A Review on Marine N2 Fixation: Mechanism, Evolution of Methodologies, Rates, and Future Concerns

  • P. S. Bhavya
  • Jun-Oh Min
  • Min-Seob Kim
  • Hyo Keun Jang
  • Kwanwoo Kim
  • Jae Joong Kang
  • Jae Hyung Lee
  • Dabin Lee
  • Naeun Jo
  • Myung Joon Kim
  • Yejin Kim
  • Junbeom Lee
  • Chang Hwa Lee
  • Hyeonji Bae
  • Hyeju Yoo
  • Sanghoon Park
  • Mi Sun Yun
  • Sang Heon LeeEmail author


Investigations on marine N2 fixation have gained momentum since 1960s with eventual establishments of relevant methodologies to identify species involved and quantify the rates. The evolution of various methodologies to understand N2 fixation and to estimate its rates were underpinned by the constant efforts of pioneers in the ocean biogeochemical research field. Those efforts succeeded in introducing various methodologies that include experimental (15N2 bubble method and acetylene reduction method), geochemical (N* and P* method), mathematical modelling, and remote sensing techniques. However, the construction of an accurate N budget is still under progress due to inseparable issues associated with each method and difficulties in conducting the experiments onboard on a larger scale. Nevertheless, the contributions by each of the methodologies are significant and helped in forming basic ideas about N2 fixation activities on a global scale. It is not only important to recognize the contributions made by the formation of various methodologies by marine research pioneers, but also vital to summarize what we have achieved in the marine N2 fixation research area so far. Hence, this review is an attempt to brief on the various milestones achieved in research on the N2 fixation mechanism, species involved, evolution of methodologies to estimate N2 fixation rates, species identification, budgets, and future concerns.


N2 fixation climate change 15N2 labelling cyanobacteria 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



This research was a part of the project entitled “Construction of Ocean Research Station and their application” and “Im provements of ocean prediction accuracy using numerical modeling and artificial intelligence technology” funded by the Ministry of Oceans and Fisheries, Korea. This research was also partly supported by a grant from the National Institute of Fisheries Science (NIFS) in the Republic of Korea (grant number: R2019062).


  1. Ahmed A, Gauns M, Kurian S, Bardhan P, Pratihary A, Naik H, Damodar M, Naqvi SWA (2017) Nitrogen fixation rates in the eastern Arabian Sea. Estuar Coast Shelf S 191:74–83CrossRefGoogle Scholar
  2. Altabet MA (2007) Constraints on oceanic N balance/imbalance from sedimentary 15N records. Biogeosciences 4:75–86. doi: CrossRefGoogle Scholar
  3. Arístegui J, Agustí S, Middelburg JJ, Duarte CM (2005) Respiration in the mesopelagic and bathypelagic zones of the oceans. In: Giorgio PAD, Williams P (eds) Respiration in aquatic ecosystems. Oxford University Press, Oxford, pp 182–206Google Scholar
  4. Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, Leggat W, Price GD (1998) The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Can J Botany 76(6):1052–1071Google Scholar
  5. Bauer JE, Cai WJ, Raymond PA, Bianchi TS, Hopkinson CS, Regnier PA (2013) The changing carbon cycle of the coastal ocean. Nature 504(7478):61–70CrossRefGoogle Scholar
  6. Benavides M, Agawin NS, Arístegui J, Ferriol P, Stal LJ (2011) Nitrogen fixation by Trichodesmium and small diazotrophs in the subtropical northeast Atlantic. Aquat Microb Ecol 65(1):43–53CrossRefGoogle Scholar
  7. Benavides M, Bonnet S, Berman-Frank I, Riemann L (2018) Deep into oceanic N2 fixation. Front Mar Sci 5:108. doi: CrossRefGoogle Scholar
  8. Benavides M, Voss M (2015) Five decades of N2 fixation research in the North Atlantic Ocean. Front Mar Sci 2:40. doi: CrossRefGoogle Scholar
  9. Benavides MH, Moisander P, Berthelot H, Dittmar T, Grosso O, Bonnet S (2015) Mesopelagic N2 fixation related to organic matter composition in the Solomon and Bismarck Seas (Southwest pacific). PLoS One 10:e0143775. doi: CrossRefGoogle Scholar
