Oceanography The Official Magazine of
The Oceanography Society
Volume 26 Issue 03

View Issue TOC
Volume 26, No. 3
Pages 124 - 131


The Importance of Dissimilatory Nitrate Reduction to Ammonium (DNRA) in the Nitrogen Cycle of Coastal Ecosystems

By Anne E. Giblin , Craig R. Tobias, Bongkeun Song , Nathaniel Weston , Gary T. Banta , and Victor H. Rivera-Monroy 
Jump to
Article Abstract Citation References Copyright & Usage
Article Abstract

Until recently, it was believed that biological assimilation and gaseous nitrogen (N) loss through denitrification were the two major fates of nitrate entering or produced within most coastal ecosystems. Denitrification is often viewed as an important ecosystem service that removes reactive N from the ecosystem. However, there is a competing nitrate reduction process, dissimilatory nitrate reduction to ammonium (DNRA), that conserves N within the ecosystem. The recent application of nitrogen stable isotopes as tracers has generated growing evidence that DNRA is a major nitrogen pathway that cannot be ignored. Measurements comparing the importance of denitrification vs. DNRA in 55 coastal sites found that DNRA accounted for more than 30% of the nitrate reduction at 26 sites. DNRA was the dominant pathway at more than one-third of the sites. Understanding what controls the relative importance of denitrification and DNRA, and how the balance changes with increased nitrogen loading, is of critical importance for predicting eutrophication trajectories. Recent improvements in methods for assessing rates of DNRA have helped refine our understanding of the rates and controls of this process, but accurate measurements in vegetated sediment still remain a challenge.


Giblin, A.E., C.R. Tobias, B. Song, N. Weston, G.T. Banta, and V.H. Rivera-Monroy. 2013. The importance of dissimilatory nitrate reduction to ammonium (DNRA) in the nitrogen cycle of coastal ecosystems. Oceanography 26(3):124–131, https://doi.org/10.5670/oceanog.2013.54.


Algar, C.K., and J.J. Vallino. In press. Predicting nitrate reduction pathways in coastal sediments. Applied Environmental Microbiology

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, https://doi.org/10.3354/meps237041.

Atkinson, S.J., C.G. Mowat, G.A. Reid, and S.K. Chapman. 2007. An octaheme c-type cytochrome from Shewanella oneidensis can reduce nitrite and hydroxylamine. FEBS Letters 581:3,805–3,808, https://doi.org/10.1016/j.febslet.2007.07.005

Boon, P.L., D.J.W. Moriarty, and P.G. Saffigna. 1986. Nitrate metabolism in sediments from seagrass (Zostera capricorni) beds of Moreton Bay, Australia. Marine Biology 91:269–275, https://doi.org/10.1007/BF00569443.

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 5:89–96, https://doi.org/​10.1890/1540-9295(2007)5[89:HWOTRO]​2.0.CO;2.

Buresh, R.J., and W.H. Patrick. 1978. Nitrate reduction to ammonium in anaerobic soil. Soil Society of America Journal 42:913–918, https://doi.org/10.2136/sssaj1978.03615995004200060017x.

Canfield, D.E., A.N. Glazer, and P.G. Falkowski. 2010. The evolution and future of Earth’s nitrogen cycle. Science 330:192–196, https://doi.org/10.1126/science.1186120.

Christensen, P.B., S. Rysgaard, N.P. Sloth, T. Dalgaard, and S. Schwaeter. 2000. Sediment mineralization, nutrient fluxes, denitrification, and dissimilatory nitrate reduction to ammonium in an estuarine fjord with sea cage trout farms. Aquatic Microbial Ecology 21:73–84, https://doi.org/10.3354/ame021073.

Crowe, S.A., D.E. Canfield, A. Mucci, B. Sundby, and R. Maranger. 2012. Anammox, denitrification and fixed-nitrogen removal in sediments from the lower St. Lawrence Estuary. Biogeosciences 9:4,309-4,321, https://doi.org/10.5194/bgd-8-9503-2011.

