Advertisement

Dinitrogen fixation in the world’s oceans

  • D. Karl
  • A. Michaels
  • B. Bergman
  • D. Capone
  • E. Carpenter
  • R. Letelier
  • F. Lipschultz
  • H. Paerl
  • D. Sigman
  • L. Stal
Chapter

Abstract

The surface water of the marine environment has traditionally been viewed as a nitrogen (N) limited habitat, and this has guided the development of conceptual biogeochemical models focusing largely on the reservoir of nitrate as the critical source of N to sustain primary productivity. However, selected groups of Bacteria, including cyanobacteria, and Archaea can utilize dinitrogen (N2) as an alternative N source. In the marine environment, these microorganisms can have profound effects on net community production processes and can impact the coupling of C-N-P cycles as well as the net oceanic sequestration of atmospheric carbon dioxide. As one component of an integrated ‘Nitrogen Transport and Transformations’ project, we have begun to re-assess our understanding of (1) the biotic sources and rates of N2 fixation in the world’s oceans, (2) the major controls on rates of oceanic N2 fixation, (3) the significance of this N2 fixation for the global carbon cycle and (4) the role of human activities in the alteration of oceanic N2 fixation. Preliminary results indicate that rates of N2 fixation, especially in subtropical and tropical open ocean habitats, have a major role in the global marine N budget. Iron (Fe) bioavailability appears to be an important control and is, therefore, critical in extrapolation to global rates of N2 fixation. Anthropogenic perturbations may alter N2 fixation in coastal environments through habitat destruction and eutrophication, and open ocean N2 fixation may be enhanced by warming and increased stratification of the upper water column. Global anthropogenic and climatic changes may also affect N2 fixation rates, for example by altering dust inputs (i.e. Fe) or by expansion of subtropical boundaries. Some recent estimates of global ocean N2 fixation are in the range of 100−200 Tg N (1−2 × 1014 g N) yr −1, but have large uncertainties. These estimates are nearly an order of magnitude greater than historical, pre-1980 estimates, but approach modern estimates of oceanic denitrification.

Key words

bacteria biogeochemistry climate cyanobacteria iron nitrogen oceanic N2 fixation phosphorus Trichodesmium 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 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: 83–88CrossRefGoogle Scholar
  2. 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: 535–554CrossRefGoogle Scholar
  3. Beget JE (1996) Tephrochronology and paleoclimatology of the last interglacial-glacial cycle recorded in Alaskan loess deposits. Quat. Int. 34–36: 121–126CrossRefGoogle Scholar
  4. 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 YorkCrossRefGoogle Scholar
  5. Bergman B & Carpenter EJ (1991) Nitrogenase confined to randomly distributed trichomes in the marine cyanobacterium Trichodesmium thiebautii. J. Phycol. 27: 158–165CrossRefGoogle Scholar
  6. 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: 3239–3244PubMedGoogle Scholar
  7. Bergman B, Gallon JR, Rai AN & Stal LJ (1997) N2 fixation by non-heterocystous cyanobacteria. FEMS Microbiol. Rev. 19: 139–185Google Scholar
  8. Bishop PE, Jarlenski DML & Hetherington DR (1980) Evidence for an alternative nitrogen fixation system in Azotobacter vinelandii. Proc. Natl. Acad. Sci. USA 77: 7342–7346PubMedCrossRefGoogle Scholar
  9. 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 YorkGoogle Scholar
  10. 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 NetherlandsCrossRefGoogle Scholar
  11. 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: 1680–1689CrossRefGoogle Scholar
  12. Broughton WJ & Pühler A (Eds) (1986) Nitrogen Fixation, Volume 4: Molecular Biology. Clarendon Press, OxfordGoogle Scholar
