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

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Abstract

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.

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References

  • 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 191:74–83

    Google Scholar 

  • Altabet MA (2007) Constraints on oceanic N balance/imbalance from sedimentary 15N records. Biogeosciences 4:75–86. doi:https://doi.org/10.5194/bg-4-75-2007

    Google Scholar 

  • 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 182–206

    Google Scholar 

  • 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):1052–1071

    Google Scholar 

  • Bauer JE, Cai WJ, Raymond PA, Bianchi TS, Hopkinson CS, Regnier PA (2013) The changing carbon cycle of the coastal ocean. Nature 504(7478):61–70

    Google Scholar 

  • 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):43–53

    Google Scholar 

  • Benavides M, Bonnet S, Berman-Frank I, Riemann L (2018) Deep into oceanic N2 fixation. Front Mar Sci 5:108. doi:https://doi.org/10.3389/fmars.2018.00108

    Google Scholar 

  • Benavides M, Voss M (2015) Five decades of N2 fixation research in the North Atlantic Ocean. Front Mar Sci 2:40. doi:https://doi.org/10.3389/fmars.2015.00040

    Google Scholar 

  • 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:https://doi.org/10.1371/journal.pone.0143775

    Google Scholar 

  • 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:https://doi.org/10.1038/ismej.2014.119

    Google Scholar 

  • 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):286–302

    Google Scholar 

  • 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:https://doi.org/10.1002/2017GL073856

    Google Scholar 

  • 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:https://doi.org/10.1007/s12237-015-9982-y

    Google Scholar 

  • 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):447–456

    Google Scholar 

  • Bombar D, Paerl RW, Riemann L (2016) Marine non-cyanobacterial diazotrophs: Moving beyond molecular detection. Trends Microbiol 24:916–927. doi:https://doi.org/10.1016/j.tim.2016.07.002

    Google Scholar 

  • 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:https://doi.org/10.3389/fmars.2018.00006

    Google Scholar 

  • 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:https://doi.org/10.1029/2008GB003439

    Google Scholar 

  • 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:https://doi.org/10.1371/journal.pone.0081265

    Google Scholar 

  • 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:https://doi.org/10.5194/bg-15-4215-2018

    Google Scholar 

  • 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:https://doi.org/10.1073/pnas.1619514114

    Google Scholar 

  • 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:https://doi.org/10.1002/2015GB005117

    Google Scholar 

  • 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):200–216

    Google Scholar 

  • 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 359:25–36

    Google Scholar 

  • 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:https://doi.org/10.1029/2004GB002331

    Google Scholar 

  • Capone DG, Carpenter EJ (1982) Nitrogen fixation in the marine environment. Science 217:1140–1142. doi:https://doi.org/10.1126/science.217.4565.1140

    Google Scholar 

  • 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:https://doi.org/10.3354/meps172281

    Google Scholar 

  • Capone DG, Zehr JP, Paerl HW, Bergman B, Carpenter EJ (1997) Trichodesmium, a globally significant marine Cyanobacterium. Science 276:1221–1229. doi:https://doi.org/10.1126/science.276.5316.1221

    Google Scholar 

  • 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:https://doi.org/10.4319/lo.1977.22.1.0060

    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. doi:https://doi.org/10.1126/science.254.5036.1356

    Google Scholar 

  • 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:https://doi.org/10.1038/s41467-017-02342-1

    Google Scholar 

  • 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:https://doi.org/10.4319/10.2008.53.5.1705

    Google Scholar 

  • 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):63–77

    Google Scholar 

  • 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):3–14

    Google Scholar 

  • 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:https://doi.org/10.1029/2008gb003418

    Google Scholar 

  • Coles VJ, Wilson C, Hood RR (2004) Remote sensing of new production fueled by nitrogen fixation. Geophys Res Lett 31(6):GL019018. doi:https://doi.org/10.1029/2003GL019018

    Google Scholar 

  • 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:https://doi.org/10.1371/journal.pone.0110335

    Google Scholar 

  • 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:https://doi.org/10.1002/gbc.20063

    Google Scholar 

  • Deutsch C, Sarmiento JL, Sigman DM, Gruber N, Dunne JP (2007) Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445:163–167

    Google Scholar 

  • Doney SC (2010) The growing human footprint on coastal and open-ocean biogeochemistry. Science 328:1512–1516

    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, Goering JJ, Ryther JH (1964) High nitrogen fixation rates in the Sargasso sea and the arabian sea. Limnol Oceanogr 9(4):507–510

    Google Scholar 

  • 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:https://doi.org/10.1128/AEM.70.2.765-770.2004

    Google Scholar 

  • 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:https://doi.org/10.1371/journal.pone.0019223

    Google Scholar 

  • 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):125–138

    Google Scholar 

  • 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):149–174

    Google Scholar 

  • 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:https://doi.org/10.5194/bg-7-3167-2010

