Skip to main content
SpringerLink
Log in

Sediment Nitrogen Fixation: a Call for Re-evaluating Coastal N Budgets

Estuaries and Coasts volume 39, pages 1626–1638 (2016)Cite this article

Abstract

Coastal ocean primary productivity is often limited by nitrogen (N) availability, which is determined by the balance between N sources (e.g., N-fixation, groundwater, river inputs, etc.) and sinks (e.g., denitrification, sediment burial, etc.). Historically, heterotrophic N-fixation in sediments was excluded as a significant source of N in estuarine budgets, based on low, indirectly measured rates (e.g., acetylene reduction assay) and because it was unnecessary to achieve mass balance. Many recent studies using net N2 flux measurements have shown that sediment N-fixation can equal or exceed N2 loss. In an effort to quantify N2 production and consumption simultaneously, we measured N-fixation and denitrification directly in sediment cores from a temperate estuary (Waquoit Bay, MA). N-fixation, dissimilatory nitrate reduction to ammonium, and denitrification occurred simultaneously, and the net N2 flux shifted from uptake (N-fixation) to efflux (denitrification) over the 120-h incubation. Evidence for N-fixation included net 28N2 and 30N2 uptake, 15NH4 + production from 30N2 additions, 15Norganic matter production, and nifH expression. N-fixation from 30N2 was up to eight times higher than potential denitrification. However, N-fixation calculated from 15NO3 − was one half of the measured fixation from 30N2, indicating that 15NO3-isotope labeling calculations may underestimate N-fixation. These results highlight the dynamic nature of sediment N cycling and suggest that quantifying individual processes allows a greater understanding of what net N2 fluxes signify and how that balance varies over time.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • An, S., and W.S. Gardner. 2002. Dissimilatory nitrate reduction to ammonium (DNRA) as a nitrogen link, versus denitrification as a sink in a shallow estuary (Laguna Madre/Baffin Bay, Texas). Marine Ecology Progress Series 237: 41–50.

    Article  CAS  Google Scholar 

  • An, S., and S.B. Joye. 2001. Enhancement of coupled nitrification-denitrification by benthic photosynthesis in shallow estuarine sediments. Limnology and Oceanography 46(1): 62–74.

    Article  CAS  Google Scholar 

  • An, S., W.S. Gardner, and T. Kana. 2001. Simultaneous measurement of denitrification and nitrogen fixation using isotope pairing with membrane inlet mass spectrometry analysis. Applied and Environmental Microbiology 67(3): 1171–1178.

    Article  CAS  Google Scholar 

  • Bentzon-Tilia, M., S.J. Traving, M. Mantikci, H. Knudsen-Leerbeck, J.L. Hansen, S. Markager, and L. Riemann. 2015. Significant N2 fixation by heterotrophs, photoheterotrophs and heterocystous cyanobacteria in two temperate estuaries. The ISME Journal 9(2): 273–285.

    Article  CAS  Google Scholar 

  • Billen, G., M. Somville, E. De Becker, and P. Servais. 1985. A nitrogen budget of the Scheldt hydrographical basin. Netherlands Journal of Sea Research 19(3): 223–230.

    Article  Google Scholar 

  • Boudreau, B.P. 1996. A method-of-lines code for carbon and nutrient diagenesis in aquatic sediments. Computers & Geosciences 22(5): 479–496.

    Article  CAS  Google Scholar 

  • Bowen, J.L., and I. Valiela. 2001. The ecological effects of urbanization of coastal watersheds: Historical increases in nitrogen loads and eutrophication of Waquoit Bay estuaries. Canadian Journal of Fisheries and Aquatic Sciences 58(8): 1489–1500.

    Article  CAS  Google Scholar 

  • Braker, G., A. Fesefeldt, and K.P. Witzel. 1998. Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Applied and Environmental Microbiology 64(10): 3769–3775.

    CAS  Google Scholar 

  • Brin, L.D., A.E. Giblin, and J.J. Rich. 2014. Environmental controls of anammox and denitrification in southern New England estuarine and shelf sediments. Limnology and Oceanography 59(3): 851–860.

    Article  CAS  Google Scholar 

  • Brown, S.M., and B.D. Jenkins. 2014. Profiling gene expression to distinguish the likely active diazotrophs from a sea of genetic potential in marine sediments. Environmental Microbiology 16(10): 3128–3142.

    Article  CAS  Google Scholar 

  • Brunet, R.C., and L.J. Garcia-Gil. 1996. Sulfide-induced dissimilatory nitrate reduction anaerobic freshwater sediments. FEMS Microbiology Ecology 21(2): 131–138.