  13. Bryceson I & Fay P (1981) Nitrogen fixation in Oscillatoria (Trichodesmium) erythraea in relation to bundle formation and trichome differentiation. Mar. Biol. 61: 159–166CrossRefGoogle Scholar
  14. Burns RC & Hardy RWF (1975) Nitrogen fixation in bacteria and higher plants. Springer-Verlag, New YorkCrossRefGoogle Scholar
  15. Burris RH (1991) Nitrogenases. J. Biol. Chem. 266: 9339–9342PubMedGoogle Scholar
  16. Capone DG (1988) Benthic nitrogen fixation. In: Blackburn H & Sorensen J (Eds) NitrogenGoogle Scholar
  17. Cycling in Coastal Marine Environments (pp 85–123). John Wiley, New YorkGoogle Scholar
  18. Capone DG & Carpenter EJ (1982) Nitrogen fixation in the marine environment. Science 217: 1140–1142PubMedCrossRefGoogle Scholar
  19. Capone DG & Carpenter EJ (1999) Nitrogen fixation by marine cyanobacteria: Historical and global perspectives. Bull. Inst. Oceanogr. Monaco 19: 235–256Google Scholar
  20. 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: 3989–3995PubMedGoogle Scholar
  21. 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: 3532–3536PubMedGoogle Scholar
  22. Capone DG, Zehr JP, Paerl HW, Bergman B & Carpenter EJ (1997) Trichodesmium a globally significant marine cyanobacterium. Science 276: 1221–1229Google Scholar
  23. Carpenter EJ (1972) Nitrogen fixation by a blue-green epiphyte on pelagic Sargassum. Science 178: 1207–1209PubMedCrossRefGoogle Scholar
  24. 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 YorkGoogle Scholar
  25. 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: 3122–3129PubMedGoogle Scholar
  26. 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 NetherlandsCrossRefGoogle Scholar
  27. 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: 151–158CrossRefGoogle Scholar
  28. Carpenter EJ & Culliney JL (1975) Nitrogen fixation in marine shipworms. Science 187: 551–552PubMedCrossRefGoogle Scholar
  29. Carpenter EJ, Harvey HR, Fry B & Capone DG (1997) Biogeochemical tracers of the marine cyanobacterium Trichodesmium. Deep-Sea Res. 44: 27–38CrossRefGoogle Scholar
  30. 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: 295–304CrossRefGoogle Scholar
  31. Carpenter EJ & Price CC, IV (1976) Marine Oscillatoria (Trichodesmium): Explanation for aerobic nitrogen fixation without heterocysts. Science 191: 1278–1280PubMedCrossRefGoogle Scholar
  32. Carpenter EJ & Roenneberg T (1995) The marine planktonic cyanobacteria Trichodesmium spp.: photosynthetic rate measurements in the SW Atlantic Ocean. Mar. Ecol. Prog. Ser. 118: 267–273CrossRefGoogle Scholar
  33. Carpenter EJ & Romans, K (1991) Major role of the cyanobacterium Trichodesmium in nutrient cycling in the North Atlantic Ocean. Science 254: 1356–1358PubMedCrossRefGoogle Scholar
  34. Checkley DM Jr & Miller CA (1989) Nitrogen isotope fractionation by oceanic zooplankton. Deep-Sea Res. 36: 1449–1456CrossRefGoogle Scholar
  35. 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 YorkGoogle Scholar
  36. Cole JJ, Lane JM, Marino R & Howarth RW (1993) Molybdenum assimilation by cyanobacteria and phytoplankton in freshwater and salt water. Limnol. Oceanogr. 38: 25–35CrossRefGoogle Scholar
  37. 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, AlbertaGoogle Scholar
  38. 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 pressGoogle Scholar
  39. Davey A & Marchant HJ (1983) Seasonal variation in nitrogen fixation by Nostoc commune Vaucher at the Vestfold Hills, Antarctica. Phycologia 22: 337–385CrossRefGoogle Scholar
  40. Dean DR, Bolin JT & Zheng L (1993) Nitrogenase metalloclusters: Structures, organization, and synthesis. J. Bact. 175: 6737–6744PubMedGoogle Scholar
  41. Delwiche CC (1970) The nitrogen cycle. Sci. Amer. 223: 137–146PubMedCrossRefGoogle Scholar
  42. Delwiche C & Likens G (1977) Global chemical cycles and their alteration by man. Dahlem Konferenzen, BerlinGoogle Scholar
