Abstract
Sediment denitrification is a major pathway of fixed nitrogen loss from aquatic systems. Due to technical difficulties in measuring this process and its spatial and temporal variability, estimates of local, regional and global denitrification have to rely on a combination of measurements and models. Here we review approaches to describing denitrification in aquatic sediments, ranging from mechanistic diagenetic models to empirical parameterizations of nitrogen fluxes across the sediment-water interface. We also present a compilation of denitrification measurements and ancillary data for different aquatic systems, ranging from freshwater to marine. Based on this data compilation we reevaluate published parameterizations of denitrification. We recommend that future models of denitrification use (1) a combination of mechanistic diagenetic models and measurements where bottom-waters are temporally hypoxic or anoxic, and (2) the much simpler correlations between denitrification and sediment oxygen consumption for oxic bottom waters. For our data set, inclusion of bottom water oxygen and nitrate concentrations in a multivariate regression did not improve the statistical fit.
Similar content being viewed by others
Abbreviations
- DNRA:
-
Dissimalatory nitrate reduction to ammonium
- ODUs:
-
Oxygen-demand units
- SFM:
-
Sediment flux model
- SOC:
-
Sediment oxygen consumption
References
Aller RC (1980) Quantifying solute distributions in the bioturbated zone of marine sediments by defining an average microenvironment. Geochim Cosmochim Acta 44(12):1955–1965
Aller RC (1988) Benthic fauna and biogeochemical processes in marine sediments: the role of burrow structures. In: Blackburn TH, Soerensen J (eds) Nitrogen cycling in coastal marine environments. Wiley, New York, pp 301–338
Aller RC, Mackin JE, Ullman WJ, Wang CH, Tsai SM, Jin JC et al (1985) Early chemical diagenesis, sediment-water solute exchange, and storage of reactive organic matter near the mouth of the Changjiang, East China Sea. Cont Shelf Res 4(1/2):227–251
Altabet MA, Francois R, Murray DW, Prell WL (1995) Climate-related variations in denitrification in the Arabian Sea from sediment 15 N/14 N ratios. Nature 373(6514):506–509
An S, Gardner WS, Kana T (2001) Simultaneous measurement of denitrification and nitrogen fixation using isotope pairing with membrane inlet mass spectrometry analysis. Appl Environ Microbiol 67:1171–1178
Bender M, Jahnke R, Weiss R, Martin W, Heggie DT, Orchardo J et al (1989) Organic carbon oxidation and benthic nitrogen and silica dynamics in San Clemente Basin, a continental borderland site. Geochim Cosmochim Acta 53(3):685–697
Berner RA (1980) Early diagenesis: a theoretical approach. Princeton University Press, Princeton
Billen G, Garnier J (1999) Nitrogen transfers through the Seine drainage network: a budget based on the application of the Riverstrahler’ model. Hydrobiologia 410:139–150
Billen G, Garnier J, Hanset P (1994) Modelling phytoplankton development in whole drainage networks: the Riverstrahler Model applied to the Seine river system. Hydrobiologia 289(1):119–137
Boudreau BP (1997) Diagenetic models and their implementation: modelling transport and reactions in aquatic sediments. Springer, Berlin
Boyer EW, Alexander RB, Parton WJ, Li C, Butterbach-Bahl K, Donner SD et al (2006) Modeling denitrification in terrestrial and aquatic ecosystems at regional scales: current approaches and needs. Ecol Appl 16:2123–2142
Burdige DJ (2006) Geochemistry of marine sediments. Princeton University Press, Princeton
Caffrey JM, Sloth NP, Kaspar HF, Blackburn TH (1993) Effect of organic loading on nitrification and denitrification in a marine microcosm. FEMS Microbiol Ecol 12:159–167
Caraco N, Cole J, Likens GE (1990) A comparison of phosphorus immobilization in sediments of freshwater and coastal marine systems. Biogeochemistry 9(3):277–290
