Modelling N2 fixation related to Trichodesmium sp.: driving processes and impacts on primary production in the tropical Pacific Ocean

Abstract. Dinitrogen fixation is now recognized as one of the major sources of bio-available nitrogen in the ocean. Thus, N2 fixation sustains a significant part of the global primary production by supplying the most common limiting nutrient for phytoplankton growth. The “Oligotrophy to UlTra-oligotrophy PACific Experiment” (OUTPACE) improved the data coverage of the western tropical South Pacific, an area recently recognized as a hotspot of N2 fixation. This new development leads us to develop and test an explicit N2 fixation formulation based on the Trichodesmium physiology (the most studied nitrogen fixer) within a 3-D coupled dynamical–biogeochemical model (ROMS-PISCES). We performed a climatological numerical simulation that is able to reproduce the main physical (e.g. sea surface temperature) and biogeochemical patterns (nutrient and chlorophyll concentrations, as well as N2 fixation) in the tropical Pacific. This simulation displayed a Trichodesmium regional distribution that extends from 150∘ E to 120∘ W in the south tropical Pacific, and from 120∘ E to 140∘ W in the north tropical Pacific. The local simulated maximuma were found around islands (Hawaii, Fiji, Samoa, New Caledonia, Vanuatu). We assessed that 15 % of the total primary production may be due to Trichodesmium in the low-nutrient low-chlorophyll regions (LNLC) of the tropical Pacific. Comparison between our explicit and the often used (in biogeochemical models) implicit parameterization of N2 fixation showed that the latter leads to an underestimation of N2 fixation rates by about 25 % in LNLC regions. Finally, we established that iron fluxes from island sediments control the spatial distribution of Trichodesmium biomasses in the western tropical South Pacific. Note, this last result does not take into account the iron supply from rivers and hydrothermal sources, which may well be of importance in a region known for its strong precipitation rates and volcanic activity.

[1]  S. Bonnet,et al.  In-depth characterization of diazotroph activity across the western tropical South Pacific hotspot of N2 fixation (OUTPACE cruise) , 2018, Biogeosciences.

[2]  Iron from a submarine source impacts the productive layer of the Western Tropical South Pacific (WTSP) , 2018, Scientific Reports.

[3]  Tom O. Delmont,et al.  Nitrogen-fixing populations of Planctomycetes and Proteobacteria are abundant in surface ocean metagenomes , 2018, Nature Microbiology.

[4]  A. Doglioli,et al.  N 2 fixation as a dominant new N source in the western tropical South Pacific Ocean (OUTPACE cruise) , 2018 .

[5]  P. Ciais,et al.  The Impact of Variable Phytoplankton Stoichiometry on Projections of Primary Production, Food Quality, and Carbon Uptake in the Global Ocean , 2018 .

[6]  A. White,et al.  Chasing after Non-cyanobacterial Nitrogen Fixation in Marine Pelagic Environments , 2017, Front. Microbiol..

[7]  H. Berthelot,et al.  High‐nitrogen fixation rates in the particulate and dissolved pools in the Western Tropical Pacific (Solomon and Bismarck Seas) , 2017 .

[8]  S. Bonnet,et al.  Hot spot of N2 fixation in the western tropical South Pacific pleads for a spatial decoupling between N2 fixation and denitrification , 2017, Proceedings of the National Academy of Sciences.

[9]  S. Bonnet,et al.  Distribution and drivers of symbiotic and free-living diazotrophic cyanobacteria in the western tropical South Pacific , 2017 .

[10]  L. Riemann,et al.  Marine Non-Cyanobacterial Diazotrophs: Moving beyond Molecular Detection. , 2016, Trends in microbiology.

[11]  I. Berman‐Frank,et al.  Diazotroph derived nitrogen supports diatom growth in the South West Pacific: A quantitative study using nanoSIMS , 2016 .

[12]  S. Bonnet,et al.  Transfer of diazotroph-derived nitrogen towards non-diazotrophic planktonic communities: a comparative study between Trichodesmium erythraeum, Crocosphaera watsonii and Cyanothece sp. , 2016 .

[13]  Samuel T. Wilson,et al.  Temporal variability of nitrogen fixation and particulate nitrogen export at Station ALOHA , 2016 .