    Google Scholar 

  • Flett RJ, Hamilton RD, Campbell NER (1976) Aquatic acetylene-reduction techniques: Solutions to several problems. Can J Microbiol 22(1):43–51

    Google Scholar 

  • 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:https://doi.org/10.1029/2010GB003970

    Google Scholar 

  • 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):459–463

    Google Scholar 

  • 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):3272–3289

    Google Scholar 

  • 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:https://doi.org/10.4319/10.1966.11.4.0614

    Google Scholar 

  • 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:https://doi.org/10.1002/lno.10542

    Google Scholar 

  • 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:https://doi.org/10.3389/fmicb.2012.00236

    Google Scholar 

  • 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 97–148

    Google Scholar 

  • Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451:293–296. doi:https://doi.org/10.1038/nature06592

    Google Scholar 

  • Gruber N, Sarmiento JL (1997) Global patterns of marine nitrogen fixation and denitrification. Global Biogeochem Cy 11:235–266. doi:https://doi.org/10.1029/97GB00077

    Google Scholar 

  • 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:https://doi.org/10.3354/ame01494

    Google Scholar 

  • Hansell DA, Bates NR, Olson DB (2004) Excess nitrate and nitrogen fixation in the North Atlantic Ocean. Mar Chem 84(3–4):243–265

    Google Scholar 

  • 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):13371–13375

    Google Scholar 

  • Hardy R, Burns RC, Holsten RD (1973) Applications of the acetylene-ethylene assay for measurement of nitrogen fixation. Soil Biol Biochem 5(1):47–81

    Google Scholar 

  • Hardy RW, Holsten RD, Jackson EK, Burns RC (1968) The acetylene-ethylene assay for N2 fixation: Laboratory and field evaluation. Plant Physiol 43(8):1185–1207

    Google Scholar 

  • 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:https://doi.org/10.3354/ame046015

    Google Scholar 

  • Hill S (1978) Factors influencing the efficiency of nitrogen fixation in free-living bacteria. Ecol Bull 26:130–136

    Google Scholar 

  • 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):527–531

    Google Scholar 

  • 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:https://doi.org/10.1029/2002JC001753

    Google Scholar 

  • 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):123–147

    Google Scholar 

  • 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):213–223

    Google Scholar 

  • 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:https://doi.org/10.1155/2013/350594

    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. Nature 388(6642):533–538

    Google Scholar 

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

    Google Scholar 

  • 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:https://doi.org/10.1073/pnas.1515641113

    Google Scholar 

  • 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:https://doi.org/10.3389/fmars.2017.00080

    Google Scholar 

  • 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:https://doi.org/10.1016/j.dsr.2015.11.009

    Google Scholar 

  • Landolfi A, Kähler P, Koeve W, Oschlies A (2018) Global marine N2 fixation estimates: From observations to models. Front Microbiol 9:2112. doi:https://doi.org/10.3389/fmicb.2018.02112

    Google Scholar 

  • Langlois RJ, LaRoche J, Raab PA (2005) Diazotrophic diversity and distribution in the tropical and subtropical Atlantic Ocean. Appl Environ Microb 71(12):7910–7919

    Google Scholar 

  • 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):1922–1931

    Google Scholar 

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

    Google Scholar 

  • 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:https://doi.org/10.1029/2000GB001319

    Google Scholar 

  • 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:https://doi.org/10.1007/BF02179830

    Google Scholar 

  • 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:https://doi.org/10.1038/ismej.2014.71

    Google Scholar 

  • 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:https://doi.org/10.5194/bg-13-2889-2016

    Google Scholar 

  • 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:https://doi.org/10.5194/essd-4-47-2012

    Google Scholar 

  • Meybeck M (1982) Carbon, nitrogen, and phosphorus transport by world rivers. Am J Sci 282(4):401–450

    Google Scholar 

  • 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):1013–1038

    Google Scholar 

  • 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:https://doi.org/10.1007/BF02179827

    Google Scholar 

  • Mohr W, Grosskopf T, Wallace DW, LaRoche J (2010) Methodological underestimation of oceanic nitrogen fixation rates. PLoS One 5(9):e12583. doi:https://doi.org/10.1371/journal.pone.0012583

    Google Scholar 

  • 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):1512–1514

    Google Scholar 

  • 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:https://doi.org/10.3389/fmicb.2017.01736

    Google Scholar 

  • 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:https://doi.org/10.1038/nature02824

    Google Scholar 

  • Montoya JP, Voss M, Kahler P, Capone DG (1996) A simple, high precision, high-sensitivity tracer assay for N2 fixation. Appl Environ Microb 62:986–993

    Google Scholar 

  • 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):989–996

    Google Scholar 

  • 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:https://doi.org/10.1038/ngeo667

    Google Scholar 

  • 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:https://doi.org/10.4319/lo.2011.56.3.0999

    Google Scholar 

  • 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):839–849

    Google Scholar 

  • Mulholland MR, Capone DG (2001) Stoichiometry of nitrogen and carbon utilization in cultured populations of Trichodesmium IMS101: Implications for growth. Limnol Oceanogr 46(2):436–443