    Article  CAS  Google Scholar 

  • Burgin, A.J., and S.K. Hamilton. 2007. Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Frontiers in Ecology and the Environment 5(2): 89–96.

    Article  Google Scholar 

  • Capone, D.G., and E.J. Carpenter. 1982. Nitrogen fixation in the marine environment. Science 217(4565): 1140–1142.

    Article  CAS  Google Scholar 

  • Capone, D.G., J.P. Zehr, H.W. Paerl, B. Bergman, and E.J. Carpenter. 1997. Trichodesmium, a globally significant marine cyanobacterium. Science 276(5316): 1221–1229.

    Article  CAS  Google Scholar 

  • Cornwell, J.C., W.M. Kemp, and T.M. Kana. 1999. Denitrification in coastal ecosystems: Methods, environmental controls, and ecosystem level controls, a review. Aquatic Ecology 33(1): 41–54.

    Article  CAS  Google Scholar 

  • Crank J. 1975. The mathematics of diffusion. 2nd Edition, Oxford University Press.

  • Dalsgaard, T., B. Thamdrup, and D.E. Canfield. 2005. Anaerobic ammonium oxidation (anammox) in the marine environment. Research in Microbiology 156(4): 457–464.

    Article  CAS  Google Scholar 

  • Desnoues, N., M. Lin, X. Guo, L. Ma, R. Carreño-Lopez, and C. Elmerich. 2003. Nitrogen fixation genetics and regulation in a Pseudomonas stutzeri strain associated with rice. Microbiology 149(8): 2251–2262.

    Article  CAS  Google Scholar 

  • Eyre, B.D., and L.J. McKee. 2002. Carbon, nitrogen, and phosphorus budgets for a shallow subtropical coastal embayment (Moreton Bay, Australia). Limnology and Oceanography 47(4): 1043–1055.

    Article  CAS  Google Scholar 

  • Eyre, B.D., S. Rysgaard, T. Dalsgaard, and P.B. Christensen. 2002. Comparison of isotope pairing and N2:Ar methods for measuring sediment denitrification—assumption, modifications, and implications. Estuaries 25(6): 1077–1087.

    Article  CAS  Google Scholar 

  • Eyre, B.D., D.T. Maher, and P. Squire. 2013. Quantity and quality of organic matter (detritus) drives N2 effluxes (net denitrification) across seasons, benthic habitats, and estuaries. Global Biogeochemical Cycles 27.4(2013): 1083–1095.

    Article  Google Scholar 

  • Fan Lu. 2013. Response of diazotrophic microbial community to nitrogen input and glyphosate application in soils cropped to soybean. Ph.D. Dissertation, Auburn University, Auburn.

  • Ferguson, A., and B. Eyre. 2013. Interaction of benthic microalgae and macrofauna in the control of benthic metabolism, nutrient fluxes and denitrification in a shallow sub-tropical coastal embayment (western Moreton Bay, Australia). Biogeochemistry 112(1-3): 423–440.

    Article  CAS  Google Scholar 

  • Foster, S.Q., and R.W. Fulweiler. 2014. Spatial and historic variability of benthic nitrogen cycling in an anthropogenically impacted estuary. Frontiers in Marine Science 1: 56.

    Article  Google Scholar 

  • Foster, S. Q., and R.W. Fulweiler. (2015). Corrigendum: Spatial and historic variability of benthic nitrogen cycling in an anthropogenically impacted estuary. Frontiers in Marine Science 2: 70.

  • Francis, C.A., K.J. Roberts, J.M. Beman, A.E. Santoro, and B.B. Oakley. 2005. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences of the United States of America 102(41): 14683–14688.

    Article  CAS  Google Scholar 

  • Froelich, P., G.P. Klinkhammer, M.A.A. Bender, N.A. Luedtke, G.R. Heath, D. Cullen, et al. 1979. Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: Suboxic diagenesis. Geochimica et Cosmochimica Acta 43(7): 1075–1090.

    Article  CAS  Google Scholar 

  • Fulweiler, R.W., and E.M. Heiss. 2014. A decade of directly measured sediment N. Oceanography 27(1): 184.

    Article  Google Scholar 

  • Fulweiler, R.W., S.W. Nixon, B.A. Buckley, and S.L. Granger. 2007. Reversal of the net dinitrogen gas flux in coastal marine sediments. Nature 448(7150): 180–182.

    Article  CAS  Google Scholar 

  • Fulweiler, R.W., S.M. Brown, S.W. Nixon, and B.D. Jenkins. 2013. Evidence and a conceptual model for the cooccurrence of nitrogen fixation and denitrification in heterotrophic marine sediments. Marine Ecology Progress Series 482: 57–68.