Cerco CF, Seitzinger SP (1997) Measured and modeled effects of benthic algae on eutrophication in Indian River-Rehoboth Bay, Delaware. Estuar Coasts 20(1):231–248
Childs CR, Rabalais NN, Turner RE, Proctor LM (2002) Sediment denitrification in the Gulf of Mexico zone of hypoxia. Mar Ecol Prog Ser 240:285–290
Christensen JP (1994) Carbon export from continental shelves, denitrification and atmospheric carbon dioxide. Cont Shelf Res 14(5):547–576
Cornwell J, Owens M (1999) Benthic phosphorus cycling in Lake Champlain: results of an integrated field sampling/water quality modeling study. Part B: Field studies. Lake Champlain Basin Program. Horn Point Laboratory, Cambridge MD. Technical report TS-168-98
Cowan JLW, Boynton WR (1996) Sediment-water oxygen and nutrient exchanges along the longitudinal axis of Chesapeake Bay: seasonal patterns, controlling factors and ecological significance. Estuaries 19(3):562–580
Dalsgaard T, Canfield DE, Petersen J, Thamdrup B, Acuna-Gonzalez J (2003) N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422(6932):606–608
Devol AH (2008) Chapter 6: Denitrification including anammox. In: Capone D, Carpenter E, Mullholland M, Bronk D (eds) Nitrogen in the marine environment. Elsevier, Amsterdam, pp 263–302
Devol AH, Christensen JP (1993) Benthic fluxes and nitrogen cycling in sediments of the continental margin of the eastern North Pacific. J Mar Res 51:345–372
Devol AH, Codispoti LA, Christensen JP (1997) Summer and winter denitrification rates in western Arctic shelf sediments. Cont Shelf Res 17(9):1029–1050
DiToro DM (2001) Sediment flux modeling. Wiley-Interscience, New York
DiToro DM, Fitzpatrick JJ (1993) Chesapeake Bay sediment flux model. US EPA Contract Report, Annapolis
Emery K (1968) Relict sediments on continental shelves of world. AAPG Bull 52(3):445–464
Engström P, Dalsgaard T, Hulth S, Aller RC (2005) Anaerobic ammonium oxidation by nitrite (anammox): implications for N2 production in coastal marine sediments. Geochim Cosmochim Acta 69(8):2057–2065
Falkowski PG (1997) Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387:272–275
Fennel K, Follows M, Falkowski PG (2005) The co-evolution of the nitrogen, carbon and oxygen cycles in the Proterozoic Ocean. Am J Sci 305:526–545
Fennel K, Wilkin J, Levin J, Moisan J, O’Reilly J, Haidvogel D (2006) Nitrogen cycling in the Middle Atlantic Bight: Results from a three-dimensional model and implications for the North Atlantic nitrogen budget. Global Biogeochemical Cycles 20, GB3007, doi:10.1029/2005GB002456
Fulweiler RW (2007) Climate impacts on benthic-pelagic coupling and biogeochemistry in Narragansett Bay, RI. PhD Dissertation, University of Rhode Island
Fulweiler RW, Nixon SW (2008) Responses of benthic-pelagic coupling to climate change in a temperate estuary. Hydrobiologia (in press)
Fulweiler R, Nixon S, Buckley B, Granger S (2007) Reversal of the net dinitrogen gas flux in coastal marine sediments. Nature 448:180–182
Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB et al (2003) The nitrogen cascade. Bioscience 53(4):341–356
Gardner WS, Briones EE, Kaegi EC, Rowe GT (1993) Ammonium excretion by benthic invertebrates and sediment-water nitrogen flux in the Gulf of Mexico near the Mississippi River plume. Estuaries 16(4):799–808
Gardner WS, McCarthy MJ, An S, Sobolev D, Sell KS, Brock D (2006) Nitrogen fixation and dissimilatory nitrate reduction to ammonium (DNRA) support nitrogen dynamics in Texas estuaries. Limnol Oceanogr 51(1):558–568
Garnier J, Billen G, Coste M (1995) Seasonal succession of diatoms and chlorophyceae in the drainage network of the Seine River: Observations and modeling. Limnol Oceanogr 40(4):750–765
Giblin AE, Hopkinson CS, Tucker J (1997) Benthic metabolism and nutrient cycling in Boston Harbor, Massachusetts. Estuaries 20:346–364
Gold AJ, Jacinthe PA, Groffman PM, Wright WR, Puffer RH (1998) Patchiness in groundwater nitrate removal in a riparian forest. Environ Qual 27:146–155