  43. Deutsch CA, Gruber NP, Key RM, Sarmiento JL & Ganachaud A (2001) Denitrification and N2 fixation in the Pacific Ocean. Global Biogeochem. Cycles 15: 483–506CrossRefGoogle Scholar
  44. Dickey TD (1991) The emergence of concurrent high-resolution physical and bio-opticalGoogle Scholar
  45. measurements in the upper ocean and their applications. Rev. Geophys. 29: 383–413Google Scholar
  46. Dore JE, Popp BN, Karl DM & Sansone FJ (1998) A large source of atmospheric nitrous oxide from subtropical North Pacific surface waters. Nature 396: 63–66CrossRefGoogle Scholar
  47. Duarte CM (1992) Nutrient concentration of aquatic plants: Patterns across species. Limnol. Oceanogr. 37: 882–889CrossRefGoogle Scholar
  48. Dugdale RC & Goering JJ (1967) Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol. Oceanogr. 12: 196–206CrossRefGoogle Scholar
  49. Dugdale RC, Menzel DW & Ryther JH (1961) Nitrogen fixation in the Sargasso Sea. Deep-Sea Res. 7: 298–300Google Scholar
  50. 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 NetherlandsCrossRefGoogle Scholar
  51. 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, 16Google Scholar
  52. Dupouy C, Petit M & Dandonneau Y (1988) Satellite detected cyanobacteria bloom in the southwestern tropical Pacific. Int. J. Remote Sens. 9: 389–396CrossRefGoogle Scholar
  53. Falkowski PG (1997) Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387: 272–275CrossRefGoogle Scholar
  54. Fallik E, Chan Y-K & Robson RL (1991) Detection of alternative nitrogenases in aerobic gram-negative nitrogen-fixing bacteria. J Bact. 173: 365–371PubMedGoogle Scholar
  55. Fanning KA (1989) Influence of atmospheric pollution on nutrient limitation in the ocean. Nature 339: 460–463CrossRefGoogle Scholar
  56. Fanning KA (1992) Nutrient provinces in the sea: Concentration ratios, reaction rate ratios, and ideal covariation. J. Geophys. Res. 97: 5693–5712CrossRefGoogle Scholar
  57. Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol. Rev. 546: 340–373Google Scholar
  58. Fogg GE (1974) Nitrogen fixation. In: Stewart WDP (Ed) Algal Physiology and Biochemistry (pp 560–582 ). Blackwell, OxfordGoogle Scholar
  59. Fogg GE (1982) Nitrogen cycling in sea waters. Phil. Trans. R. Soc. London 296: 299–576Google Scholar
  60. Fredriksson C & Bergman B (1997) Ultrastructural characterization of cells specialized for nitrogen fixation in a non-heterocystous cyanobcterium, Trichodesmium. Protoplasma 197: 76–85CrossRefGoogle Scholar
  61. Gallon JR (1981) The oxygen sensitivity of nitrogenase: a problem for biochemists and microorganisms. Trends Biochem. Sci. 6: 19–23Google Scholar
  62. Gallon JR (1992) Reconciling the incompatible: N2 fixation and 02. Tansley review No. 144. New Phytol. 122: 571–609CrossRefGoogle Scholar
  63. 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 NetherlandsCrossRefGoogle Scholar
  64. Galloway JN, Schlesinger WH, Levy II H, Michaels A & Schnoor JL (1995) Nitrogen fixation: Anthropogenic enhancement-environmental response. Global Biogeochem. Cycles 9: 235–252CrossRefGoogle Scholar
  65. 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: 41CrossRefGoogle Scholar
  66. Glibert PM & Bronk DA (1994) Release of dissolved organic nitrogen by marine diazotrophic cyanobacteria, Trichodesmium spp. Appl. Environ. Microbiol. 60: 3996–4000PubMedGoogle Scholar
  67. 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: 83–88CrossRefGoogle Scholar
  68. Gruber N & Sarmiento JL (1997) Global patterns of marine nitrogen fixation and denitrification. Global Biogeochem. Cycles 11: 235–266CrossRefGoogle Scholar
  69. Guerinot ML & Colwell RR (1985) Enumeration, isolation, and characterization of N2-fixing bacteria from seawater. Appl Environ. Microbiol. 50: 350–355Google Scholar
  70. Guerinot ML & Patriquin DG (1981) The association of N2-fixing bacteria with sea urchins. Mar. Biol. 62: 197–207CrossRefGoogle Scholar