    Google Scholar 

  • Mulholland MR, DA Bronk, Capone DG (2004) N2 fixation and release of NH4 + and dissolved organic nitrogen by Trichodesmium IMS101. Limnol Oceanogr 37:85–94

    Google Scholar 

  • 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 51:1762–1776

    Google Scholar 

  • Neess JC, Dugdale RC, Dugdale VA, Goering JJ (1962) Nitrogen metabolism in lakes measurement of nitrogen fixation with 15N. Limnol Oceanog 7(2):163–169

    Google Scholar 

  • 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:https://doi.org/10.1016/S0967-0645(00)00157-0

    Google Scholar 

  • 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):243–258

    Google Scholar 

  • 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:https://doi.org/10.1029/2010GB003955

    Google Scholar 

  • Postgate J (1998) The origins of the unit of nitrogen fixation at the University of Sussex. Note Rec Roy Soc Lond 52(2):355–362

    Google Scholar 

  • 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:https://doi.org/10.3389/fmicb.2013.00227

    Google Scholar 

  • 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):597–607

    Google Scholar 

  • Riebesell U (2004) Effects of CO2 enrichment on marine phytoplankton. J Oceanogr 60(4):719–729

    Google Scholar 

  • Saino T, Hattori A (1980) 15N natural abundance in oceanic suspended particulate matter. Nature 283(5749):752–754

    Google Scholar 

  • 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:https://doi.org/10.1038/35075041

    Google Scholar 

  • 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:https://doi.org/10.1002/2017GB005681

    Google Scholar 

  • 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:https://doi.org/10.1002/2014GB004886

    Google Scholar 

  • 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:https://doi.org/10.1002/2014GL059835

    Google Scholar 

  • 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:https://doi.org/10.4319/lo.2013.58.1.0049

    Google Scholar 

  • 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:https://doi.org/10.5194/bg-12-4751-2015

    Google Scholar 

  • 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:https://doi.org/10.5194/bg-12-6931-2015

    Google Scholar 

  • 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:https://doi.org/10.1002/2017GL074218

    Google Scholar 

  • 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 181:103–110

    Google Scholar 

  • 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:https://doi.org/10.1016/j.dsr2.2013.04.008

    Google Scholar 

  • 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):159–166

    Google Scholar 

  • 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:https://doi.org/10.1029/2011GL048315

    Google Scholar 

  • 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):2071–2078

    Google Scholar 

  • Stewart WD, Fitzgerald GP, Burris RH (1968) Acetylene reduction by nitrogen-fixing blue-green algae. Arch Mikrobiol 62(4):336–348

    Google Scholar 

  • 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):618–627

    Google Scholar 

  • 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:https://doi.org/10.1002/grl.50250

    Google Scholar 

  • 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:https://doi.org/10.1126/science.1261359

    Google Scholar 

  • Thomas MK, Kremer CT, Klausmeier CA, and Litchman E (2012) A global pattern of thermal adaptation in marine phytoplankton. Science 338(6110):1085–1088

    Google Scholar 

  • Thompson A, Carter BJ, Turk-Kubo K, Malfatti F, Azam F, Zehr JP (2014) Ge ost. Environ Microbiol 16(10):3238–3249

    Google Scholar 

  • 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):1546–1550

    Google Scholar 

  • 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):1201–1212

    Google Scholar 

  • 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:https://doi.org/10.3389/fmicb.2012.00386

    Google Scholar 

  • 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:https://doi.org/10.3389/fmicb.2018.01616

    Google Scholar 

  • 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):451–461

    Google Scholar 

  • 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:https://doi.org/10.1111/1462-2920.12346

    Google Scholar 

  • 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 163–175

    Google Scholar 

  • Wada E, Hattori A (1976) Natural abundance of 15N in particulate organic matter in the North Pacific Ocean. Geochim Cosmochim Ac 40(2):249–251

    Google Scholar 

  • 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:https://doi.org/10.1029/2004JC002517

    Google Scholar 

  • Zehr JP (2011) Nitrogen fixation by marine cyanobacteria. Trends Microbiol 19:162–173. doi:https://doi.org/10.1016/j.tim.2010.12.004

    Google Scholar 

  • Zehr JP, Carpenter EJ, Villareal TA (2000) New perspectives on nitrogen fixing microrganisms in tropical and subtropical oceans. Trends Microbiol 8:68–73. doi:https://doi.org/10.1016/S0966-842X(99)01670-4

    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 Microb 64:3444–3450

    Google Scholar 

  • 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 481–523

    Google Scholar 

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Acknowledgements

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).

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Bhavya, P.S., Min, JO., Kim, MS. et al. A Review on Marine N2 Fixation: Mechanism, Evolution of Methodologies, Rates, and Future Concerns. Ocean Sci. J. 54, 515–528 (2019). https://doi.org/10.1007/s12601-019-0037-3

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