Harrison J, Maranger R, Alexander RB, Cornwell J, Giblin A, Jacinthe PA, et al. (2008) The regional and global significance of nitrogen removal in lakes and reservoirs. Biogeochemistry. doi:10.1007/s10533-008-9272-x
Huettel M, Webster IT (2001) Advective flow in permeable sediments. In: Boudreau BP, Jørgensen BB (eds) The benthic boundary layer: transport processes and biogeochemistry. Oxford University Press, Oxford, pp 144–179
Jacinthe PA, Groffman PM, Gold AJ, Mosier A (1998) Patchiness in microbial nitrogen transformations in groundwater in a riparian forest. J Environ Quality 27:156–164
Jahnke R (1985) A model of microenvironments in deep-sea sediments: formation and effects on pore water profiles. Limnol Oceanogr 30(5):956–965
Jahnke RA, Emerson SR, Murray JW (1982) A model of oxygen reduction, denitrification, and organic matter mineralization in marine sediments. Limnol Oceanogr 27(4):610–623
Jahnke RA, Richards M, Nelson J, Robertson C, Rao A, Jahnke D (2005) Organic matter remineralization and pore water exchange rates in permeable South Atlantic Bight continental shelf sediments. Contl Shelf Res 25:1433–1452
Kana TM, Darkangelo C, Hunt MD, Oldham JB, Bennett GE, Cornwell JC (1994) Membrane inlet mass spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples. Anal Chem 66(23):4166–4170
Kana TM, Sullivan MB, Cornwell JC, Groszkowski KM (1998) Denitrification in estuarine sediments determined by membrane inlet mass spectrometry. Limnol Oceanogr 43(2):334–339
Kemp WM, Sampou P, Caffrey J, Mayer M, Henriksen K, Boynton WR (1990) Ammonium recycling versus denitrification in Chesapeake Bay sediments. Limnol Oceanogr 35(7):1545–1563
Kemp WM, Boynton WR, Adolf JE, Boesch DF, Boicourt WC, Brush G et al (2005) Eutrophication of Chesapeake Bay: historical trends and ecological interactions. Mar Ecol Prog Ser 303:1–29
Klump JV, Martens CS (1987) Biogeochemical cycling in an organic-rich coastal marine basin. 5. Sedimentary nitrogen and phosphorus budgets based upon kinetic models mass balaces, and the stoichiometry of nutrient regeneration. Geochim Cosmochim Acta 51(5):1161–1173
Kuypers MM, Sliekers AO, Lavik G, Schmid M, Jorgensen BB, Kuenen JG et al (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422(6932):608–611
Kuypers MMM, Lavik G, Woebken D, Schmid M, Fuchs BM, Amann R et al (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci USA 102(18):6478–6483
Laursen AE, Seitzinger SP (2002) The role of denitrification in nitrogen removal and carbon mineralization in Mid-Atlantic Bight sediments. Cont Shelf Res 22:1397–1416
McCarthy MJ, Gardner WS, Lavrentyev PJ, Moats KM, Jochem FJ, Klarer DM (2007) Effects of hydrological flow regime on sediment-water interface and water column nitrogen dynamics in a Great Lakes coastal wetland (Old Woman Creek, Lake Erie). J Great Lakes Res 33(1):219
McCarthy M, McNeal K, Morse J, Gardner W (2008) Bottom-water hypoxia effects on sediment-water interface nitrogen transformations in a seasonally hypoxic, shallow bay (Corpus Christi Bay, Texas, USA). Estuar Coasts 31:521–531. doi: 10.1007/s12237-008-9041-z
Meissner KJ, Galbraith ED, Völker C (2005) Denitrification under glacial and interglacial conditions: A physical approach. Paleoceanography 20(3):PA3001
Middelburg JJ, Soetaert K, Herman PMJ, Heip C (1996) Denitrification in marine sediments: a model study. Global Biogeochem Cyc 10:661–673
Middelburg JJ, Soetaert K, Herman PMJ (1997) Empirical relationships for use in global diagenetic models. Deep-Sea Res I 44(2):327–344
Moore JK, Doney SC (2007) Iron availability limits the ocean nitrogen inventory stabilizing feedbacks between marine denitrification and nitrogen fixation. Global Biogeochemical Cycles 21. doi:10.1029/2006GB002762
Mulder A, van de Graaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol Ecol 16(3):177–183