  10. Bentzon-Tilia M, Traving SJ, Mantikci M, Knudsen-Leerbeck H, Hansen JLS, Markager S, Riemann L (2015) Significant N2 fixation by heterotrophs, photoheterotrophs and heterocystous cyanobacteria in two temperate estuaries. ISME J 9:273–285. doi: CrossRefGoogle Scholar
  11. Bergman B, Sandh G, Lin S, Larsson J, Carpenter EJ (2013) Trichodesmium–a widespread marine cyanobacterium with unusual nitrogen fixation properties. FEMS Microbiol Rev 37(3):286–302CrossRefGoogle Scholar
  12. Berthelot H, Benavides M, Moisander PH, Grosso O, Bonnet S (2017) High-nitrogen fixation rates in the particulate and dissolved pools in the Western Tropical Pacific (Solomon and Bismarck Seas). Geophys Res Lett 44:8414–8423. doi: CrossRefGoogle Scholar
  13. Bhavya PS, Kumar S, Gupta GVM, Sudheesh V, Sudharma K, Varrier DS, Dhanya KR, Saravanane N (2016) Nitrogen uptake dynamics in a tropical eutrophic estuary (Cochin, India) and adjacent coastal waters. Estuar Coast 39:54–67. doi: CrossRefGoogle Scholar
  14. Bhavya PS, Kumar S, Gupta GVM, Sudheesh V (2017) Carbon uptake rates in the Cochin estuary and adjoining coastal Arabian Sea. Estuar Coast 40(2):447–456CrossRefGoogle Scholar
  15. Bombar D, Paerl RW, Riemann L (2016) Marine non-cyanobacterial diazotrophs: Moving beyond molecular detection. Trends Microbiol 24:916–927. doi: CrossRefGoogle Scholar
  16. Bombar D, Paerl RW, Anderson R, Riemann L (2018) Filtration via conventional glass fiber filters in 15N2 tracer assays fails to capture all nitrogen-fixing Prokaryotes. Front Mar Sci 5:6. doi: CrossRefGoogle Scholar
  17. Bonnet S, Biegala IC, Dutrieux P, Slemons LO, Capone DG (2009) Nitrogen fixation in the western equatorial Pacific: rates, diazotrophic cyanobacterial size class distribution, and biogeochemical signific ance. Global Biogeochem Cy 23:GB3012. doi: CrossRefGoogle Scholar
  18. Bonnet S, Dekaezemacker J, Turk-Kubo KA, Moutin T, Hamersley RM, Grosso O, Zehr JP, Capone DG (2013) Aphotic N2 fixation in the eastern tropical South Pacific Ocean. PLoS One 8:e81265. doi: CrossRefGoogle Scholar
  19. Bonnet S, Caffin M, Berthelot H, Grosso O, Benavides M, Helias-Nunige S, Guieu C, Stenegren M, Foster RA (2018) In depth characterization of diazotroph activity across the western tropical south pacific hot spot of N2 fixation (OUTPACE cruise). Biogeosciences 15:4215–4232. doi: CrossRefGoogle Scholar
  20. Bonnet S, Caffin M, Berthelot H, Moutin T (2017) Hot spot of N2 fixation in the western tropical South Pacific pleads for a spatial decoupling between N2 fixation and denitrification. P Natl Acad Sci USA 114:E2800–E2801. doi: CrossRefGoogle Scholar
  21. Bonnet S, Rodier M, Turk-Kubo KA, Germineaud C, Menkes C, Ganachaud A, Cravatte S, Raimbault P, Campbell E, Queroue F, Sarthou G, Desnues A, Maes C, Eldin G (2015) Contrasted geographical distribution of N2 fixation rates and nifH phylotypes in the Coral and Solomon Seas (Southwestern Pacific) during austral winter conditions. Global Biogeochem Cy 29:1874–1892. doi: CrossRefGoogle Scholar
  22. Böttjer D, Dore JE, Karl DM, Letelier RM, Mahaffey C, Wilson ST, Zehr J, Church MJ (2017) Temporal variability of nitrogen fixation and particulate nitrogen export at Station ALOHA. Limnol Oceanogr 62(1):200–216CrossRefGoogle Scholar
  23. Breitbarth E, Wohlers J, Kläs J, LaRoche J, Peeken I (2008) Nitrogen fixation and growth rates of Trichodesmium IMS-101 as a function of light intensity. Mar Ecol-Prog Ser 359:25–36CrossRefGoogle Scholar
  24. Capone DG, Burns JA, Montoya JP, Subramaniam A, Mahaffey C, Gunderson T, Michaels AF, Carpenter EJ (2005) Nitrogen fixation by Trichodesmium spp.: An important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Global Biogeochem Cy 19:1–17. doi: CrossRefGoogle Scholar
  25. Capone DG, Carpenter EJ (1982) Nitrogen fixation in the marine environment. Science 217:1140–1142. doi: CrossRefGoogle Scholar
  26. Capone DG, Subramaniam A, Montoya JP, Voss M, Humborg C, Johansen AM, Siefert RL, Carpenter EJ (1998) An extensive bloom of the N2-fixing cyanobacterium Trichodesmium erythraeum in the central Arabian Sea. Mar Ecol-Prog Ser 172:281–292. doi: CrossRefGoogle Scholar
  27. Capone DG, Zehr JP, Paerl HW, Bergman B, Carpenter EJ (1997) Trichodesmium, a globally significant marine Cyanobacterium. Science 276:1221–1229. doi: CrossRefGoogle Scholar