    Article  CAS  Google Scholar 

  • Fulweiler, RW., Heiss, E. M., Rogener, M. K., Newell, S. E., LeCleir, G. R., Kortebein, S. M., & Wilhelm, S. W. 2015. Examining the impact of acetylene on N-fixation and the active sediment microbial community. Frontiers in Microbiology 6.

  • Galloway, J.N., Leach, A.M., Bleeker, A., & Erisman, J.W. 2013. A chronology of human understanding of the nitrogen cycle. Philosophical Transactions of the Royal Society B: Biological Sciences 368(1621).

  • Gardner, W. S., & McCarthy, M. J. 2006. Dissimilatory Nitrate Reduction to Ammonium(DNRA) as a “link” for N and a “sink” for oxygen in shallow, hypoxic, coastal environments. EOS, Transactions, American Geophysical Union 87(36).

  • Gardner, W.S., and M.J. McCarthy. 2009. Nitrogen dynamics at the sediment–water interface in shallow, sub-tropical Florida Bay: Why denitrification efficiency may decrease with increased eutrophication. Biogeochemistry 95(2-3): 185–198.

    Article  CAS  Google Scholar 

  • Gardner, W.S., and P.A. St. John. 1991. High-performance liquid chromatographic method to determine ammonium ion and primary amines in seawater. Analytical Chemistry 63(5): 537–540.

    Article  CAS  Google Scholar 

  • Gardner, W.S., H.A. Bootsma, C. Evans, and P.A.S. John. 1995. Improved chromatographic analysis of 15N:14N ratios in ammonium or nitrate for isotope addition experiments. Marine Chemistry 48(3): 271–282.

    Article  CAS  Google Scholar 

  • Gardner, W.S., M.J. McCarthy, S. An, D. Sobolev, K.S. Sell, and D. Brock. 2006. Nitrogen fixation and dissimilatory nitrate reduction to ammonium (DNRA) support nitrogen dynamics in Texas estuaries. Limnology and Oceanography 51(1): 558–568.

    Article  CAS  Google Scholar 

  • Gardner, W.S., M.J. McCarthy, S.A. Carini, A.C. Souza, H. Lijun, K.S. McNeal, M.K. Puckett, and J. Pennington. 2009. Collection of intact sediment cores with overlying water to study nitrogen- and oxygen-dynamics in regions with seasonal hypoxia. Continental Shelf Research 29: 2207–2213.

    Article  Google Scholar 

  • Giblin, A.E., C.R. Tobias, B. Song, N. Weston, G.T. Banta, and V.H. Rivera-Monroy. 2013. The importance of DNRA in the nitrogen cycle of coastal ecosystems. Oceanography 26: 124–131.

    Article  Google Scholar 

  • Grantz, E.M., A. Kogo, and J. Thad Scott. 2012. Partitioning whole-lake denitrification using in situ dinitrogen gas accumulation and intact sediment core experiments. Limnology and Oceanography 57(4): 925–935.

    Article  CAS  Google Scholar 

  • Grasshoff, K., Kremling, K., and Ehrhardt, M. (1999). Methods of seawater analysis. 3rd ed., eds.K. Grasshoff, K. Kremling, and M. Ehrhardt Wiley-VCH.

  • Hamersley, R.M., and B.L. Howes. 2005. Evaluation of the N2 flux approach for measuring sediment denitrification. Estuarine Coastal and Shelf Science 62(4): 711–723.

    Article  CAS  Google Scholar 

  • Hartnett, H.E., and S.P. Seitzinger. 2003. High-resolution nitrogen gas profiles in sediment porewaters using a new membrane probe for membrane-inlet mass spectrometry. Marine Chemistry 83(1): 23–30.

    Article  CAS  Google Scholar 

  • Heiss, E.M., L. Fields, and R.W. Fulweiler. 2012. Directly measured net denitrification rates in offshore New England sediments. Continental Shelf Research 45: 78–86.

    Article  Google Scholar 

  • Hopkinson, C.S., I. Buffam, J. Hobbie, J. Vallino, M. Perdue, B. Eversmeyer, et al. 1998. Terrestrial inputs of organic matter to coastal ecosystems: An intercomparison of chemical characteristics and bioavailability. Biogeochemistry 43(3): 211–234.

    Article  CAS  Google Scholar 

  • Howarth, R. W., Marino, R., & Cole, J. J. 1988. Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 2. Biogeochemical controls. Limnology and Oceanography 688-701.

