1991) Evidence that molybdenum-dependent nitrogen fixation is not limited by high sulfate in marine environments. Limnol. Oceanogr. 36: 1325–1334

    Google Scholar 

  • Platt T, Harrison WG, Lewis MR, Li WKW, Sathyendranath S, Smith RE & Vezina AF (1989) Biological production of the oceans: the case for a consensus. Mar. Ecol. Prog. Ser. 52: 77–88

    Google Scholar 

  • Platt T & Sathyendranath S (1999) Spatial structure of pelagic ecosystem processes in the global ocean. Ecosystems2: 384–394

    Google Scholar 

  • Postgate JR (1982) The Fundamentals of Nitrogen Fixation. Cambridge University Press, Cambridge

    Google Scholar 

  • Prentice IC & Webb III T (1998) BIOME 6000: Reconstructing global mid-Holocene vegetation patterns from paleoecological records. J. Biogeogr. 25: 995–1005

    Google Scholar 

  • Proctor LM(1997) Nitrogen-fixing, photosynthetic, anaerobic bacteria associated with pelagic copepods. Aquat. Microbiol. Ecol. 12: 105–113

    Google Scholar 

  • Prospero JM, Barrett K, Church T, Dentener F, Duce RA, Galloway JN, Levy II H, Moody J & Quinn P (1996) Atmospheric deposition of nutrients to the North Atlantic basin. Biogeochemistry 35: 27–73

    Google Scholar 

  • Prospero JM & Nees RT (1986) Impact of the North African drought and El Niño on mineral dust in the Barbados trace winds. Nature 320: 735–738

    Google Scholar 

  • Prufert-Bebout L, Paerl HW & Lassen C (1993) Growth, nitrogen fixation, and spectral attenuation in cultivated Trichodesmium species. Appl. Environ. Microbiol. 59: 1367–1375

    Google Scholar 

  • Rasche ME & Seefeldt LC (1997)Reduction of thiocyanate, cyanate, and carbon disulfide by nitrogenase: Kinetic characterization and EPR spectroscopic analysis. Biochem. 36: 8574–8585

    Google Scholar 

  • Raven JA (1988) The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytol. 109: 279–287

    Google Scholar 

  • Rea DK (1994) The paleoclimatic record provided by eolian deposition in the deep sea: The geologic history of wind. Rev. Geophys. 32: 159–195

    Google Scholar 

  • Robson RL & Postgate JR (1980) Oxygen and hydrogen in biological nitrogen fixation. Ann. Rev. Microbiol. 34: 183–207

    Google Scholar 

  • Rue EL & Bruland KW (1995) Complexation of iron(III) by natural ligands in the central North Pacific as determined by a new competitive ligand equilibrium/absorptive cathodic stripping voltammetry method. Mar. Chem. 50: 117–138

    Google Scholar 

  • Rueter JG, Hutchins DA, Smith RW & Unsworth NL (1992) Iron nutrition of Trichodesmium. In: Carpenter EJ, Capone DG & Rueter JG (Eds) Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs (pp 289–306). Kluwer Academic Publishers, The Netherlands

    Google Scholar 

  • Saino T & Hattori A (1978) Diel variation in nitrogen fixation by a marine blue-green alga, Trichodesmium thiebautii. Deep-Sea Res. 25: 1259–1263

    Google Scholar 

  • Saino T & Hattori A (1979) Nitrogen fixation by Trichodesmium and its significance in nitrogen cycling in the Kuroshio area and adjacent waters. Proc. 4th CSK Symp. Tokyo

  • Saino T & Hattori A (1980) 15N natural abundance in oceanic suspended particulate matter. Nature 283: 752–754

    Google Scholar 

  • Saino T & Hattori A (1987) 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. 34: 807–827

    Google Scholar 

  • Scranton MI (1983) The role of the cyanobacterium Oscillatoria (Trichodesmium) thiebautii in the marine hydrogen cycle. Mar. Ecol. Prog. Ser. 11: 79–87

    Google Scholar 

  • Seefeldt LC, Rasche ME & Ensign SA (1995) Carbonyl sulfide and carbon dioxide as new substrates, and carbon disulfide as a new inhibitor, of nitrogenase. Biochem. 34: 5382–5389

    Google Scholar 

  • Siddiqui PJA, Bergman B & Carpenter EJ (1992) Filamentous cyanobacterial associates of the marine planktonic cyanobacterium Trichodesmium. Phycologia 31: 326–337

    Google Scholar 

  • Siefert RL, Johansen AM & Hoffman MR (1999) Chemical characterization of ambient aerosol collected during the southwest monsoon and intermonsoon seasons over the Arabian Sea: Labile-Fe(II) and other trace metals. J. Geophys. Res. 104: 3511–3526

