Nitrogen fixation: A poorly understood process along the freshwater‐marine continuum

N2 fixation is a major component of the global N cycle and has been extensively studied in open‐ocean and terrestrial ecosystems. Yet rates and ecological dynamics remain virtually unknown for the inland and coastal aquatic ecosystems (lakes, wetlands, rivers, streams, and estuaries) that connect terrestrial and marine biomes. This is due to the diversity of these habitats as well as the traditional paradigm that N2 fixation rates were low to nonexistent, and therefore not important, in these ecosystems. We identify three major research themes to advance understanding of aquatic N2 fixation: (1) the biological diversity of diazotrophs and variability of N2 fixation rates, (2) the ecological stoichiometry of N2 fixation, and (3) the upscaling of N2 fixation rates from genes to ecosystems. Coordinating research across these areas will advance limnology and oceanography by fully integrating N2 fixation into ecological dynamics of aquatic ecosystems from local to global scales.

[1]  B. Poulter,et al.  Half of global methane emissions come from highly variable aquatic ecosystem sources , 2021, Nature Geoscience.

[2]  J. Scott,et al.  Biological stoichiometry and growth dynamics of a diazotrophic cyanobacteria in nitrogen sufficient and deficient conditions. , 2021, Harmful algae.

[3]  M. Bartoli,et al.  N2 fixation dominates nitrogen cycling in a mangrove fiddler crab holobiont , 2020, Scientific Reports.

[4]  J. Cotner,et al.  Upper Midwest lakes are supersaturated with N2 , 2020, Proceedings of the National Academy of Sciences.

[5]  D. Capone,et al.  Changing perspectives in marine nitrogen fixation , 2020, Science.

[6]  B. Karlson,et al.  Nitrogen fixation estimates for the Baltic Sea indicate high rates for the previously overlooked Bothnian Sea , 2020, Ambio.

[7]  Yiqi Luo,et al.  Substrate stoichiometry determines nitrogen fixation throughout succession in southern Chinese forests. , 2019, Ecology letters.

[8]  J. Zehr,et al.  Diversity, Genomics, and Distribution of Phytoplankton-Cyanobacterium Single-Cell Symbiotic Associations. , 2019, Annual review of microbiology.

[9]  H. Paerl,et al.  Nitrogen transformations differentially affect nutrient‐limited primary production in lakes of varying trophic state , 2019, Limnology and Oceanography Letters.

[10]  A. Martiny,et al.  Convergent estimates of marine nitrogen fixation , 2019, Nature.

[11]  M. Friesen,et al.  To Fix or Not To Fix: Controls on Free-Living Nitrogen Fixation in the Rhizosphere , 2019, Applied and Environmental Microbiology.

[12]  Jason G. Bragg,et al.  A quantitative model of nitrogen fixation in the presence of ammonium , 2018, PloS one.

[13]  A. Oschlies,et al.  Global Marine N2 Fixation Estimates: From Observations to Models , 2018, Front. Microbiol..

[14]  D. Schindler,et al.  Biological Nitrogen Fixation Prevents the Response of a Eutrophic Lake to Reduced Loading of Nitrogen: Evidence from a 46-Year Whole-Lake Experiment , 2018, Ecosystems.

[15]  T. Pavelsky,et al.  Global extent of rivers and streams , 2018, Science.

[16]  G. Chadwick,et al.  Widespread nitrogen fixation in sediments from diverse deep‐sea sites of elevated carbon loading , 2018, Environmental microbiology.

[17]  C. Baxter,et al.  Co-occurrence of in-stream nitrogen fixation and denitrification across a nitrogen gradient in a western U.S. watershed , 2018, Biogeochemistry.

[18]  R. Maranger,et al.  Stoichiometry of carbon, nitrogen, and phosphorus through the freshwater pipe , 2018 .

[19]  S. Passy,et al.  Iron limitation effects on nitrogen-fixing organisms with possible implications for cyanobacterial blooms , 2018, FEMS microbiology ecology.

[20]  E. Rejmánková,et al.  Heterotrophic N2-fixation contributes to nitrogen economy of a common wetland sedge, Schoenoplectus californicus , 2018, PloS one.