  28. Carpenter EJ, Price CC (1977) Nitrogen fixation, distribution, and production of Oscillatoria (Trichodesmium) spp. in the western Sargasso and Caribbean Seas. Limnol Oceanogr 22:60–72. doi: CrossRefGoogle Scholar
  29. Carpenter EJ, Romans K (1991) Major role of the cyanobacterium Trichodesmium in nutrient cycling in the North Atlantic Ocean. Science 254:1356–1358. doi: CrossRefGoogle Scholar
  30. Carradec Q, Pelletier E, Da Silva C, Alberti A, Seeleuthner Y, Blanc-Mathieu R, Lima-Mendez G, Rocha F, Tirichine L, Labadie K, Kirilovsky A, Bertrand A, Engelen S, Madoui A, Meheust R, Poulain J, Romac S, Richter DJ, Yoshikawa G, Dimier C, Kandels-Lewis S, Picheral M, Searson S, Coordinaters TO, Jaillon O, Aury J, Karsenti E, Sullivan MB, Sunagawa S, Bork P, Not F, Hingamp P, Raes J, Guidi L, Ogata H, de Vargas C, Iudicone D, Bowler C, Wincker P (2018) A global ocean atlas of eukaryotic genes. Nat Commu 9(1):373. doi: CrossRefGoogle Scholar
  31. Chen YL, Chen HY, Tuo S, Ohki K (2008) Seasonal dynamics of new production from Trichodesmium N2 fixation and nitrate uptake in the upstream Kuroshio and South China Sea basin. Limnol Oceanogr 53:1705–1721. doi: CrossRefGoogle Scholar
  32. Church MJ, Björkman KM, Karl DM, Saito MA, Zehr JP (2008) Regional distributions of nitrogen-fixing bacteria in the Pacific Ocean. Limnol Oceanogr 53(1):63–77CrossRefGoogle Scholar
  33. Church MJ, Jenkins BD, Karl DM, Zehr JP (2005) Vertical distributions of nitrogen-fixing phylotypes at Stn ALOHA in the oligotrophic North Pacific Ocean. Aquat Microb Ecol 38(1):3–14CrossRefGoogle Scholar
  34. Church MJ, Mahaffey C, Letelier RM, Lukas R, Zehr JP, Karl DM (2009) Physical forcing of nitrogen fixation and diazotroph community structure in the North Pacific subtropical gyre. Global Biogeochem Cy 23:GB2020. doi: CrossRefGoogle Scholar
  35. Coles VJ, Wilson C, Hood RR (2004) Remote sensing of new production fueled by nitrogen fixation. Geophys Res Lett 31(6):GL019018. doi: CrossRefGoogle Scholar
  36. Dabundo R, Lehmann MF, Treibergs L, Tobias CR, Altabet MA, Moisander PH, Granger J (2014) The contamination of commercial 15N2 gas stocks with 15N-labeled nitrate and ammonium and consequences for nitrogen fixation measurements. PLoS One 9:e110335. doi: CrossRefGoogle Scholar
  37. Dekaezemacker J, Bonnet S, Grosso O, Moutin T, Bressac M, Capone D (2013) Evidence of active dinitrogen fixation in surface waters of the eastern tropical South Pacific during El Ni-o and La Ni-a events and evaluation of its potential nutrient controls. Global Biogeochem Cy 27:768–779. doi: CrossRefGoogle Scholar
  38. Deutsch C, Sarmiento JL, Sigman DM, Gruber N, Dunne JP (2007) Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445:163–167CrossRefGoogle Scholar
  39. Doney SC (2010) The growing human footprint on coastal and open-ocean biogeochemistry. Science 328:1512–1516CrossRefGoogle Scholar
  40. Dugdale RC, Goering JJ (1967) Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol Oceanogr 12:196–206CrossRefGoogle Scholar
  41. Dugdale RC, Goering JJ, Ryther JH (1964) High nitrogen fixation rates in the Sargasso sea and the arabian sea. Limnol Oceanogr 9(4):507–510CrossRefGoogle Scholar
  42. Falcón LI, Carpenter EJ, Cipriano F, Bergman B, Capone DG (2004) N2 fixation by unicellular bacterioplankton from the Atlantic and Pacific Oceans: Phylogeny and in situ rates. Appl Environ Microb 70:765–770. doi: CrossRefGoogle Scholar
  43. Farnelid H, Andersson AF, Bertilsson S, Al-Soud WA, Hansen LH, Sørensen S, Steward GF, Hagstrom A, Riemann L (2011) Nitrogenase gene amplicons from global marine surface waters are dominated by genes of non-cyanobacteria. PLoS One 6:e19223. doi: CrossRefGoogle Scholar
  44. Farnelid H, Turk-Kubo K, del Carmen Muñoz-Marín M, Zehr JP (2016) New insights into the ecology of the globally significant uncultured nitrogen-fixing symbiont UCYN-A. Aquat Microb Ecol 77(3):125–138CrossRefGoogle Scholar
  45. Fennel K, Spitz YH, Letelier RM, Abbott MR, Karl DM (2001) A deterministic model for N2 fixation at stn. ALOHA in the subtropical North Pacific Ocean. Deep-Sea Res Pt II 49(1–3):149–174CrossRefGoogle Scholar