[14]  I. Berman‐Frank,et al.  Dynamics of N 2 fixation and fate of diazotroph-derived nitrogen in a low-nutrient, low-chlorophyll ecosystem: results from the VAHINE mesocosm experiment (New Caledonia) , 2015 .

[15]  P. Raimbault,et al.  Contrasted geographical distribution of N2 fixation rates and nifH phylotypes in the Coral and Solomon Seas (southwestern Pacific) during austral winter conditions , 2015 .

[16]  S. Bonnet,et al.  Assessment of the dinitrogen released as ammonium and dissolved organic nitrogen by unicellular and filamentous marine diazotrophic cyanobacteria grown in culture , 2015, Front. Mar. Sci..

[17]  Olivier Aumont,et al.  PISCES-v2: an ocean biogeochemical model for carbon and ecosystem studies , 2015 .

[18]  K. Furuya,et al.  Nitrogen fixation and the diazotroph community in the temperate coastal region of the northwestern North Pacific , 2015 .

[19]  J. Zehr,et al.  Marine Nitrogen Fixation: Organisms, Significance, Enigmas, and Future Directions , 2015 .

[20]  S. Bonnet,et al.  Dinitrogen fixation and dissolved organic nitrogen fueled primary production and particulate export during the VAHINE mesocosm experiment (New Caledonia lagoon) , 2015 .

[21]  D. Capone,et al.  The paradox of marine heterotrophic nitrogen fixation: abundances of heterotrophic diazotrophs do not account for nitrogen fixation rates in the Eastern Tropical South Pacific. , 2014, Environmental microbiology.

[22]  M. Boersma,et al.  A New Approach to Homeostatic Regulation: Towards a Unified View of Physiological and Ecological Concepts , 2014, PloS one.

[23]  K. Furuya,et al.  Large‐scale impact of the island mass effect through nitrogen fixation in the western South Pacific Ocean , 2014 .

[24]  Timothy M Lenton,et al.  Multiple environmental controls on phytoplankton growth strategies determine adaptive responses of the N : P ratio. , 2014, Ecology letters.

[25]  M. Lengaigne,et al.  Ocean feedback to tropical cyclones: climatology and processes , 2014, Climate Dynamics.

[26]  K. Arrigo,et al.  Processes and patterns of oceanic nutrient limitation , 2013 .

[27]  S. Doney,et al.  Data-based assessment of environmental controls on global marine nitrogen fixation , 2013 .

[28]  K. Furuya,et al.  Advective transport of diazotrophs and importance of their nitrogen fixation on new and primary production in the western Pacific warm pool , 2013 .

[29]  E. Carpenter,et al.  Trichodesmium – a widespread marine cyanobacterium with unusual nitrogen fixation properties , 2012, FEMS microbiology reviews.

[30]  Krista,et al.  GFDL’s ESM2 Global Coupled Climate–Carbon Earth System Models. Part II: Carbon System Formulation and Baseline Simulation Characteristics* , 2013 .

[31]  M. Lengaigne,et al.  Impact of Tropical Cyclones on the Heat Budget of the South Pacific Ocean , 2012 .

[32]  L. A. Anderson,et al.  Database of diazotrophs in global ocean: abundance, biomass and nitrogen fixation rates , 2012 .

[33]  R. Schmitz,et al.  Doubling of marine dinitrogen-fixation rates based on direct measurements , 2012, Nature.

[34]  Ronald,et al.  GFDL’s ESM2 Global Coupled Climate–Carbon Earth System Models. Part I: Physical Formulation and Baseline Simulation Characteristics , 2012 .

[35]  Stephanie Dutkiewicz,et al.  Interconnection of nitrogen fixers and iron in the Pacific Ocean: Theory and numerical simulations , 2012 .

[36]  D. Wolf-Gladrow,et al.  Environmental controls on N2 fixation by Trichodesmium in the tropical eastern North Atlantic Ocean - A model-based study , 2012 .

[37]  T. Ferdelman,et al.  Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre , 2011, The ISME Journal.

[38]  T. Westberry,et al.  An algorithm for detecting Trichodesmium surface blooms in the South Western Tropical Pacific , 2011 .

[39]  O. Aumont,et al.  A global compilation of dissolved iron measurements: focus on distributions and processes in the Southern Ocean , 2011 .