[21]  L. Riemann,et al.  Deep Into Oceanic N2 Fixation , 2018, Front. Mar. Sci..

[22]  M. Lukeš,et al.  Diel regulation of photosynthetic activity in the oceanic unicellular diazotrophic cyanobacterium Crocosphaera watsonii WH8501 , 2018, Environmental microbiology.

[23]  S. Dyhrman,et al.  Coordinated gene expression between Trichodesmium and its microbiome over day–night cycles in the North Pacific Subtropical Gyre , 2018, The ISME Journal.

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

[25]  M. Evans‐White,et al.  Comparing the Ecological Stoichiometry in Green and Brown Food Webs – A Review and Meta-analysis of Freshwater Food Webs , 2017, Front. Microbiol..

[26]  Anthony M. Bolger,et al.  Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer , 2017, Front. Plant Sci..

[27]  Yuanzhi Tang,et al.  Rapid Iron Reduction Rates Are Stimulated by High-Amplitude Redox Fluctuations in a Tropical Forest Soil. , 2017, Environmental science & technology.

[28]  I. Prentice,et al.  Modelling the demand for new nitrogen fixation by terrestrial ecosystems , 2016 .

[29]  H. Paerl,et al.  It Takes Two to Tango: When and Where Dual Nutrient (N & P) Reductions Are Needed to Protect Lakes and Downstream Ecosystems. , 2016, Environmental science & technology.

[30]  R. Buick,et al.  The evolution of Earth's biogeochemical nitrogen cycle , 2016 .

[31]  J. Lennon,et al.  Scaling laws predict global microbial diversity , 2016, Proceedings of the National Academy of Sciences.

[32]  R. Fulweiler,et al.  Molecular evidence for sediment nitrogen fixation in a temperate New England estuary , 2016, PeerJ.

[33]  L. Riemann,et al.  Genomics and Ecophysiology of Heterotrophic Nitrogen-Fixing Bacteria Isolated from Estuarine Surface Water , 2015, mBio.

[34]  R. Fulweiler,et al.  Examining the impact of acetylene on N-fixation and the active sediment microbial community , 2015, Front. Microbiol..

[35]  C. Godwin,et al.  Aquatic heterotrophic bacteria have highly flexible phosphorus content and biomass stoichiometry , 2015, The ISME Journal.

[36]  A. Huryn,et al.  Does N2 fixation amplify the temperature dependence of ecosystem metabolism? , 2015, Ecology.

[37]  Eva E. Stüeken,et al.  Isotopic evidence for biological nitrogen fixation by molybdenum-nitrogenase from 3.2 Gyr , 2015, Nature.

[38]  K. Furuya,et al.  Heterotrophic bacteria as major nitrogen fixers in the euphotic zone of the Indian Ocean , 2014 .

[39]  C. Verpoorter,et al.  A global inventory of lakes based on high‐resolution satellite imagery , 2014 .

[40]  B. Jenkins,et al.  Profiling gene expression to distinguish the likely active diazotrophs from a sea of genetic potential in marine sediments , 2014, Environmental microbiology.

[41]  N. Planavsky,et al.  The rise of oxygen in Earth’s early ocean and atmosphere , 2014, Nature.

[42]  Dennis R. Dean,et al.  Mechanism of Nitrogen Fixation by Nitrogenase: The Next Stage , 2014, Chemical reviews.

[43]  P. Ciais,et al.  Global carbon dioxide emissions from inland waters , 2013, Nature.

[44]  J. W. Peters,et al.  New insights into the evolutionary history of biological nitrogen fixation , 2013, Front. Microbiol..

[45]  R. Fulweiler,et al.  Evidence and a conceptual model for the co-occurrence of nitrogen fixation and denitrification in heterotrophic marine sediments , 2013 .

[46]  A. Knapp.  The sensitivity of marine N2 fixation to dissolved inorganic nitrogen , 2012, Front. Microbio..

[47]  Samuel T. Wilson,et al.  Comparative Assessment of Nitrogen Fixation Methodologies, Conducted in the Oligotrophic North Pacific Ocean , 2012, Applied and Environmental Microbiology.