  46. Fernández A, Mouriño-Carballido B, Bode A, Varela M, Marañón E (2010) Latitudinal distribution of Trichodesmium spp. and N2 fixation in the Atlantic Ocean. Biogeosciences 7:3167–3176. doi: CrossRefGoogle Scholar
  47. Flett RJ, Hamilton RD, Campbell NER (1976) Aquatic acetylene-reduction techniques: Solutions to several problems. Can J Microbiol 22(1):43–51CrossRefGoogle Scholar
  48. Gandhi N, Singh A, Prakash S, Ramesh R, Raman M, Sheshshayee M, Shetye S (2011) First direct measurements of N2 fixation during a Trichodesmium bloom in the eastern Arabian Sea. Global Biogeochem Cy 25:GB4014. doi: CrossRefGoogle Scholar
  49. Giller KE, Witty JF (1987) Immobilized 15N-fertilizer sources improve the accuracy of field estimates of N2-fixation by isotope dilution. Soil Biol Biochem 19(4):459–463CrossRefGoogle Scholar
  50. Goebel NL, Turk KA, Achilles KM, Paerl R, Hewson I, Morrison AE, Montoya JP, Edwards CA, Zehr JP (2010) Abundance and distribution of major groups of diazotrophic cyanobacteria and their potential contribution to N2 fixation in the tropical Atlantic Ocean. Environ Microbiol 12(12):3272–3289CrossRefGoogle Scholar
  51. Goering J, Dugdale R, Menzel DW (1966) Estimates of in situ rates of nitrogen uptake by Trichodesmium sp. in the tropical Atlantic Ocean. Limnol Oceanogr 11:614–620. doi: CrossRefGoogle Scholar
  52. Gradoville MR, Bombar D, Crump BC, Letelier RM, Zehr JP, White AE (2017) Diversity and activity of nitrogen-fixing communities across ocean basins. Limnol Oceanogr 62:1895–1909. doi: CrossRefGoogle Scholar
  53. Großkopf T, LaRoche J (2012) Direct and indirect costs of dinitrogen fixation in crocosphaera watsonii WH8501 and possible implications for the nitrogen cycle. Front Microbiol 3:236. doi: CrossRefGoogle Scholar
  54. Gruber N (2004) The dynamics of the marine nitrogen cycle and its influence on atmospheric CO2 variations. In: Follows M, Oguz T (eds) The ocean carbon cycle and climate. Springer, Dordrecht, pp 97–148CrossRefGoogle Scholar
  55. Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451:293–296. doi: CrossRefGoogle Scholar
  56. Gruber N, Sarmiento JL (1997) Global patterns of marine nitrogen fixation and denitrification. Global Biogeochem Cy 11:235–266. doi: CrossRefGoogle Scholar
  57. Hamersley MR, Turk KA, Leinweber A, Gruber N, Zehr JP, Gunderson T, Capone DG (2011) Nitrogen fixation within the water column associated with two hypoxic basins in the Southern California Bight. Aquat Microb Ecol 63:193–205. doi: CrossRefGoogle Scholar
  58. Hansell DA, Bates NR, Olson DB (2004) Excess nitrate and nitrogen fixation in the North Atlantic Ocean. Mar Chem 84(3–4):243–265CrossRefGoogle Scholar
  59. Harding K, Turk-Kubo KA, Sipler RE, Mills MM, Bronk DA, Zehr JP (2018) Symbiotic unicellular cyanobacteria fix nitrogen in the Arctic Ocean. P Natl Acad Sci USA 115(52):13371–13375CrossRefGoogle Scholar
  60. Hardy R, Burns RC, Holsten RD (1973) Applications of the acetylene-ethylene assay for measurement of nitrogen fixation. Soil Biol Biochem 5(1):47–81CrossRefGoogle Scholar
  61. Hardy RW, Holsten RD, Jackson EK, Burns RC (1968) The acetylene-ethylene assay for N2 fixation: Laboratory and field evaluation. Plant Physiol 43(8):1185–1207CrossRefGoogle Scholar
  62. Hewson I, Moisander PH, Achilles KM, Carlson CA, Jenkins BD, Mondragon EA, Morrison AE, Zehr JP (2007) Characteristics of diazotrophs in surface to abyssopelagic waters of the Sargasso Sea. Aquat Microb Ecol 46:15–30. doi: CrossRefGoogle Scholar
  63. Hill S (1978) Factors influencing the efficiency of nitrogen fixation in free-living bacteria. Ecol Bull 26:130–136Google Scholar
  64. Hong H, Shen R, Zhang F, Wen Z, Chang S, Lin W, Kranz SA, Luo Y, Kao S, Morel FMM, Shi D (2017) The complex effects of ocean acidification on the prominent N2-fixing cyanobacterium Trichodesmium. Science 356(6337):527–531CrossRefGoogle Scholar
  65. Hood RR, Coles VJ, Capone DG (2004) Modeling the distribution of Trichodesmium and nitrogen fixation in the Atlantic Ocean. J Geophys Res-Oceans 109(C6):JC001753. doi: CrossRefGoogle Scholar
  66. Hood RR, Subramaniam A, May LR, Carpenter EJ, Capone DG (2001) Remote estimation of nitrogen fixation by Trichodesmium. Deep-Sea Res Pt II 49(1–3):123–147CrossRefGoogle Scholar