[40]  I. Berman‐Frank,et al.  Dust- and mineral-iron utilization by the marine dinitrogen-fixer Trichodesmium , 2011 .

[41]  M. Follows,et al.  Biogeographical controls on the marine nitrogen fixers , 2011 .

[42]  F. Lacan,et al.  Iron isotopes in the seawater of the equatorial Pacific Ocean: New constraints for the oceanic iron cycle , 2011 .

[43]  J. LaRoche,et al.  Methodological Underestimation of Oceanic Nitrogen Fixation Rates , 2010, PloS one.

[44]  Angelicque E. White,et al.  Unicellular Cyanobacterial Distributions Broaden the Oceanic N2 Fixation Domain , 2010, Science.

[45]  M. Gehlen,et al.  Hydrothermal contribution to the oceanic dissolved iron inventory , 2010 .

[46]  P. Marchesiello,et al.  Coastal upwelling, circulation and heat balance around New Caledonia's barrier reef. , 2010, Marine pollution bulletin.

[47]  S. Bonnet,et al.  Nitrogen fixation in the western equatorial Pacific: Rates, diazotrophic cyanobacterial size class distribution, and biogeochemical significance , 2009 .

[48]  K. Lindsay,et al.  Impacts of increasing anthropogenic soluble iron and nitrogen deposition on ocean biogeochemistry , 2009 .

[49]  Christoph Heinze,et al.  An isopycnic ocean carbon cycle model , 2009 .

[50]  B. Toner.  Preservation of iron(II) by carbon-rich matrices in a hydrothermal plume , 2009 .

[51]  Andreas Oschlies,et al.  Chain model of phytoplankton P, N and light colimitation , 2009 .

[52]  L. Gourdeau,et al.  Barotropic Zonal Jets Induced by Islands in the Southwest Pacific , 2008 .

[53]  Nicole L. Goebel,et al.  GROWTH AND CARBON CONTENT OF THREE DIFFERENT‐SIZED DIAZOTROPHIC CYANOBACTERIA OBSERVED IN THE SUBTROPICAL NORTH PACIFIC 1 , 2008, Journal of phycology.

[54]  I. Berman‐Frank,et al.  Iron limitation in the marine cyanobacterium Trichodesmium reveals new insights into regulation of photosynthesis and nitrogen fixation. , 2008, The New phytologist.

[55]  R. Beinart,et al.  Diversity and abundance of diazotrophic microorganisms in the South China Sea during intermonsoon , 2008, The ISME Journal.

[56]  J. LaRoche,et al.  Nitrogen fixation and growth rates of Trichodesmium IMS-101 as a function of light intensity , 2008 .

[57]  Kenneth L. Denman,et al.  Preindustrial, historical, and fertilization simulations using a global ocean carbon model with new parameterizations of iron limitation, calcification, and N2 fixation , 2008 .

[58]  N. Garcia,et al.  Evidence for efficient regenerated production and dinitrogen fixation in nitrogen-deficient waters of the South Pacific Ocean: impact on new and export production estimates , 2008 .

[59]  Nicolas Gruber,et al.  The Marine Nitrogen Cycle: Overview and Challenges , 2008 .

[60]  C. German,et al.  The distribution and stabilisation of dissolved Fe in deep-sea hydrothermal plumes , 2007 .

[61]  P. Raimbault,et al.  Seasonal nitrogen fixation and primary production in the Southwest Pacific: nanoplankton diazotrophy and transfer of nitrogen to picoplankton organisms , 2007 .

[62]  Olivier Aumont,et al.  Ocean biogeochemistry exhibits contrasting responses to a large scale reduction in dust deposition , 2007 .

[63]  P. Raimbault,et al.  Phosphate availability and the ultimate control of new nitrogen input by nitrogen fixation in the tropical Pacific Ocean , 2007 .

[64]  W. Kessler,et al.  The Annual Cycle of Circulation of the Southwest Subtropical Pacific, Analyzed in an Ocean GCM* , 2007 .

[65]  Nicolas Gruber,et al.  Spatial coupling of nitrogen inputs and losses in the ocean , 2007, Nature.

[66]  G. Madec,et al.  Progress in the 3-D circulation of the eastern equatorial Pacific in a climate ocean model , 2007 .