    Google Scholar 

  • Siefert RL, Webb SM & Hoffmann MR (1996) Determination of photochemically available iron in ambient aerosol. J. Geophys. Res. 101: 14441–14449

    Google Scholar 

  • Siegenthaler U & Sarmiento J (1993) Atmospheric carbon dioxide and the oceans. Nature365: 119–125

    Google Scholar 

  • Sigman DM, Altabet MA, McCorkle DC, Francois R & Fischer G (1999) The δ 15N of nitrate in the Southern Ocean: Nitrate consumption in surface waters. Global Biogeochem. Cycles 13: 1149–1166

    Google Scholar 

  • Sigman DM, Altabet MA, McCorkle DC, Francois R & Fischer G (2000) The δ 15N of nitrate in the Southern Ocean: Nitrogen cycling and circulation in the ocean interior. J. Geophys. Res. in press

  • Sigman DM, Altabet MA, Michener RH, McCorkle DC, Fry B & Holmes RM (1997) Natural abundance-level measurement of the nitrogen isotopic composition of oceanic nitrate: An adaptation of the ammonia diffusion method. Mar. Chem. 57: 227–242

    Google Scholar 

  • Simpson FB & Burris RH (1984) A nitrogen pressure of 50 atmospheres does not preventevolution of hydrogen by nitrogenase. Science224: 1095–1097

    Google Scholar 

  • Smith BE & Eady RR (1992) Metalloclusters of the nitrogenases. Eur. J. Biochem. 205: 1–15

    Google Scholar 

  • Soderlund R & Rosswall T (1982) The nitrogen cycles. In: Hutzinger O (Ed) The Natural Environment and the Biogeochemical Cycles (pp 61–81). Springer-Verlag, New York

    Google Scholar 

  • Soderlund R & Svensson BH (1976) The global nitrogen cycle. In: Svensson B & Soderlund R (Eds) Nitrogen, Phosphorus and Sulphur-Global Cycles (pp 23–73). SCOPE Report No. 7, Ecological Bulletin No. 21, NFR., Stockholm

    Google Scholar 

  • Sprent JI & Sprent P (1990) Nitrogen Fixing Organisms: Pure and Applied Aspects. Chapman and Hall, New York

    Google Scholar 

  • Stal LJ (1995) Physiological ecology of cyanobacteria in microbial mats and other communities. Tansley Review No. 84. New Phytol. 131: 1–32

    Google Scholar 

  • Stal LJ & Krumbein WE (1985) Oxygen protection of nitrogenase in the aerobically nitrogen fixing, non-heterocystous cyanobacterium Oscillatoria sp. Arch. Microbiol. 143: 2–76

    Google Scholar 

  • Stal LJ, Staal M & Villbrandt M (1999) Nutrient control of cyanobacterial blooms in the Baltic Sea. Aquat. Microb. Ecol. 18: 165–173

    Google Scholar 

  • Stewart WDP, Fitzgerald GP & Burris RH (1967) In situ studies on N2 fixation using the acetylene reduction technique. Proc. Natl. Acad. Aci. USA 58: 2071–2078

    Google Scholar 

  • Subramaniam A & Carpenter EJ (1994) An empirically derived protocol for the detection of blooms of the marine cyanobacterium Trichodesmium using CZCS imagery. Int. J. Remote Sensing 15: 1559–1569

    Google Scholar 

  • Subramaniam A, Carpenter EJ & Falkowski PG (1999a) Optical properties of the marine diazotrophic cyanobacteria Trichodesmium spp. II. Reflectance model for remote sensing. Limnol. Oceanogr. 44: 618–627

    Google Scholar 

  • Subramaniam A, Carpenter EJ, Karentz PG & Falkowski D (1999b) Optical properties of the marine diazotrophic cyanobacteria Trichodesmium spp. I. Absorption and spectral photosynthetic characteristics. Limnol. Oceanogr. 44: 608–617

    Google Scholar 

  • Takahashi T, Feely RA, Weiss RF, Wanninkhof RH, Chipman DW, Sutherland SC & Takahashi TT (1997) Global air-sea flux of CO2: An estimate based on measurements of sea-air pCO2 difference. Proc. Natl. Acad. Sci. USA 94: 8292–8299

    Google Scholar 

  • Tans PP, Fung IY & Takahashi T (1990) Observational constraints on the global atmospheric CO2 budget. Science 247: 1431–1438

    Google Scholar 

  • Tassan S (1995) SeaWiFS potential for remote sensing of marine Trichodesmium at sub-bloom concentration. Int. J. Remote Sensing 16: 3619–3627

    Google Scholar 

  • Toggweiler JR (1999) An ultimate limiting nutrient. Nature 400: 511–512

    Google Scholar 

  • Trenberth KE & Hoar TJ (1997) El Niño and climate change. Geophys. Res. Lett. 24: 3057–3060