  67. Howarth RW (1998) An assessment of human influences on fluxes of nitrogen from the terrestrial landscape to the estuaries and continental shelves of the North Atlantic Ocean. Nutr Cycl Agroecosys 52(2–3):213–223CrossRefGoogle Scholar
  68. Jabir T, Dhanya V, Jesmi Y, Prabhakaran MP, Saravanane N, Gupta GVM, Hatha AAM (2013) Occurrence and distribution of a diatom-diazotrophic cyanobacteria association during a Trichodesmium bloom in the southeastern Arabian Sea. Int J Oceanogr 2013:350594. doi: CrossRefGoogle Scholar
  69. 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(6642):533–538CrossRefGoogle Scholar
  70. Karl D, Michaels A, Bergman B, Capone DG, Carpenter EJ, Letelier R, Lipschultz F, Pearl H, Sigman D, Stal L (2002) Dinitrogen fixation in the world’s oceans. Biogeochemistry 57:47–98. doi: CrossRefGoogle Scholar
  71. Knapp AN, Casciotti KL, Berelson WM, Prokopenko MG, Capone DG (2016) Low rates of nitrogen fixation in eastern tropical South Pacific surface waters. P Natl Acad Sci USA 113:4398–4403. doi: CrossRefGoogle Scholar
  72. Kumar PK, Singh A, Ramesh R, Nallathambi T (2017) N2 fixation in the Eastern Arabian Sea: Probable role of heterotrophic diazotrophs. Front Mar Sci 4:80. doi: CrossRefGoogle Scholar
  73. Landolfi A, Dietze H, Volpe G (2016) Longitudinal variability of organic nutrients in the North Atlantic subtropical gyre. Deep-Sea Res Part I 111:50–60. doi: CrossRefGoogle Scholar
  74. Landolfi A, Kähler P, Koeve W, Oschlies A (2018) Global marine N2 fixation estimates: From observations to models. Front Microbiol 9:2112. doi: CrossRefGoogle Scholar
  75. Langlois RJ, LaRoche J, Raab PA (2005) Diazotrophic diversity and distribution in the tropical and subtropical Atlantic Ocean. Appl Environ Microb 71(12):7910–7919CrossRefGoogle Scholar
  76. Langlois RJ, Hümmer D, LaRoche J (2008) Abundances and distributions of the dominant nifH phylotypes in the Northern Atlantic Ocean. Appl Environ Microb 74(6):1922–1931CrossRefGoogle Scholar
  77. Letelier RM, Karl DM (1996) Role of Trichodesmium spp. in the productivity of the subtropical North Pacific Ocean. Mar Ecol-Progr Ser 133:263–273CrossRefGoogle Scholar
  78. Lipschultz F, Bates NR, Carlson CA, Hansell DA (2002) New production in the Sargasso Sea: History and current status. Global Biogeochem Cy 16(1):GB001319. doi: CrossRefGoogle Scholar
  79. Lipschultz F, Owens NJ (1996) An assessment of nitrogen fixation as a source of nitrogen to the North Atlantic Ocean. Biogeochemistry 35:261–274. doi: CrossRefGoogle Scholar
  80. Löscher CR, Großkopf T, Desai FD, Gill D, Schunck H, Croot PL, Schlosser C, Neulinger SC, Pinnow N, Lavik G, Kuypers MMM, LaRoche J, Schmitz RA (2014) Facets of diazotrophy in the oxygen minimum zone waters off Peru. ISME J 8:2180–2192. doi: CrossRefGoogle Scholar
  81. Löscher CR, Bourbonnais A, Dekaezemacker J, Charoenpong CN, Altabet MA, Bange HW, Czeschel R, Hoffmann C, Schmitz R (2016) N2 fixation in eddies of the eastern tropical South Pacific Ocean. Biogeosciences 13:2889–2899. doi: CrossRefGoogle Scholar
  82. Luo YW, Doney SC, Anderson LA, Benavides M, Berman-Frank I, Bode A (2012) Database of diazotrophs in global ocean: Abundance, biomass and nitrogen fixation rates. Earth Syst Sci Data 4:47–73. doi: CrossRefGoogle Scholar
  83. Meybeck M (1982) Carbon, nitrogen, and phosphorus transport by world rivers. Am J Sci 282(4):401–450CrossRefGoogle Scholar
  84. Michaels AF, Knap AH, Dow RL, Gundersen K, Johnson RJ, Sorensen J, Close A, Knauer GA, Lohrenz SE, Asper VA, Tuel M, Bidigare R (1994) Seasonal patterns of ocean biogeochemistry at the US JGOFS Bermuda Atlantic Time-series Study site. Deep-Sea Res Pt I 41(7):1013–1038CrossRefGoogle Scholar
  85. 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. Biogeochemistry 35:181–226. doi: CrossRefGoogle Scholar
  86. Mohr W, Grosskopf T, Wallace DW, LaRoche J (2010) Methodological underestimation of oceanic nitrogen fixation rates. PLoS One 5(9):e12583. doi: CrossRefGoogle Scholar
  87. Moisander PH, Beinart RA, Hewson I, White AE, Johnson KS, Carlson CA, Montoya JP, Zehr JP (2010) Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain. Science 327(5972):1512–1514CrossRefGoogle Scholar