  71. Guerinot ML, West PA, Lee JV & Colwell RR (1982) Vibrio diazotrophicus sp. nov., a marine nitrogen-fixing bacterium. Int. J. Syst. Bact. 32: 350–357Google Scholar
  72. Hanson RB (1977) Pelagic Sargassum community metabolism: Carbon and nitrogen. J. Exp. Mar. Biol. Ecol. 29: 107–118CrossRefGoogle Scholar
  73. Haxo FT, Lewin RA, Lee KW & Li M-R (1987) Fine structure and pigments of Oscillatoria (Trichodesmium) aff. Thiebautii (Cyanophyta) in culture. Phycologia 26: 443–456CrossRefGoogle Scholar
  74. Hecky RE, Campbell P & Hendzel LL (1993) The stoichiometry of carbon, nitrogen, and phosphorus in particulate matter of lakes and oceans. Limnol. Oceanogr. 38: 709–724CrossRefGoogle Scholar
  75. Hood RR, Michaels AF & Capone DG (2000) Answers sought to the enigma of marine nitrogen fixation. Eos, Trans. Amer. Geophys. Un. 81: 133, 138, 139Google Scholar
  76. Howard JB & Rees DC (1996) Structural basis of biological nitrogen fixation. Chem. Rev. 96: 2965–2982PubMedCrossRefGoogle Scholar
  77. 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: 203–231Google Scholar
  78. Howarth RW & Cole JJ (1985) Molybdenum availability, nitrogen limitation and phytoplankton growth in natural waters. Science 229: 653–655PubMedCrossRefGoogle Scholar
  79. Howarth RW, Marino R, Lane J & Cole JJ (1988) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 2. Biogeochemical controls. Limnol. Oceanogr. 33: 688–701CrossRefGoogle Scholar
  80. 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: 16889–16909CrossRefGoogle Scholar
  81. 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: 57–65Google Scholar
  82. Janson S, Carpenter EJ & Bergman B (1994) Compartmentalization of nitrogenase in a nonheterocystous cyanobacterium Trichodesmium contortum. FEMS Microbiol. Lett. 118: 914Google Scholar
  83. 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: 463–477CrossRefGoogle Scholar
  84. Janson S, Wouters J, Bergman B & Carpenter EJ (1999b) Host specificity in the Richeliadiatom symbiosis by hetR gene sequence analysis. Environ. Microbiol. 1: 431–438PubMedCrossRefGoogle Scholar
  85. Johnson KJ, Gordon RM & Coale KH (1997) What controls dissolved iron concentrations in the world ocean? Mar. Chem. 57: 181Google Scholar
  86. Joussaume S (1993) Paleoclimatic tracers: An investigation using an atmospheric general circulation model under ice age conditions–1. Desert dust. J. Geophys. Res. 98: 2767–2805CrossRefGoogle Scholar
  87. Kana TM (1993) Rapid oxygen cycling in Trichodesmium thiebautii. Limnol. Oceanogr. 38: 18–24CrossRefGoogle Scholar
  88. Karl DM (1999) A sea of change: Biogeochemical variability in the North Pacific subtropical gyre. Ecosystems 2: 181–214CrossRefGoogle Scholar
  89. Karl DM (2000) A new source of `new’ nitrogen in the sea. Trends in Microbiol. 8: 301 (Comment section)Google Scholar
  90. 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. II 48: 1529–1566Google Scholar
  91. 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 NetherlandsCrossRefGoogle Scholar
  92. 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. Nature 388: 533–538CrossRefGoogle Scholar
  93. Karl DM & Tien G (1997) Temporal variability in dissolved phosphorus concentrations in the subtropical North Pacific Ocean. Mar. Chem. 56: 77–96CrossRefGoogle Scholar
  94. Keene WC & Savoie DL (1998) The pH of deliquesced sea-salt aerosol in polluted marine air. Geophys. Res. Lett. 25: 2181–2184CrossRefGoogle Scholar
  95. Kim J & Rees DC (1994) Nitrogenase and biological nitrogen fixation. Biochem. 33: 389–397CrossRefGoogle Scholar
  96. 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: 305–309CrossRefGoogle Scholar
  97. Kuchler DA & Jupp DLB (1988) Shuttle photograph captures massive phytoplankton bloom in the Great Barrier Reef. Int. J. Remote Sensing 9: 1299–1301CrossRefGoogle Scholar
  98. Letelier RM & Karl DM (1996) Role of Trichodesmium spp. in the productivity of the subtropical North Pacific Ocean. Mar. Ecol. Prog. Ser. 133: 263–273CrossRefGoogle Scholar