Dong, L.F., C.J. Smith, S. Papaspyrou, A. Stott, A.M. Osborn, and D.B. Nedwell. 2009. Changes in benthic denitrification, nitrate ammonification and anammox process rates and nitrate and nitrite reductase gene abundances along an estuarine nutrient gradient (the Colne Estuary, United Kingdom). Applied and Environmental Microbiology 75:3,171–3,179, https://doi.org/​10.1128/AEM.02511-08

Drake, D.C., B.J. Peterson, K.A. Galvan, L.A. Deegan, C. Hopkinson, J.M. Johnson, K. Koop-Jakobsen, L.E. Lemay, and C. Picard. 2009. Salt marsh ecosystem biogeochemical responses to nutrient enrichment: A paired super 15N tracer study. Ecology 90:2,535–2,546, https://doi.org/10.1890/08-1051.1.

Dunn, R.J.K., D.T. Welsh, M.A. Jordan, N.J. Waltham, and C.J. Lemckert. 2012. Benthic metabolism and nitrogen dynamics in a sub-tropical coastal lagoon: Microphytobenthos stimulate nitrification and nitrate reduction through photosynthetic oxygen. Estuarine, Coastal and Shelf Science 113:272–282, https://doi.org/10.1016/j.ecss.2012.08.016.

Einsle, O., A. Messerschmidt, P. Stach, G.P. Bourenkov, H.D. Bartunik, R. Huber, and P.M. Kroneck. 1999. Structure of cytochrome c nitrite reductase. Nature 400:476–480, https://doi.org/10.1038/22802.

Fernandes, S.O., P.C. Bonin, V.D. Michotey, N. Garcia, and P.A. LokaBharathi. 2012. Nitrogen-limited mangrove ecosystems conserve N through dissimilatory nitrate reduction to ammonium. Scientific Reports 2:419–423, https://doi.org/10.1038/srep00419.

Ferrón, S., T. Ortega, and J.M. Forja. 2009. Benthic fluxes in a tidal salt marsh creek affected by fish farm activities: Río San Pedro (Bay of Cádiz, SW Spain). Marine Chemistry 113:50–62, https://doi.org/10.1016/j.marchem.2008.12.002.

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 95:185–198, https://doi.org/10.1007/s10533-009-9329-5.

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 Texan Estuaries. Limnology and Oceanography 51(1):558–568.

Giblin, A.E., N. Weston, G. Banta, J. Tucker, and C.S. Hopkinson. 2010. The effects of salinity on nitrogen loss from an oligohaline estuarine sediment. Estuaries and Coasts 33:1,054–1,068, https://doi.org/10.1007/s12237-010-9280-7.

Inglett, P.W., V.H. Rivera-Monroy, and J.R. Wozniak. 2011. Biogeochemistry of nitrogen across the Everglades landscape. Critical Reviews in Environmental Science and Technology 41:187–216, https://doi.org/​10.1080/10643389.2010.530933.

Kelly-Gerreyn, B.A., M. Trimmer, and D.K. Hydes 2001. A diagenetic model discriminating denitrification and dissimilatory nitrate reduction to ammonium in a temperate estuarine sediment. Marine Ecology Progress Series 220:33–46, https://doi.org/10.3354/meps220033.

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):789–802, https://doi.org/​10.4319/lo.2010.55.2.0789.

Lin, X., M.J. McCarthy, S.A. Carini, and W.S. Gardner. 2011. Net, actual, and potential sediment-water interface NH4+ fluxes in the northern Gulf of Mexico (NGOMEX): Evidence for NH4+ limitation of microbial dynamics. Continental Shelf Research 31:120–128, https://doi.org/10.1016/j.csr.2010.11.012.

McGlathery, K.J., K. Sundbäck, and I.C. Anderson. 2007. Eutrophication in shallow coastal bays and lagoons: The role of plants in the coastal filter. Marine Ecology Progress Series 348:1–18, https://doi.org/10.3354/meps07132.