[67]  Ricardo M Letelier,et al.  Modeling carbohydrate ballasting by Trichodesmium spp. , 2006 .

[68]  Cécile Dupouy,et al.  Spectral diversity of phycoerythrins and diazotroph abundance in tropical waters , 2006 .

[69]  Andreas Oschlies,et al.  Nitrogen Fixation and Temperature Physiological Constraints on the Global Distribution of Trichodesmium – Effect of Temperature on Diazotrophy Nitrogen Fixation and Temperature , 2022 .

[70]  L. Bopp,et al.  Globalizing results from ocean in situ iron fertilization studies , 2006 .

[71]  J. Gallon.  Reconciling the incompatible: N2 fixation And O2 , 2006 .

[72]  K. Lindsay,et al.  Nitrogen fixation amplifies the ocean biogeochemical response to decadal timescale variations in mineral dust deposition , 2006 .

[73]  J. McWilliams,et al.  Evaluation and application of the ROMS 1-way embedding procedure to the central california upwelling system , 2006 .

[74]  N. Gruber.  Oceanography: A bigger nitrogen fix , 2005, Nature.

[75]  Cécile Dupouy,et al.  Phosphate availability controls Trichodesmium spp. biomass in the SW Pacific Ocean , 2005 .

[76]  D. Karl,et al.  Vertical distributions of nitrogen-fixing phylotypes at Stn ALOHA in the oligotrophic North Pacific Ocean , 2005 .

[77]  E. Carpenter,et al.  Growth kinetics of marine unicellular N2-fixing cyanobacterial isolates in continuous culture in relation to phosphorus and temperature , 2005 .

[78]  Joachim Segschneider,et al.  The HAMburg Ocean Carbon Cycle Model HAMOCC5.1 - Technical Description Release 1.1 , 2005 .

[79]  Julie LaRoche,et al.  Importance of the diazotrophs as a source of new nitrogen in the ocean , 2005 .

[80]  Alexander F. Shchepetkin,et al.  The regional oceanic modeling system (ROMS): a split-explicit, free-surface, topography-following-coordinate oceanic model , 2005 .

[81]  K. Arrigo.  Marine microorganisms and global nutrient cycles , 2005, Nature.

[82]  Keith Lindsay,et al.  Upper ocean ecosystem dynamics and iron cycling in a global three‐dimensional model , 2004 .

[83]  G. Asner,et al.  Nitrogen Cycles: Past, Present, and Future , 2004 .

[84]  J. Montoya,et al.  High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean , 2004, Nature.

[85]  Matthew M. Mills,et al.  Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic , 2004, Nature.

[86]  S. Levin,et al.  Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton , 2004, Nature.

[87]  M. Roman,et al.  Toxicity of blooms of the cyanobacterium Trichodesmium to zooplankton , 1992, Journal of Applied Phycology.

[88]  Randall F. Miller,et al.  The oldest articulated chondrichthyan from the Early Devonian period , 2003, Nature.

[89]  L. Stal,et al.  Temperature excludes N2-fixing heterocystous cyanobacteria in the tropical oceans , 2003, Nature.

[90]  E. Carpenter,et al.  Iron requirements for dinitrogen‐ and ammonium‐supported growth in cultures of Trichodesmium (IMS 101): Comparison with nitrogen fixation rates and iron: carbon ratios of field populations , 2003 .

[91]  J. Elser,et al.  Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere , 2002 .

[92]  E. Carpenter,et al.  Buoyancy Regulation and the Potential for Vertical Migration in the Oceanic Cyanobacterium Trichodesmium , 2002, Microbial Ecology.

[93]  Hans W. Paerl,et al.  The oceanic fixed nitrogen and nitrous oxide budgets: Moving targets as we enter the anthropocene?* , 2001 .

[94]  D. Capone,et al.  NUTRIENT CONTROLS ON NITROGEN UPTAKE AND METABOLISM BY NATURAL POPULATIONS AND CULTURES OF TRICHODESMIUM (CYANOBACTERIA) , 2001 .

[95]  P. Falkowski,et al.  Segregation of Nitrogen Fixation and Oxygenic Photosynthesis in the Marine Cyanobacterium Trichodesmium , 2001, Science.

[96]  Nicolas Gruber,et al.  Denitrification and N2 fixation in the Pacific Ocean , 2001 .