Naqvi SW, Jayakumar DA, Narvekar PV, Naik H, Sarma VV, D’Souza W et al (2000) Increased marine production of N2O due to intensifying anoxia on the Indian continental shelf. Nature 408(6810):346–349
Oviatt CA, Keller AA, Sampou PA, Beatty LL (1986) Patterns of productivity during eutrophication: a mesocosm experiment. Mar Ecol Prog Ser 28(1–2):69–80
Paerl H, Zehr J (2000) Marine nitrogen fixation. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, Wilmington, pp 387–426
Parkin TB (1987) Soil microsites as a source of denitrification variability. Soil Sci Soc Am J 51:1194–1199
Rao AMF, McCarthy MJ, Gardner WS, Jahnke RA (2007) Respiration and denitrification in permeable continental shelf deposits on the South Atlantic Bight: rates of carbon and nitrogen cycling from sediment column experiments. Cont Shelf Res 27(13):1801–1819
Richards FA, Cline JD, Broenkow WW, Atkinson LP (1965) Some consequences of the decomposition of organic matter in Lake Nitinat, an Anoxic Fjord. Limnol Oceanogr 10:185–201
Risgaard-Petersen N, Meyer RL, Schmid M, Jetten MSM, Enrich-Prast A, Rysgaard S et al (2004) Anaerobic ammonium oxidation in an estuarine sediment. Aquat Microb Ecol 36(3):293–304
Ruelland D, Billen G, Brunstein D, Garnier J (2007) SENEQUE: a multi-scaling GIS interface to the Riverstrahler model of the biogeochemical functioning of river systems. Sci Total Environ 375:257–273
Seitzinger S, Harrison JA, Bohlke JK, Bouwman AF, Lowrance R, Peterson B et al (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16(6):2064–2090
Soetaert K, Herman PMJ, Middelburg JJ (1996a) Dynamic response of deep-sea sediments to seasonal variations: a model. Limnol Oceanogr 41(8):1651–1668
Soetaert K, Herman PMJ, Middelburg JJ (1996b) A model of early diagenetic processes from the shelf to abyssal depths. Geochim Cosmochim Acta 60(6):1019–1040
Soetaert K, Middelburg JJ, Herman PMJ, Buis K (2000) On the coupling of benthic and pelagic biogeochemical models. Earth-Sci Rev 51:173–201
Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68(3):1312–1318
Thibodeaux LJ, Boyle JD (1987) Bedform-generated convective transport in bottom sediment. Nature 325(6102):341–343
Thouvenot M, Billen G, Garnier J (2007) Modelling nutrient exchange at the sediment-water interface of river systems. J Hydrology 341(1–2):55–78
Trimmer M, Nicholls JC, Deflandre B (2003) Anaerobic ammonium oxidation measured in sediments along the thames estuary, United Kingdom. Appl Environ Microbiol 69(11):6447–6454
Trimmer M, Nicholls JC, Morley N, Davies CA, Aldridge J (2005) Biphasic behavior of anammox regulated by nitrite and nitrate in an estuarine sediment. Appl Environ Microbiol 71(4):1923–1930
Vanderborght JP, Wollast R, Billen G (1977a) Kinetic models of diagenesis in disturbed sediments. Part 1. Mass transfer properties and silica diagenesis. Limnol Oceanogr 22(5):787–793
Vanderborght JP, Wollast R, Billen G (1977b) Kinetic models of diagenesis in disturbed sediments. Part 2. Nitrogen diagenesis. Limnol Oceanogr 22(5):794–803
Acknowledgments
Discussions reflected in this paper were initiated in November 2006 at a Modeling Workshop organized by the Research Coordination Network on Denitrification (http://www.denitrification.org/). We thank the organizers and gratefully acknowledge the constructive criticism from Eric Davidson and two anonymous reviewers. We thank Jane Tucker for working up the data sets from Massachusetts Bay and Boston Harbor. Financial support for AEG to work on the manuscript came from NSF NSF-DEB-0423565. KF, DB and DDT acknowledge support from NOAA CHRP grant NA07NOS4780191. NOAA publication number 102.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Fennel, K., Brady, D., DiToro, D. et al. Modeling denitrification in aquatic sediments. Biogeochemistry 93, 159–178 (2009). https://doi.org/10.1007/s10533-008-9270-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-008-9270-z