    Google Scholar 

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

    Google Scholar 

  • Urdaci MC, Stal LJ & Marchand M (1988) Occurrence of nitrogen fixation among Vibrio spp. Arch. Microbiol. 150: 224–229

    Google Scholar 

  • Venrick EL (1974) The distribution and significance of Richelia intracellularis Schmidt in the North Pacific Central Gyre. Limnol. Oceanogr. 19: 437–445

    Google Scholar 

  • Villareal TA (1991) Nitrogen-fixation by the cyanobacterial symbiont of the diatom genus Hemiaulus. Mar. Ecol. Prog. Ser. 76: 201–204

    Google Scholar 

  • Villareal TA, Altabet MA & Culver-Rymsza K (1993) Nitrogen transport by vertically migrating diatom mats in the North Pacific Ocean. Nature 363: 709–712

    Google Scholar 

  • Villareal TA, Pilskaln C, Brzezinski M, Lipschultz F, Dennett M & Gardner GB (1999) Upward transport of oceanic nitrate by migrating diatom mats. Nature 397: 423–425

    Google Scholar 

  • Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB & Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57/58: 1–45

    Google Scholar 

  • Wada E (1980) Nitrogen isotope fractionation and its significance in biogeochemical processes occurring in marine environments. In: Goldberg ED, Horibe Y & Saruhashi K (Eds) Isotope Marine Chemistry (pp 375–398). Uchida-Rokakuho, Tokyo

    Google Scholar 

  • Wada E & Hattori A (1991) Nitrogen in the Sea: Forms, Abundances, and Rate Processes. CRC Press, Boca Raton, FL.

    Google Scholar 

  • Waterbury JB, Watson SW & Valois FW (1988) Temporal separation of photosynthesis and dinitrogen fixation in the marine unicellular cyanobacterium: Erythrospira marina. Eos 69: 1089

    Google Scholar 

  • Wu J & Luther GW(1995) Complexation of Fe(III) by natural organic ligands in the northwest Atlantic Ocean by competitive ligand equilibration method and kinetic approach. Mar. Chem. 50: 159–177

    Google Scholar 

  • Zehr JP (1995) Nitrogen fixation in the marine environment: Why only Trichodesmium? In: Joint IR (Ed) Molecular Ecology of Aquatic Microbes (pp 335–364). Springer-Verlag, Berlin

    Google Scholar 

  • Zehr JP, Braun S, Chen YB & Mellon MT (1996) Nitrogen fixation in the marine environment: Relating genetic potential to nitrogenase activity. J. Exp. Mar. Biol. Ecol. 203: 61–73

    Google Scholar 

  • Zehr JP & Capone DG (1996) Problems and promise of assaying the genetic potential for nitrogen fixation in the marine environment. Microb. Ecol. 32: 263–281

    Google Scholar 

  • Zehr JP & McReynolds LA (1989) Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii. Appl. Environ. Microbiol. 55: 2522–2526

    Google Scholar 

  • Zehr JP, Mellon MT & Zani S (1998) New nitrogen-fixing microorganisms detected in oligotrophic oceans by amplification of nitrogenase (nifH) genes. Appl. Environ. Microbiol. 64: 3444–3450

    Google Scholar 

  • Zehr JP & Paerl H (1998) Nitrogen fixation in the marine environment: Genetic potential and nitrogenase expression. In: Cooksey KE (Ed) Molecular Approaches to the Study of the Ocean (pp 285–301). Chapman and Hall, London

    Google Scholar 

  • Zehr JP, Carpenter EJ & Villareal TA (2000) New perspectives on nitrogen-fixing microorganisms in tropical and subtropical oceans. Trends in Microbiol. 8: 68–73

    Google Scholar 

  • Zhu XR, Prospero JM & Millero FJ (1997) Diel variability of soluble Fe(II) and soluble total Fe in North African dust in the trade winds at Barbados. J. Geophys. Res. 102: 21297–21305

    Google Scholar 

  • Zhuang G, Yi Z, Duce RA & Brown PR (1992) Link between iron and sulfur suggested by the detection of Fe(II) in remote marine aerosols. Nature 355: 537–539

    Google Scholar 

  • Zuckermann H, Staal M, Stal LJ, Reuss J, Hekkert SL, Harren F & Parker D (1997) Online monitoring of nitrogenase activity in cyanobacteria by sensitive laser photoacoustic detection of ethylene. Appl. Environ. Microbiol. 63: 4243–4251

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karl, D., Michaels, A., Bergman, B. et al. Dinitrogen fixation in the world's oceans. Biogeochemistry 57, 47–98 (2002). https://doi.org/10.1023/A:1015798105851

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1015798105851

Navigation