  • Kana, T.M., and D.L. Weiss. 2004. Comment on “Comparison of isotope pairing and N2:Ar methods for measuring sediment denitrification” by BD Eyre, S. Rysgaard, T. Dalsgaard, and P. Bondo Christensen. Estuaries and Coasts 27(1): 173–176.

    Article  CAS  Google Scholar 

  • Kana, T.M., C. Darkangelo, M.D. Hunt, J.B. Oldham, G.E. Bennett, and J.C. Cornwell. 1994. Membrane inlet mass spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples. Analytical Chemistry 66(23): 4166–4170.

    Article  CAS  Google Scholar 

  • Kartal, B., M.M. Kuypers, G. Lavik, J. Schalk, H.J. Op den Camp, M.S. Jetten, and M. Strous. 2007. Anammox bacteria disguised as denitrifiers: Nitrate reduction to dinitrogen gas via nitrite & ammonium. Environmental Microbiology 9(3): 635–642.

    Article  CAS  Google Scholar 

  • Knapp, A. N. 2012. The sensitivity of marine N2 fixation to dissolved inorganic nitrogen. Frontiers in microbiology 3.

  • Koike, I., and A. Hattori. 1978. Simultaneous determinations of nitrification and nitrate reduction in coastal sediments by a 15N dilution technique. Marine Ecology-Progress Series 35: 853–857.

    CAS  Google Scholar 

  • Koop-Jakobsen, K., and A.E. Giblin. 2010. The effect of increased nitrate loading on nitrate reduction via denitrification and DNRA in salt marsh sediments. Limnology and Oceanography 55(2): 789.

    Article  CAS  Google Scholar 

  • Körner, H., and W.G. Zumft. 1989. Expression of denitrification enzymes in response to the dissolved oxygen level and respiratory substrate in continuous culture of Pseudomonas stutzeri. Applied and Environmental Microbiology 55(7): 1670–1676.

    Google Scholar 

  • Lam, P., Lavik, G., Jensen, M. M., van de Vossenberg, J., Schmid, M., Woebken, D.,… & Kuypers, M. M. 2009. Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proceedings of the National Academy of Sciences 106(12):4752–4757.

  • LaMontagne, M.G., V. Astorga, A.E. Giblin, and I. Valiela. 2002. Denitrification and the stoichiometry of nutrient regeneration in Waquoit Bay, Massachusetts. Estuaries 25(2): 272–281.

    Article  CAS  Google Scholar 

  • Lindell, D., and A.F. Post. 2001. Ecological aspects of ntcA gene expression and its use as an indicator of the nitrogen status of MarineSynechococcus spp. Applied and Environmental Microbiology 67(8): 3340–3349.

    Article  CAS  Google Scholar 

  • McCarthy, M.J., S.A. Carini, Z. Liu, N.E. Ostrom, and W.S. Gardner. 2013. Oxygen consumption in the water column and sediments of the northern Gulf of Mexico hypoxic zone. Estuarine Coastal and Shelf Science 123: 46–53.

    Article  CAS  Google Scholar 

  • McCarthy, M. J., Newell, S. E., Carini, S. A., & Gardner, W. S. 2015. Denitrification dominates sediment nitrogen removal and is enhanced by bottom-water hypoxia in the Northern Gulf of Mexico. Estuaries and Coasts 1-16.

  • Mortazavi, B., A.A. Riggs, J.M. Caffrey, H. Genet, and S.W. Phipps. 2012. The contribution of benthic nutrient regeneration to primary production in a shallow eutrophic estuary, Weeks Bay, Alabama. Estuaries and Coasts 35(3): 862–877.

    Article  CAS  Google Scholar 

  • Mulder, A., A.A. Van de Graaf, L.A. Robertson, and J.G. Kuenen. 1995. Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. FEMS Microbiology Ecology 16(3): 177–183.

    Article  CAS  Google Scholar 

  • Newell, S. E., Babbin, A. R., Jayakumar, A., & Ward, B. B. 2011. Ammonia oxidation rates and nitrification in the Arabian Sea. Global Biogeochemical Cycles 25(4)

  • Nixon, S.W., S.L. Granger, and B.L. Nowicki. 1995. An assessment of the annual mass balance of carbon, nitrogen, and phosphorus in Narragansett Bay. Biogeochemistry 31(1): 15–61.

    Article  Google Scholar 

  • Owens, N.J.P. 1988. Rapid and total automation of shipboard 15N analysis: Examples from the North Sea. Journal of Experimental Marine Biology and Ecology 122(2): 163–171.