[48]  J. Scott,et al.  Partitioning whole‐lake denitrification using in situ dinitrogen gas accumulation and intact sediment core experiments , 2012 .

[49]  Camila Fernandez,et al.  Nitrogen Fixation in Denitrified Marine Waters , 2011, PloS one.

[50]  Paul G Falkowski,et al.  The Evolution and Future of Earth’s Nitrogen Cycle , 2010, Science.

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

[52]  T. Treude,et al.  Burrowing deeper into benthic nitrogen cycling: the impact of bioturbation on nitrogen fixation coupled to sulfate reduction , 2010 .

[53]  E. Rejmánková,et al.  Nutrient enrichment in tropical wetlands: shifts from autotrophic to heterotrophic nitrogen fixation , 2010 .

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

[55]  J. Elser,et al.  Molybdenum—nitrogen co‐limitation in freshwater and coastal heterocystous cyanobacteria , 2010 .

[56]  J. Huisman,et al.  The ecological stoichiometry of toxins produced by harmful cyanobacteria: an experimental test of the carbon-nutrient balance hypothesis. , 2009, Ecology letters.

[57]  David W. Schindler,et al.  Eutrophication of lakes cannot be controlled by reducing nitrogen input: Results of a 37-year whole-ecosystem experiment , 2008, Proceedings of the National Academy of Sciences.

[58]  W. Wurtsbaugh,et al.  Is in-stream N2 fixation an important N source for benthic communities and stream ecosystems? , 2008, Journal of the North American Benthological Society.

[59]  R. Fulweiler,et al.  Reversal of the net dinitrogen gas flux in coastal marine sediments , 2007, Nature.

[60]  A. Bouwman,et al.  Denitrification across landscapes and waterscapes: a synthesis. , 2006, Ecological applications : a publication of the Ecological Society of America.

[61]  T. Fukushima,et al.  Effect of iron complexation with dissolved organic matter on the growth of cyanobacteria in a eutrophic lake , 2006 .

[62]  W. Wurtsbaugh,et al.  Temperature and nutrient supply interact to control nitrogen fixation in oligotrophic streams: An experimental examination , 2006 .

[63]  P. Leavitt,et al.  Spatial variation of nitrogen fixation in lakes of the northern Great Plains , 2006 .

[64]  S. Joye,et al.  Seasonal patterns of nitrogen fixation and denitrification in oceanic mangrove habitats , 2006 .

[65]  E. Flores,et al.  Nitrogen assimilation and nitrogen control in cyanobacteria. , 2005, Biochemical Society transactions.

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

[67]  P. Lockhart,et al.  Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin. , 2004, Molecular biology and evolution.

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

[69]  Jason Raymond,et al.  The natural history of nitrogen fixation. , 2004, Molecular biology and evolution.

[70]  J. Elser,et al.  Growth rate–stoichiometry couplings in diverse biota , 2003 .

[71]  Jonathan P Zehr,et al.  Nitrogenase gene diversity and microbial community structure: a cross-system comparison. , 2003, Environmental microbiology.

[72]  R. Eady.  Structure−Function Relationships of Alternative Nitrogenases , 1996 .

[73]  F. Stuart Chapin,et al.  Mechanisms of Primary Succession Following Deglaciation at Glacier Bay, Alaska , 1994 .

[74]  E. Carpenter,et al.  Basis for Diel Variation in Nitrogenase Activity in the Marine Planktonic Cyanobacterium Trichodesmium thiebautii , 1990, Applied and environmental microbiology.

[75]  R. Howarth,et al.  Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 1. Rates and importance1 , 1988 .

[76]  B. Whitton.  Ecology of Cyanobacteria II , 2012, Springer Netherlands.

[77]  M. Power,et al.  Light-mediated thresholds in stream-water nutrient composition in a river network. , 2011, Ecology.

[78]  Stephen Porder,et al.  Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. , 2010, Ecological applications : a publication of the Ecological Society of America.

[79]  J. Zehr,et al.  Nitrogen fixation: Nitrogenase genes and gene expression , 2001 .

[80]  N. Grimm,et al.  Nitrogen fixation in a desert stream ecosystem , 1997 .