[97]  D. Capone,et al.  Stoichiometry of nitrogen and carbon utilization in cultured populations of Trichodesmium IMS101: Implications for growth , 2001 .

[98]  K. Fennel,et al.  A deterministic model for N2 fixation at stn. ALOHA in the subtropical North Pacific Ocean , 2001 .

[99]  Nicholas R. Bates,et al.  Modeling the effect of nitrogen fixation on carbon and nitrogen fluxes at BATS , 2001 .

[100]  Alexander F. Shchepetkin,et al.  Open boundary conditions for long-term integration of regional oceanic models , 2001 .

[101]  Katja Fennela,et al.  A deterministic model for N 2 fixation at stn . ALOHA in the subtropical North Pacific Ocean , 2001 .

[102]  S. Doney,et al.  An intermediate complexity marine ecosystem model for the global domain , 2001 .

[103]  D. Capone,et al.  The nitrogen physiology of the marine N2-fixing cyanobacteria Trichodesmium spp. , 2000, Trends in plant science.

[104]  Cécile Dupouy,et al.  Satellite captures Trichodesmium blooms in the southwestern tropical Pacific [\textit{Trichodesmium}] , 2000 .

[105]  K. Flynn,et al.  INTERACTIONS BETWEEN IRON, LIGHT, AMMONIUM, AND NITRATE: INSIGHTS FROM THE CONSTRUCTION OF A DYNAMIC MODEL OF ALGAL PHYSIOLOGY , 1999 .

[106]  Francisco P. Chavez,et al.  Continental-shelf sediment as a primary source of iron for coastal phytoplankton , 1999, Nature.

[107]  Kendall L. Carder,et al.  Carbon cycling in the upper waters of the Sargasso Sea: I. Numerical simulation of differential carbon and nitrogen fluxes , 1999 .

[108]  Ricardo M Letelier,et al.  TRICHODESMIUM SPP. PHYSIOLOGY AND NUTRIENT FLUXES IN THE NORTH PACIFIC SUBTROPICAL GYRE , 1998 .

[109]  M. Fasham,et al.  Modelling the interactions between ammonium and nitrate uptake in marine phytoplankton , 1997 .

[110]  W. Sunda,et al.  Interrelated influence of iron, light and cell size on marine phytoplankton growth , 1997, Nature.

[111]  Ricardo M Letelier,et al.  The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean , 1997, Nature.

[112]  Edward J. Carpenter,et al.  Trichodesmium, a Globally Significant Marine Cyanobacterium , 1997 .

[113]  Inez Y. Fung,et al.  Contribution to the atmospheric mineral aerosol load from land surface modification , 1995 .

[114]  W. Large,et al.  Oceanic vertical mixing: a review and a model with a nonlocal boundary layer parameterization , 1994 .

[115]  Y. Fujita,et al.  Regulation of nitrogenase activity in relation to the light-dark regime in the filamentous non-heterocystous cyanobacterium Trichodesmium sp. NIBB 1067 , 1992 .

[116]  A. Walsby,et al.  Buoyancy regulation and vertical migration of Trichodesmium: a computer-model prediction , 1992 .

[117]  E. Carpenter,et al.  Marine pelagic cyanobacteria : Trichodesmium and other diazotrophs , 1992 .

[118]  M. Roman,et al.  Grazers and Associated Organisms of Trichodesmium , 1992 .

[119]  E. Carpenter,et al.  Diel buoyancy regulation in the marine diazotrophic cyanobacterium Trichodesmium thiebautii , 1990 .

[120]  H. Paerl,et al.  Immunochemical Localization of Nitrogenase in Marine Trichodesmium Aggregates: Relationship to N2 Fixation Potential , 1989, Applied and environmental microbiology.

[121]  J. Raven.  The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources , 1988 .

[122]  J. Rueter.  IRON STIMULATION OF PHOTOSYNTHESIS AND NITROGEN FIXATION IN ANABAENA 7120 AND TRICHODESMIUM (CYANOPHYCEAE) 1 , 1988 .

[123]  J. Postgate.  Biological nitrogen fixation: fundamentals , 1982 .

[124]  E. Carpenter.  Nitrogen Fixation by a Blue-Green Epiphyte on Pelagic Sargassum , 1972, Science.