Mohan, S.B., M. Schmid, M. Jetten, and J. Cole. 2004. Detection and widespread distribution of the nrfA gene encoding nitrite reduction to ammonia: A short circuit in the biological nitrogen cycle that competes with denitrification. FEMS Microbiology Ecology 49:433–443, https://doi.org/10.1016/j.femsec.2004.04.012.

Molnar, N., D.T. Welsh, C. Marchand, J. Deborde, and T. Meziane. 2013. Impacts of shrimp farm effluent on water quality, benthic metabolism and N-dynamics in a mangrove forest (New Caledonia). Estuarine, Coastal and Shelf Science 117:12–21, https://doi.org/10.1016/​j.ecss.2012.07.012.

Neubauer, S.C., I.C. Anderson, and B.B. Neikirk. 2005. Nitrogen cycling and ecosystem exchanges in a Virginia tidal freshwater marsh. Estuaries 28(6):909–922, https://doi.org/​10.1007/BF02696019.

Porubsky, W.P., S.B. Joye, W.S. Moore, K. Tuncay, and C. Meile. 2011. Field measurements and modeling of groundwater flow and biogeochemistry at Moses Hammock, a backbarrier island on the Georgia coast. Biogeochemistry 104:69–90, https://doi.org/​10.1007/s10533-010-9484-8.

Porubsky, W.P., L. Velasquez, and S. Joye. 2008. Nutrient-replete benthic microalgae as a source of dissolved organic carbon to coastal waters. Estuaries and Coasts 31:860–876, https://doi.org/10.1007/s12237-008-9077-0.

Porubsky, W.P., N. Weston, and S.B. Joye. 2009. Benthic metabolism and the fate of dissolved inorganic nitrogen in intertidal sediments. Estuarine, Coastal and Shelf Science 83:392–402, https://doi.org/10.1016/j.ecss.2009.04.012.

Poulin, P., É. Pelletier, V.G. Koutitonski, and U. Neumeier. 2009. Seasonal nutrient fluxes variability of northern salt marshes: Examples from the lower St. Lawrence Estuary. Wetlands Ecology and Management 17:655–673, https://doi.org/10.1007/s11273-009-9141-y.

Rivera-Monroy, V.H., B. Branoff, E. Meselhe, A. McCorquodale, M. Dortch, G. Stayer, J. Visser, and H. Wan. In press. Landscape-level estimation of nitrogen loss in coastal Louisiana wetlands: Potential sinks under different restoration scenarios. Journal of Coastal Research. 

Rivera-Monroy, V.H., P. Lenaker, R.R. Twilley, R.D. DeLaune, C.W. Lindau, W. Nuttle, E. Habib, R.W. Fulweiler, and E. Castaneda-Moya. 2010. Denitrification in coastal Louisiana: A spatial assessment and research needs. Journal of Sea Research 63:157–172, https://doi.org/10.1016/j.seares.2009.12.004.

Rivera-Monroy, V.H., and R.R. Twilley. 1996. The relative role of denitrification and immobilization in the fate of inorganic nitrogen in mangrove sediments. Limnology and Oceanography 41:284–296.

Rivera-Monroy, V.H., R.R. Twilley, R.G. Boustany, J.W. Day, F. Vera-Herrera, and M. del Carmon Ramirez. 1995. Direct denitrification in mangrove sediments in Terminos Lagoon, Mexico. Marine Ecology Progress Series 97:97–109, https://doi.org/10.3354/meps126097

Rysgaard, S., N. Risgaard-Petersen, and N.P. Sloth. 1996. Nitrification, denitrification, and nitrate ammonification in sediments of two coastal lagoons in southern France. Hydrobiologia 329:133–141, https://doi.org/​10.1007/BF00034553.

Sanford, R.A., D.D. Wagner, Q. Wu, J.C. Chee-Sanford, S.H. Thomas, C. Cruz-García, G. Rodríguez, A. Massol-Deyá, K.K. Krishnanif, K.M. Ritalahti, and others. 2012. Unexpected nondenitrifer nitrous oxide reductase gene diversity and abundance in soils. Proceedings of the National Academy of Sciences of the United States of America 48:19,709–19,714, https://doi.org/10.1073/pnas.1211238109.