    Article  CAS  Google Scholar 

  • Poly, F., L.J. Monrozier, and R. Bally. 2001. Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Research in Microbiology 152(1): 95–103.

    Article  CAS  Google Scholar 

  • Scott, J.T., M.J. McCarthy, W.S. Gardner, and R.D. Doyle. 2008. Denitrification, dissimilatory nitrate reduction to ammonium, and nitrogen fixation along a nitrate concentration gradient in a created freshwater wetland. Biogeochem 87(1): 99–111.

    Article  CAS  Google Scholar 

  • Seitzinger, S.P., and J.H. Garber. 1987. Nitrogen fixation and 15N2 calibration of the acetylene reduction assay in coastal marine sediment. Marine Ecology Progress Series 37: 65–73.

    Article  CAS  Google Scholar 

  • Seitzinger, S.P., W.S. Gardner, and A.K. Spratt. 1991. The effect of salinity on ammonium sorption in aquatic sediments: Implications for benthic nutrient recycling. Estuaries 14(2): 167–174.

    Article  CAS  Google Scholar 

  • Solorzano, L. 1969. Determination of ammonia in natural waters by the phenolypochlorite method. Limnology and Oceanography 14: 799–801.

    Article  CAS  Google Scholar 

  • Tiedje, J.M. 1988. Ecology of denitrification and dissimilatory nitrate reduction to ammonium. Biology of Anaerobic Microorganisms 717: 179–244.

    Google Scholar 

  • Valiela, I., M. Geist, J. McClelland, and G. Tomasky. 2000. Nitrogen loading from watersheds to estuaries: Verification of the Waquoit Bay nitrogen loading model. Biogeochemistry 49(3): 277–293.33.

    Article  CAS  Google Scholar 

  • Vieillard, A.M., and R.W. Fulweiler. 2012. Impacts of long-term fertilization on salt marsh tidal creek benthic nutrient and N2 gas fluxes. Marine Ecology Progress Series 471: 11–22.

    Article  CAS  Google Scholar 

  • Ward, B. B., Devol, A. H., Rich, J. J., Chang, B. X., Bulow, S. E., Naik, H.,… & Jayakumar, A. 2009. Denitrification as the dominant nitrogen loss process in the Arabian Sea. Nature 461(7260):78–81.

  • Welsh, D.T. 2000. Nitrogen fixation in seagrass meadows: Regulation, plant–bacteria interactions and significance to primary productivity. Ecology Letters 3(1): 58–71.

    Article  Google Scholar 

  • Wulff, F., B.D. Eyre, and R. Johnstone. 2011. Nitrogen versus phosphorus limitation in a subtropical coastal embayment (Moreton Bay; Australia): Implications for management. Ecological Modelling 222(1): 120–130.

    Article  CAS  Google Scholar 

  • Zehr, J.P., and P.J. Turner. 2001. 14 nitrogen fixation: Nitrogenase genes and gene expression. Marine Microbiology 30: 271.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Chris Weidman and the staff at WB-NERR for boat time and Sarah Foster, Hollie Emery, Kristin Yoshimura, and Kaitlyn Pritchard for assistance in the field and in the lab. We also thank Allen Hunt for his help with the diffusion calculations. SEN was funded by an NSF Postdoctoral Fellowship in Biology (1103692). This work was supported in part by funding from the Woods Hole Sea Grant to RWF, as well as the Sloan Foundation fellowship to RWF.

Author information

Authors and Affiliations

  1. Department of Earth and Environment, Boston University, Boston, MA, 02215, USA

    Silvia E. Newell & Robinson W. Fulweiler

  2. Department of Earth and Environmental Sciences, Wright State University, 3640 Colonel Glenn Highway, Dayton, OH, 45435, USA

    Silvia E. Newell & Mark J. McCarthy

  3. University of Texas Marine Science Institute, Port Aransas, TX, 78373, USA

    Mark J. McCarthy & Wayne S. Gardner

  4. Department of Biology, Boston University, Boston, MA, 02215, USA

    Robinson W. Fulweiler

Authors
  1. Silvia E. Newell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mark J. McCarthy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wayne S. Gardner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robinson W. Fulweiler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Silvia E. Newell.

Additional information

Communicated by David Reide Corbett

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Newell, S.E., McCarthy, M.J., Gardner, W.S. et al. Sediment Nitrogen Fixation: a Call for Re-evaluating Coastal N Budgets. Estuaries and Coasts 39, 1626–1638 (2016). https://doi.org/10.1007/s12237-016-0116-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-016-0116-y

Keywords

search

Navigation