  88. Moisander PH, Benavides M, Bonnet S, Berman-Frank I, White AE, Riemann L (2017) Chasing after non-cyanobacterial nitrogen fixation in marine pelagic environments. Front Microbiol 8:1736. doi: CrossRefGoogle Scholar
  89. Montoya JP, Holl CM, Zehr JP, Hansen A, Villareal TA, Capone DG (2004) High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 430:1027–1032. doi: CrossRefGoogle Scholar
  90. Montoya JP, Voss M, Kahler P, Capone DG (1996) A simple, high precision, high-sensitivity tracer assay for N2 fixation. Appl Environ Microb 62:986–993Google Scholar
  91. Moore LR, Post AF, Rocap G, Chisholm SW (2002) Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnol Oceanogr 47(4):989–996CrossRefGoogle Scholar
  92. Moore CM, Mills MM, Achterberg EP, Geider RJ, LaRoche J, Lucas MI, McDonagh EL, Pan X, Poulton AJ, Rijkenberg MJA, Suggett DJ, Ussher SJ, Woodward EMS (2009) Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability. Nat Geosci 2:867–871. doi: CrossRefGoogle Scholar
  93. Mouriño-Carballido B, Graña R, Fernández A, Bode A, Varela M, Domínguez JF, Escanez J, de Armas D, Maranon E (2011) Importance of N2 fixation vs. nitrate eddydiffusion along a latitudinal transect in the Atlantic Ocean. Limnol Oceanogr 56:999–1007. doi: CrossRefGoogle Scholar
  94. Mulholland MR, Bernhardt PW (2005) The effect of growth rate, phosphorus concentration, and temperature on N2 fixation, carbon fixation, and nitrogen release in continuous cultures of Trichodesmium IMS101. Limnol Oceanogr 50(3):839–849CrossRefGoogle Scholar
  95. Mulholland MR, Capone DG (2001) Stoichiometry of nitrogen and carbon utilization in cultured populations of Trichodesmium IMS101: Implications for growth. Limnol Oceanogr 46(2):436–443CrossRefGoogle Scholar
  96. Mulholland MR, DA Bronk, Capone DG (2004) N2 fixation and release of NH4 + and dissolved organic nitrogen by Trichodesmium IMS101. Limnol Oceanogr 37:85–94Google Scholar
  97. Mulholland MR, Heil CA, Bronk DA, O’Neil JM (2006) Nitrogen fixation and release of fixed nitrogen by Trichodesmium spp. in the Gulf of Mexico. Limnol Oceanogr 51:1762–1776CrossRefGoogle Scholar
  98. Neess JC, Dugdale RC, Dugdale VA, Goering JJ (1962) Nitrogen metabolism in lakes measurement of nitrogen fixation with 15N. Limnol Oceanog 7(2):163–169CrossRefGoogle Scholar
  99. Orcutt KM, Lipschultz F, Gundersen K, Arimoto R, Michaels AF, Knap AH, Gallon JR (2001) A seasonal study of the significance of N2 fixation by Trichodesmium spp. at the Bermuda Atlantic Time-series Study (BATS) site. Deep-Sea Res Pt II 48:1583–1608. doi: CrossRefGoogle Scholar
  100. Paerl HW, Hall NS, Peierls BL, Rossignol KL (2014) Evolving paradigms and challenges in estuarine and coastal eutrophication dynamics in a culturally and climatically stressed world. Estuar Coast 37(2):243–258CrossRefGoogle Scholar
  101. Palter JB, Lozier MS, Sarmiento JL, Williams RG (2011) The supply of excess phosphate across the Gulf Stream and the maintenance of subtropical nitrogen fixation. Global Biogeochem Cy 25(4):GB003955. doi: CrossRefGoogle Scholar
  102. Postgate J (1998) The origins of the unit of nitrogen fixation at the University of Sussex. Note Rec Roy Soc Lond 52(2):355–362CrossRefGoogle Scholar
  103. Rahav E, Bar-Zeev E, Ohayon S, Elifantz H, Belkin N, Herut B, Mulholland MR, Berman-Frank I (2013) Dinitrogen fixation in aphotic oxygenated marine environments. Front Microbiol 4:227. doi: CrossRefGoogle Scholar
  104. Regnier P, Friedlingstein P, Ciais P, Mackenzie FT, Gruber N, Janssens IA, Laruelle GG, Lauerwald R, Luyssaert S, Andersson AJ, Arndt S, Arnsti C, Borges AV, Dale AW, Gallego-Sala A, Godderis Y, Goossens N, Hartmann J, Heinze C, Ilyina T, Joos F, LaRowe DE, Meysman FJR, Munhoven G, Raymond PA, Spahni R, Suntharalingam P, Thullner M (2013) Anthropogenic perturbation of the carbon fluxes from land to ocean. Nat Geosci 6(8):597–607CrossRefGoogle Scholar
  105. Riebesell U (2004) Effects of CO2 enrichment on marine phytoplankton. J Oceanogr 60(4):719–729CrossRefGoogle Scholar
  106. Saino T, Hattori A (1980) 15N natural abundance in oceanic suspended particulate matter. Nature 283(5749):752–754CrossRefGoogle Scholar
  107. Sañudo-Wilhelmy SA, Kustka AB, Gobler CJ, Hutchins DA, Yang M, Lwiza K, Burns J, Capone DG, Raven JA, Carpenter EJ (2001) Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature 411:66–69. doi: CrossRefGoogle Scholar