Simon, J., M. Kern, B. Hermann, O. Einsle, and J.N. Butt. 2011. Physiological function and catalytic versatility of bacterial multihaem cytochromes c involved in nitrogen and sulfur cycling. Biochemical Society Transactions 39:1,864–1,870, https://doi.org/​10.1042/BST20110713.

Smyth, A.R., S.P. Thompson, K.N. Siporin, W.S. Gardner, M.J. McCarthy, and M.F. Piehler. 2013. Assessing nitrogen dynamics throughout the estuarine landscape. Estuaries and Coasts 36:44–55, https://doi.org/10.1007/s12237-012-9554-3.

Streminska, M.A., H. Felgate, G. Rowley, D.J. Richardson, and E.M. Baggs. 2012. Nitrous oxide production in soil isolates of nitrate-ammonifying bacteria. Environmental Microbiology Reports 4:66–71, https://doi.org/​10.1111/j.1758-2229.2011.00302.x.

Thamdrup, B. 2012. New pathways and processes in the global nitrogen cycle. Annual Review of Ecology, Evolution, and Systematics 43:407–428, https://doi.org/​10.1146/annurev-ecolsys-102710-145048.

Tiedje, J., A. Sexston, D. Myrold, and J. Robinson. 1982. Denitrification: Ecological niches, competition, and survival. Antonie van Leeuwenhoek 48:569–583, https://doi.org/​10.1007/BF00399542.

Tikhonova, T.V, A. Slutsky, A.N. Antipov, K.M. Boyko, K.M. Polyakov, D.Y. Sorokin, R.A. Zvyagilskaya, and V.O. Popov. 2006. Molecular and catalytic properties of a novel cytochrome c nitrite reductase from nitrate-reducing haloalkaliphilic sulfur-oxidizing bacterium Thioalkalivibrio nitratireducens. Biochimica et Biophysica Acta 1,764:715–723, https://doi.org/10.1016/j.bbapap.2005.12.021.

Tobias, C.R., I.C. Anderson, E.A. Canuel, and S.A. Macko. 2001a. Nitrogen cycling through a fringing marsh-aquifer ecotone. Marine Ecology Progress Series 210:25–39, https://doi.org/​10.3354/meps210025.

Tobias, C., A. Giblin, J. McClelland, J. Tucker, and B. Peterson. 2003. Sediment DIN fluxes and preferential recycling of benthic microalgal nitrogen in a shallow macrotidal estuary. Marine Ecological Progress Series 257:25–36, https://doi.org/10.3354/meps257025

Tobias, C.R., S.A. Macko, I.C. Anderson, E.A. Canuel, and J.W. Harvey. 2001b. Tracking the fate of a high concentration groundwater nitrate plume through a fringing marsh: A combined groundwater tracer and in situ isotope enrichment study. Limnology and Oceanography 46(8):1,977–1,989, https://doi.org/10.4319/lo.2001.46.8.1977.

Uldahl, A. 2011. Nitrate reduction processes and plant N status in S. alterniflora dominated marshes. MS thesis, University of Roskilde, Roskilde, DK. 

Viellard, A.M., and R.W. Fulweiller. 2012. Impacts of long-term fertilization on salt marsh tidal creek benthic nutrient and N2 gas fluxes. Marine Ecological Progress Series 47:11–22, https://doi.org/10.3354/meps10013.

Copyright & Usage

This is an open access article made available under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution, and reproduction in any medium or format as long as users cite the materials appropriately, provide a link to the Creative Commons license, and indicate the changes that were made to the original content. Images, animations, videos, or other third-party material used in articles are included in the Creative Commons license unless indicated otherwise in a credit line to the material. If the material is not included in the article’s Creative Commons license, users will need to obtain permission directly from the license holder to reproduce the material.