  99. Letelier RM & Karl DM (1998) Trichodesmium spp. physiology and nutrient fluxes in the North Pacific subtropical gyre. Aquat. Microb. Ecol. 15: 265–276Google Scholar
  100. LeTraon PY (1990) A method for optimal analysis of fields with spatially variable mean. J. Geophys. Res. 95: 13543–13547CrossRefGoogle Scholar
  101. Li WKW, Glover HE & Morris I (1980) Physiology of carbon assimilation by Oscillatoria thiebautii in the Caribbean Sea. Limnol. Oceanogr. 25: 447–456CrossRefGoogle Scholar
  102. 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: 3052–3064Google Scholar
  103. Lipschultz F & Owens NJ (1996) An assessment of nitrogen fixation as a source of nitrogen to the North Atlantic Ocean. Biogeochem. 35: 261–274CrossRefGoogle Scholar
  104. Liu K-K, Su M-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: 273–292CrossRefGoogle Scholar
  105. Liu T, An Z, Yuan B & Han J (1985) The loess-paleosol sequence in China and climatic history. Episodes 8: 21–28Google Scholar
  106. Longhurst A (1998) Ecological Geography of the Sea. Academic Press, San Diego, CaliforniaGoogle Scholar
  107. Longhurst AR & Harrison WG (1989) The biological pump: profiles of plankton production and consumption in the upper ocean. Prog. Oceanog. 22: 47–123CrossRefGoogle Scholar
  108. 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.Google Scholar
  109. Mague TH, Weare NM & Holm-Hansen 0 (1974) Nitrogen fixation in the North Pacific Ocean. Mar. Biol. 24: 109–119CrossRefGoogle Scholar
  110. 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 pressGoogle Scholar
  111. Martinez L, Silver MW, King JM & Alldredge AL (1983) Nitrogen fixation by floating diatom mats: A source of new nitrogen to oligotrophic ocean waters. Science 221: 152–154PubMedCrossRefGoogle Scholar
  112. 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, LondonGoogle Scholar
  113. McElroy MB (1983) Marine biological controls on atmospheric CO2 climate. Nature 302: 328–329CrossRefGoogle Scholar
  114. Michaels AF, Bates NR, Buesseler KO, Carlson CA & Knap AH (1994) Carbon-cycle imbalances in the Sargasso Sea. Nature 372: 537–540CrossRefGoogle Scholar
  115. Michaels AF, Karl DM & Capone D (2001) Redfield stoichiometry, new production and nitrogen fixation. Oceanography (Special JGOFS edition), in pressGoogle Scholar
  116. 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: 181–226CrossRefGoogle Scholar
  117. Mitsui A, Kumazawa S, Takahashi A, Ikemoto H, Cao S & Arai T (1986) Strategy by which nitrogen-fixing unicellular cyanobacteria grow photoautotrophically. Nature 323: 720–722CrossRefGoogle Scholar
  118. Montoya JP, Voss M, Kaehler P & Capone DG (1996) A simple, high precision tracer assay for dinitrogen fixation. Appl. Environ. Microbiol. 62: 986–993PubMedGoogle Scholar
  119. 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: 51–58CrossRefGoogle Scholar
  120. Mulholland MR, Ohki K & Capone DG (1999) Nitrogen utilization and metabolism relative to patterns of N2 fixation in cultures of Trichodesmium NIBB 1067. J. Phycol. 35: 977–988CrossRefGoogle Scholar
  121. Niemi A (1979) Blue-green algal blooms and N:P ratios in the Baltic Sea. Acta Bot. Fenn. 110: 57–61Google Scholar
  122. Ohki K & Fujita Y (1982) Laboratory culture of the pelagic blue-green alga Trichodesmium thiebautii: Conditions for unialgal culture. Mar. Ecol. Prog. Ser. 7: 185–190CrossRefGoogle Scholar
  123. 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: 111–114CrossRefGoogle Scholar
  124. Ohki K, Rueter JG & Fujita Y (1986) Cultures of the pelagic cyanophytes Trichodesmium erythraeum and T. thiebautii in synthetic medium. Mar. Biol. 91: 9–13CrossRefGoogle Scholar
  125. 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. NIBB 1067. Arch. Microbiol. 156: 335–337CrossRefGoogle Scholar
  126. Owens NJP (1987) Natural variations in 15N in the marine environment. Adv. Mar. Biol. 24: 389–451CrossRefGoogle Scholar