  108. Shiozaki T, Bombar D, Riemann L, Hashihama F, Takeda S, Yamaguchi T, Ehama M, Hamasaki K, Furuya K (2017) Basin scale variability of active diazotrophs and nitrogen fixation in the North Pacific, from the tropics to the subarctic Bering Sea. Global Biogeochem Cy 31:996–1009. doi: CrossRefGoogle Scholar
  109. Shiozaki T, Ijichi M, Kodama T, Takeda S, Furuya K (2014a) Heterotrophic bacteria are major nitrogen fixers in the euphotic zone of the Indian Ocean. Global Biogeochem Cy 28:1096–1110. doi: CrossRefGoogle Scholar
  110. Shiozaki T, Kodama T, Furuya K (2014b) Large-scale impact of the island mass effect through nitrogen fixation in the western South Pacific Ocean. Geophys Res Lett 41:2907–2913. doi: CrossRefGoogle Scholar
  111. Shiozaki T, Kodama T, Kitajima S, Sato M, Furuya K (2013) Advective transport of diazotrophs and importance of their nitrogen fixation on new and primary production in the western Pacific warm pool. Limnol Oceanogr 58:49–60. doi: CrossRefGoogle Scholar
  112. Shiozaki T, Nagata T, Ijichi M, Furuya K (2015a) Nitrogen fixation and the diazotroph community in the temperate coastal region of the northwestern North Pacific. Biogeosciences 12:4751–4764. doi: CrossRefGoogle Scholar
  113. Shiozaki T, Takeda S, Itoh S, Kodama T, Liu X, Hashihama F, Furuya K (2015b) Why is Trichodesmium abundant in the Kuroshio? Biogeosciences 12:6931–6943. doi: CrossRefGoogle Scholar
  114. Singh A, Bach LT, Fischer T, Hauss H, Kiko R, Paul AJ, Stange P, Vandromme P, Riebesell U (2017) Niche construction by non-diazotrophs for N2 fixers in the eastern tropical North Atlantic Ocean. Geophys Res Lett 44:6904–6913. doi: CrossRefGoogle Scholar
  115. Singh A, Gandhi N, Ramesh R (2019) Surplus supply of bioavailable nitrogen through N2 fixation to primary producers in the eastern Arabian Sea during autumn. Cont Shelf Res 181:103–110CrossRefGoogle Scholar
  116. Singh A, Lomas M, Bates N (2013) Revisiting N2 fixation in the North Atlantic Ocean: significance of deviations from the Redfield Ratio, atmospheric deposition and climate variability. Deep-Sea Res Pt II 93:148–158. doi: CrossRefGoogle Scholar
  117. Sipler RE, Gong D, Baer SE, Sanderson MP, Roberts QN, Mulholland MR, Bronk DA (2017) Preliminary estimates of the contribution of Arctic nitrogen fixation to the global nitrogen budget. Limnol Oceanogr Lett 2(5):159–166CrossRefGoogle Scholar
  118. Sohm JA, Hilton JA, Noble AE, Zehr JP, Saito MA, Webb EA (2011) Nitrogen fixation in the South Atlantic Gyre and the Benguela Upwelling System. Geophys Res Lett 38:1–6. doi: CrossRefGoogle Scholar
  119. Stewart WD, Fitzgerald GP, Burris N (1967) In situ studies on N2 fixation using the acetylene reduction technique. P Natl Acad Sci USA 58(5):2071–2078CrossRefGoogle Scholar
  120. Stewart WD, Fitzgerald GP, Burris RH (1968) Acetylene reduction by nitrogen-fixing blue-green algae. Arch Mikrobiol 62(4):336–348CrossRefGoogle Scholar
  121. Subramaniam A, Carpenter EJ, Falkowski PG (1999) Bio-optical properties of the marine diazotrophic cyanobacteria Trichodesmium spp. II. A reflectance model for remote sensing. Limnol Oceanogr 44(3):618–627CrossRefGoogle Scholar
  122. Subramaniam A, Mahaffey C, Johns W, Mahowald N (2013) Equatorial upwelling enhances nitrogen fixation in the Atlantic Ocean. Geophys Res Lett 40:1766–1771. doi: CrossRefGoogle Scholar
  123. Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G, Djahanschiri B, Zeller G, Mende DR, Alberti A, Cornejo-Castillo FM, Costea PI, Cruaud C, dOvidio F, Engelen S, Ferrera I, Gasol JM, Guidi L, Hildebrand F, Kokoszka F, Lepoivre C, Lima-Mendez G, Poulain J, Poulos BT, Royo-Lionch M, Sarmento H, Vieira-Silva S, Dimier C, Picheral M, Searson S, Kandels-Lewis S, Coodinators TO, Bowler C, de Vargas C, Gorsky G, Grimsley N, Hingamp P, Iudicone D, Jaillon O, Not F, Ogata H, Pesant S, Speich S, Stemmann L, Sullivan MB, Weissenhach J, Winker P, Karsenti E, Raes J, Acinas SG, Bork P (2015) Structure and function of the global ocean microbiome. Science 348(6237):1261359. doi: CrossRefGoogle Scholar
