Iron, phosphorus, and nitrogen supply ratios define the biogeography of nitrogen fixation

We present a unified conceptual framework describing the competition between diazotrophs and non-nitrogen-fixing marine plankton and their interaction with three essential nutrient elements: nitrogen (N), phosphorus (P), and iron (Fe). The theory explains the global biogeography of diazotrophs and the observed large-scale variations in surface ocean nutrient concentrations. The ratios in which N, P, and Fe are delivered to the surface ocean, relative to the demands of the phytoplankton community, define several biogeochemical provinces in terms of the limiting nutrients and the presence or absence of diazotrophs. Nutrient supply ratios provided by a global ecosystem model support the theoretical view that diazotroph biogeography is dominated by the Fe : N supply ratio, with the P : N supply ratio taking an important secondary role. The theory yields robust predictions for which strong empirical support is found in global observations of surface nutrient concentrations and diazotroph abundance.

[1]  C. Lovejoy,et al.  Nitrogen fixation and identification of potential diazotrophs in the Canadian Arctic , 2012 .

[2]  T. Lenton,et al.  Biotic stoichiometric controls on the deep ocean N:P ratio , 2007 .

[3]  S. Fan,et al.  Aeolian input of bioavailable iron to the ocean , 2006 .

[4]  Paul G. Falkowski,et al.  Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean , 1997, Nature.

[5]  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 .

[6]  I. Berman‐Frank,et al.  Nitrogen‐fixation strategies and Fe requirements in cyanobacteria , 2007 .

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

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

[9]  Nicolas Gruber,et al.  Global patterns of marine nitrogen fixation and denitrification , 1997 .

[10]  P. Falkowski,et al.  Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium , 2001 .

[11]  Curtis Deutsch,et al.  Oceanic nitrogen reservoir regulated by plankton diversity and ocean circulation , 2012, Nature.

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

[13]  F. Morel,et al.  Iron nutrition of phytoplankton and its possible importance in the ecology of ocean regions with hight nutrient and low biomass , 1991 .

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

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

[16]  J. Schade,et al.  A conceptual framework for ecosystem stoichiometry: balancing resource supply and demand , 2005 .

[17]  Anthony H. Knap,et al.  Overview of the U.S. JGOFS Bermuda Atlantic Time-series Study and the Hydrostation S program , 1996 .

[18]  K. Arrigo,et al.  Magnitude of oceanic nitrogen fixation influenced by the nutrient uptake ratio of phytoplankton , 2010 .

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

[20]  Stephanie Dutkiewicz,et al.  Modeling the coupling of ocean ecology and biogeochemistry , 2009 .

[21]  N. Gruber,et al.  A probabilistic estimate of global marine N‐fixation and denitrification , 2012 .

[22]  A. C. Redfield.  The biological control of chemical factors in the environment. , 1960, Science progress.

[23]  J. Zehr.  Nitrogen fixation by marine cyanobacteria. , 2011, Trends in microbiology.

[24]  W. Sunda,et al.  Iron uptake and growth limitation in oceanic and coastal phytoplankton , 1995 .

[25]  J. Sarmiento,et al.  The supply of excess phosphate across the Gulf Stream and the maintenance of subtropical nitrogen fixation , 2011 .

[26]  E. Boyle,et al.  Mesoscale Iron Enrichment Experiments 1993-2005: Synthesis and Future Directions , 2007, Science.

[27]  Adina Paytan,et al.  Atmospheric iron deposition: global distribution, variability, and human perturbations. , 2009, Annual review of marine science.

[28]  E. Achterberg,et al.  Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability , 2009 .

[29]  C. Deutsch,et al.  Nutrient ratios as a tracer and driver of ocean biogeochemistry. , 2012, Annual review of marine science.

[30]  A. Oschlies,et al.  Organic nutrients and excess nitrogen in the North Atlantic subtropical gyre , 2008 .

[31]  E. Carpenter,et al.  A REVISED ESTIMATE OF THE IRON USE EFFICIENCY OF NITROGEN FIXATION, WITH SPECIAL REFERENCE TO THE MARINE CYANOBACTERIUM TRICHODESMIUM SPP. (CYANOPHYTA) 1 , 2003 .

[32]  M. Follows,et al.  Distribution of diverse nitrogen fixers in the global ocean , 2010 .

[33]  Toby Tyrrell,et al.  The relative influences of nitrogen and phosphorus on oceanic primary production , 1999, Nature.

[34]  Edward A. Boyle,et al.  Decoupling of iron and phosphate in the global ocean , 2005 .

[35]  N. Mahowald,et al.  Combustion iron distribution and deposition , 2007 .

[36]  B. Tilbrook,et al.  The Southern Ocean Biological Response to Aeolian Iron Deposition , 2007, Science.

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

[38]  K. Furuya,et al.  Latitudinal distribution of diazotrophs and their nitrogen fixation in the tropical and subtropical western North Pacific , 2009 .

[39]  A. Devol,et al.  Nitrogen in the Marine Environment , 1985 .

[40]  E. Boyle,et al.  Phosphate depletion in the western North Atlantic Ocean. , 2000, Science.

[41]  K. Coale,et al.  The flux of iron from continental shelf sediments: A missing source for global budgets , 2004 .

[42]  David Tilman,et al.  Resources: A Graphical-Mechanistic Approach to Competition and Predation , 1980, The American Naturalist.

[43]  S. Fitzwater,et al.  The case for iron , 1991 .

[44]  D. Tilman.  Resource competition and community structure. , 1983, Monographs in population biology.

[45]  E. Carpenter.  Chapter 3 – NITROGEN FIXATION BY MARINE OSCILLATORIA (TRICHODESMIUM) IN THE WORLD's OCEANS , 1983 .

[46]  V. V. Bulygin,et al.  Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii , 2011, Proceedings of the National Academy of Sciences.

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

[48]  F. Cipriano,et al.  N2 Fixation by Unicellular Bacterioplankton from the Atlantic and Pacific Oceans: Phylogeny and In Situ Rates , 2004, Applied and Environmental Microbiology.

[49]  M. Lohan.  Marine Biogeochemical Cycles of Trace Elements and their Isotopes , 2010 .

[50]  P. Falkowski,et al.  Mix and match: how climate selects phytoplankton , 2007, Nature Reviews Microbiology.

[51]  M. Krom.  Insights on nitrogen balance in the Eastern Mediterranean Sea. , 2011, Environmental microbiology.

[52]  R. Geider,et al.  Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis , 2002 .

[53]  M. Saito,et al.  Regional distributions of nitrogen‐fixing bacteria in the Pacific Ocean , 2008 .