  127. Paerl HW (1994) Spatial segregation of CO2 fixation in Trichodesmium sp.: Linkage to N2 fixation potential. J. Phycol. 30: 790–799CrossRefGoogle Scholar
  128. Paerl HW (2000) Physical-chemical constraints on cyanobacterial growth in the oceans. International Symposium on Marine Cyanobacteria and Related Organisms, Institut Oceanographique, ParisGoogle Scholar
  129. Paerl HW & Bebout BM (1988) Direct measurement of 02-depleted microzones in marine Oscillatoria: relation to N2 fixation. Science 241: 442–445PubMedCrossRefGoogle Scholar
  130. Paerl HW, Bebout BM & Prufert LE (1989a) Bacterial associations with marine Oscillatoria sp. (Trichodesmium sp.) populations: Ecophysiological implications. J. Phycol. 25: 773–784CrossRefGoogle Scholar
  131. 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: 218–226PubMedGoogle Scholar
  132. 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: 525–536CrossRefGoogle Scholar
  133. Paerl HW & Pinckney JL (1996) A mini-review of microbial consortia: their roles in aquatic production and biogeochemical cycling. Microb. Ecol. 31: 225–247PubMedCrossRefGoogle Scholar
  134. Paerl HW, Priscu JC & Brawner DL (1989b) Immunochemical localization of nitrogenase in marine Trichodesmium aggregates: Relationship to N2 fixation potential. Appl. Environ. Microbiol. 55: 2965–2975PubMedGoogle Scholar
  135. 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: 1044–1047PubMedGoogle Scholar
  136. Paerl HW & Zehr JP (2000) Marine nitrogen fixation. In: Kirchman DL (Ed) Paerl HW & Zehr JP (pp 387–426 ). Wiley-LissGoogle Scholar
  137. Paul EA (1978) Contribution of nitrogen fixation to ecosystem functioning and nitrogen fluxes on a global basis. Ecol. Bull. 26: 282–293Google Scholar
  138. 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: 1325–1334CrossRefGoogle Scholar
  139. 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: 77–88CrossRefGoogle Scholar
  140. Platt T & Sathyendranath S (1999) Spatial structure of pelagic ecosystem processes in the global ocean. Ecosystems 2: 384–394CrossRefGoogle Scholar
  141. Postgate JR (1982) The Fundamentals of Nitrogen Fixation. Cambridge University Press, CambridgeGoogle Scholar
  142. Prentice IC & Webb III T (1998) BIOME 6000: Reconstructing global mid-HoloceneGoogle Scholar
  143. vegetation patterns from paleoecological records. J. Biogeogr. 25: 995–1005Google Scholar
  144. Proctor LM (1997) Nitrogen-fixing, photosynthetic, anaerobic bacteria associated with pelagic copepods. Aquat. Microbiol. Ecol. 12: 105–113CrossRefGoogle Scholar
  145. 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: 27–73CrossRefGoogle Scholar
  146. Prospero JM & Nees RT (1986) Impact of the North African drought and El Nino on mineral dust in the Barbados trace winds. Nature 320: 735–738CrossRefGoogle Scholar
  147. Prufert-Bebout L, Paerl HW & Lassen C (1993) Growth, nitrogen fixation, and spectral attenuation in cultivated Trichodesmium species. Appl. Environ. Microbiol. 59: 1367–1375PubMedGoogle Scholar
  148. Rasche ME & Seefeldt LC (1997) Reduction of thiocyanate, cyanate, and carbon disulfide by nitrogenase: Kinetic characterization and EPR spectroscopic analysis. Biochem. 36: 8574–8585CrossRefGoogle Scholar
  149. Raven JA (1988) The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytol. 109: 279–287CrossRefGoogle Scholar
  150. Rea DK (1994) The paleoclimatic record provided by eolian deposition in the deep sea: The geologic history of wind. Rev. Geophys. 32: 159–195CrossRefGoogle Scholar
  151. Robson RL & Postgate JR (1980) Oxygen and hydrogen in biological nitrogen fixation. Ann. Rev. Microbiol. 34: 183–207CrossRefGoogle Scholar
  152. 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: 117–138CrossRefGoogle Scholar
  153. 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 NetherlandsCrossRefGoogle Scholar