  124. Thomas MK, Kremer CT, Klausmeier CA, and Litchman E (2012) A global pattern of thermal adaptation in marine phytoplankton. Science 338(6110):1085–1088CrossRefGoogle Scholar
  125. Thompson A, Carter BJ, Turk-Kubo K, Malfatti F, Azam F, Zehr JP (2014) Ge ost. Environ Microbiol 16(10):3238–3249CrossRefGoogle Scholar
  126. Thompson AW, Foster RA, Krupke A, Carter BJ, Musat N, Vaulot D, Kuyper MMM, Zehr JP (2012) Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337(6101):1546–1550CrossRefGoogle Scholar
  127. Turk KA, Rees AP, Zehr JP, Pereira N, Swift P, Shelley R. Lohan M, Woodward EMS, Gilbert J (2011) Nitrogen fixation and nitrogenase (nifH) expression in tropical waters of the eastern North Atlantic. ISME J 5(7):1201–1212CrossRefGoogle Scholar
  128. Turk-Kubo KA, Achilles KM, Serros TR, Ochiai M, Montoya JP, Zehr JP (2012) Nitrogenase (nifH) gene expression in diazotrophic cyanobacteria in the Tropical North Atlantic in response to nutrient amendments. Front Microbiol 3:386. doi: CrossRefGoogle Scholar
  129. Turk-Kubo KA, Connell PE, Caron DA, Hogan ME, Farnelid HM, Zehr JP (2018) In situ diazotroph population dynamics under different resource ratios in the North Pacific Subtropical Gyre. Front Microbiol 9:1616. doi: CrossRefGoogle Scholar
  130. Turk-Kubo KA, Farnelid HM, Shilova IN, Henke B, Zehr JP (2017) Distinct ecological niches of marine symbiotic N2-fixing cyanobacterium Candidatus Atelocyanobacterium thalassa sublineages. J Phycol 53(2):451–461CrossRefGoogle Scholar
  131. Turk-Kubo KA, Karamchandani M, Capone DG, Zehr JP (2014) The paradox of marine heterotrophic nitrogen fixation: abundances of heterotrophic diazotrophs do not account for nitrogen fixation rates in the Eastern Tropical South Pacific. Environ Microbiol 16:3095–3114. doi: CrossRefGoogle Scholar
  132. Villareal TA (1992) Marine nitrogen-fixing diatom-cyanobacteria symbioses. In: Carpenter EJ, Capone DG, Rueter JG (eds) Marine pelagic cyanobacteria: Trichodesmium and other diazotrophs. Springer, Dordrecht, pp 163–175CrossRefGoogle Scholar
  133. Wada E, Hattori A (1976) Natural abundance of 15N in particulate organic matter in the North Pacific Ocean. Geochim Cosmochim Ac 40(2):249–251CrossRefGoogle Scholar
  134. Westberry TK, Siegel DA, Subramaniam A (2005) An improved bio-optical model for the remote sensing of Trichodesmium spp. blooms. J Geophys Res-Oceans 110(C6):JC002517. doi: CrossRefGoogle Scholar
  135. Zehr JP (2011) Nitrogen fixation by marine cyanobacteria. Trends Microbiol 19:162–173. doi: CrossRefGoogle Scholar
  136. Zehr JP, Carpenter EJ, Villareal TA (2000) New perspectives on nitrogen fixing microrganisms in tropical and subtropical oceans. Trends Microbiol 8:68–73. doi: CrossRefGoogle Scholar
  137. Zehr JP, Mellon MT, Zani S (1998) New nitrogen-fixing microorganisms detected in oligotrophic oceans by amplification of nitrogenase (nifH) genes. Appl Environ Microb 64:3444–3450Google Scholar
  138. Zehr JP, Paerl HW (2008) Molecular ecological aspects of nitrogen fixation in the marine environment. In: Kirchman DL (ed) Microbial ecology of the oceans. John Wiley & Sons, New Jersey, pp 481–523CrossRefGoogle Scholar

Copyright information

© Korea Institute of Ocean Science & Technology (KIOST) and the Korean Society of Oceanography (KSO) and Springer Science+Business Media B.V. 2019

Authors and Affiliations

  • P. S. Bhavya
    • 1
  • Jun-Oh Min
    • 2
  • Min-Seob Kim
    • 3
  • Hyo Keun Jang
    • 1
  • Kwanwoo Kim
    • 1
  • Jae Joong Kang
    • 1
  • Jae Hyung Lee
    • 1
  • Dabin Lee
    • 1
  • Naeun Jo
    • 1
  • Myung Joon Kim
    • 1
  • Yejin Kim
    • 1
  • Junbeom Lee
    • 1
  • Chang Hwa Lee
    • 1
  • Hyeonji Bae
    • 1
  • Hyeju Yoo
    • 1
  • Sanghoon Park
    • 1
  • Mi Sun Yun
    • 4
  • Sang Heon Lee
    • 1
    Email author
  1. 1.Department of Oceanography, College of Natural SciencesPusan National UniversityBusanKorea
  2. 2.Department of Marine Science and Convergence EngineeringHanyang UniversityAnsanKorea
  3. 3.Fundamental Environment Research Department, Environmental Measurement & Analysis CenterNational Institute of Environmental ResearchIncheonKorea
  4. 4.College of Marine and Environmental SciencesTianjin University of Science and TechnologyTianjinChina

Personalised recommendations