  154. Saino T & Hattori A (1978) Diel variation in nitrogen fixation by a marine blue-green alga, Trichodesmium thiebautii. Deep-Sea Res. 25: 1259–1263CrossRefGoogle Scholar
  155. 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. TokyoGoogle Scholar
  156. Saino T & Hattori A (1980) 15N natural abundance in oceanic suspended particulate matter. Nature 283: 752–754Google Scholar
  157. 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: 807–827CrossRefGoogle Scholar
  158. Scranton MI (1983) The role of the cyanobacterium Oscillatoria (Trichodesmium) thiebautii in the marine hydrogen cycle. Mar. Ecol. Prog. Ser. 11: 79–87CrossRefGoogle Scholar
  159. 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: 53825389Google Scholar
  160. Siddiqui PJA, Bergman B & Carpenter EJ (1992) Filamentous cyanobacterial associates of the marine planktonic cyanobacterium Trichodesmium. Phycologia 31: 326–337CrossRefGoogle Scholar
  161. 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: 3511–3526CrossRefGoogle Scholar
  162. Siefert RL, Webb SM & Hoffmann MR (1996) Determination of photochemically available iron in ambient aerosol. J. Geophys. Res. 101: 14441–14449CrossRefGoogle Scholar
  163. Siegenthaler U & Sarmiento J (1993) Atmospheric carbon dioxide and the oceans. Nature 365: 119–125CrossRefGoogle Scholar
  164. Sigman DM, Altabet MA, McCorkle DC, Francois R & Fischer G (1999) The 8 15 N of nitrate in the Southern Ocean: Nitrate consumption in surface waters. Global Biogeochem. Cycles 13: 1149–1166CrossRefGoogle Scholar
  165. Sigman DM, Altabet MA, McCorkle DC, Francois R & Fischer G (2000) The 815N of nitrate in the Southern Ocean: Nitrogen cycling and circulation in the ocean interior. J. Geophys. Res. in pressGoogle Scholar
  166. 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: 227–242CrossRefGoogle Scholar
  167. Simpson FB & Burris RH (1984) A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase. Science 224: 1095–1097PubMedCrossRefGoogle Scholar
  168. Smith BE & Eady RR (1992) Metalloclusters of the nitrogenases. Eur. J. Biochem. 205: 1–15 Soderlund R & Rosswall T (1982) The nitrogen cycles. In: Hutzinger O (Ed) The Natural Environment and the Biogeochemical Cycles (pp 61–81 ).Google Scholar
  169. Springer-Verlag, New York 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., StockholmGoogle Scholar
  170. Sprent JI & Sprent P (1990) Nitrogen Fixing Organisms: Pure and Applied Aspects. Chapman and Hall, New YorkCrossRefGoogle Scholar
  171. Stal LJ (1995) Physiological ecology of cyanobacteria in microbial mats and other communities. Tansley Review No. 84. New Phytol. 131: 1–32CrossRefGoogle Scholar
  172. Stal LJ & Krumbein WE (1985) Oxygen protection of nitrogenase in the aerobically nitrogen fixing, non-heterocystous cyanobacterium Oscillatoria sp. Arch. Microbiol. 143: 72–76CrossRefGoogle Scholar
  173. Stal LJ, Staal M & Villbrandt M (1999) Nutrient control of cyanobacterial blooms in the Baltic Sea. Aquat. Microb. Ecol. 18: 165–173CrossRefGoogle Scholar
  174. Stewart WDP, Fitzgerald GP & Burris RH (1967) In situ studies on N2 fixation using the acetylene reduction technique. Proc. Natl. Acad. Aci. USA 58: 2071–2078Google Scholar
  175. 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: 1559–1569CrossRefGoogle Scholar
  176. 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: 618–627CrossRefGoogle Scholar
  177. 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: 608–617CrossRefGoogle Scholar
  178. 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: 8292–8299PubMedCrossRefGoogle Scholar
  179. Tans PP, Fung IY & Takahashi T (1990) Observational constraints on the global atmospheric CO2 budget. Science 247: 1431–1438PubMedCrossRefGoogle Scholar
  180. Tassan S (1995) SeaWiFS potential for remote sensing of marine Trichodesmium at sub-bloom concentration. Int. J. Remote Sensing 16: 3619–3627CrossRefGoogle Scholar
  181. Toggweiler JR (1999) An ultimate limiting nutrient. Nature 400: 511–512CrossRefGoogle Scholar
  182. Trenberth KE & Hoar Tl (1997) El Nino and climate change. Geophys. Res. Lett. 24: 30573060Google Scholar
  183. Tyrrell T (1999) The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400: 525–531CrossRefGoogle Scholar
  184. Urdaci MC, Stal LJ & Marchand M (1988) Occurrence of nitrogen fixation among Vibrio spp. Arch. Microbiol. 150: 224–229CrossRefGoogle Scholar
  185. Venrick EL (1974) The distribution and significance of Richelia intracellularis Schmidt in the North Pacific Central Gyre. Limnol. Oceanogr. 19: 437–445CrossRefGoogle Scholar
  186. Villareal TA (1991) Nitrogen-fixation by the cyanobacterial symbiont of the diatom genus Hemiaulus. Mar. Ecol. Prog. Ser. 76: 201–204CrossRefGoogle Scholar
  187. Villareal TA, Altabet MA & Culver-Rymsza K (1993) Nitrogen transport by vertically migrating diatom mats in the North Pacific Ocean. Nature 363: 709–712CrossRefGoogle Scholar
  188. Villareal TA, Pilskaln C, Brzezinski M, Lipschultz F, Dennett M & Gardner GB (1999) Upward transport of oceanic nitrate by migrating diatom mats. Nature 397: 423–425CrossRefGoogle Scholar
  189. 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: 1–45CrossRefGoogle Scholar
  190. 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, TokyoGoogle Scholar
  191. Wada E & Hattori A (1991) Nitrogen in the Sea: Forms, Abundances, and Rate Processes. CRC Press, Boca Raton, FL.Google Scholar
  192. Waterbury JB, Watson SW & Valois FW (1988) Temporal separation of photosynthesis and dinitrogen fixation in the marine unicellular cyanobacterium: Erythrospira marina. Eos 69: 1089Google Scholar
  193. 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: 159–177CrossRefGoogle Scholar
  194. 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, BerlinCrossRefGoogle Scholar
  195. 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: 61–73CrossRefGoogle Scholar
  196. Zehr JP & Capone DG (1996) Problems and promise of assaying the genetic potential for nitrogen fixation in the marine environment. Microb. Ecol. 32: 263–281PubMedCrossRefGoogle Scholar
  197. 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: 2522–2526PubMedGoogle Scholar
  198. 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: 3444–3450PubMedGoogle Scholar
  199. 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, LondonCrossRefGoogle Scholar
  200. Zehr JP, Carpenter EJ & Villareal TA (2000) New perspectives on nitrogen-fixing microorganisms in tropical and subtropical oceans. Trends in Microbiol. 8: 68–73CrossRefGoogle Scholar
  201. 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: 2129721305Google Scholar
  202. 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: 537–539CrossRefGoogle Scholar
  203. 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: 4243–4251PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2002

Authors and Affiliations

  • D. Karl
    • 1
  • A. Michaels
    • 2
  • B. Bergman
    • 3
  • D. Capone
    • 2
  • E. Carpenter
    • 4
  • R. Letelier
    • 5
  • F. Lipschultz
    • 6
  • H. Paerl
    • 7
  • D. Sigman
    • 8
  • L. Stal
    • 9
  1. 1.School of Ocean and Earth Science and Technology, Department of OceanographyUniversity of HawaiiHonoluluUSA
  2. 2.Wrigley Institute for Environmental StudiesUniversity of Southern CaliforniaLos AngelesUSA
  3. 3.Department of BotanyStockholm UniversityStockholmSweden
  4. 4.Romberg Tiburon CenterSan Francisco State UniversityTiburonUSA
  5. 5.College of Oceanic and Atmospheric SciencesOregon State UniversityCorvallisUSA
  6. 6.Bermuda Biological Station for ResearchBermudaUSA
  7. 7.Institute of Marine SciencesUniversity of North Carolina — Chapel HillMorehead CityUSA
  8. 8.Department of GeosciencesPrinceton UniversityPrincetonUSA
  9. 9.Netherlands Institute of EcologyCentre for Estuarine & Coastal EcologyAC YersekeThe Netherlands

Personalised recommendations