Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways

The removal of nitrogen (N) in aquatic ecosystems is of great interest because excessive nitrate in groundwater and surface water is a growing problem. High nitrate loading degrades water quality and is linked to eutrophication and harmful algal blooms, especially in coastal marine waters. Past research on nitrate removal processes has emphasized plant or microbial uptake (assimilation) or respiratory denitrification by bacteria. The increasing application of stable isotopes and other tracer techniques to the study of nitrate removal has yielded a growing body of evidence for alternative, microbially mediated processes of nitrate transformation. These include dissimilatory (the reduction of nitrogen into other inorganic compounds, coupled to energy producing processes) reduction of nitrate to ammonium (DNRA), chemoautotrophic denitrification via sulfur or iron oxidation, and anaerobic ammonium oxidation (anammox), as well as abiotic nitrate removal processes. Here, we review evidence for the importance of...

[1]  B. Wehrli,et al.  Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). , 2006, Environmental microbiology.

[2]  A. Kamp,et al.  Anaerobic Sulfide Oxidation with Nitrate by a Freshwater Beggiatoa Enrichment Culture , 2006, Applied and Environmental Microbiology.

[3]  W. Dodds.  Nutrients and the “dead zone”: the link between nutrient ratios and dissolved oxygen in the northern Gulf of Mexico , 2006 .

[4]  Mike S. M. Jetten,et al.  A microbial consortium couples anaerobic methane oxidation to denitrification , 2006, Nature.

[5]  Dmitrij Frishman,et al.  Deciphering the evolution and metabolism of an anammox bacterium from a community genome , 2006, Nature.

[6]  Y. Seike,et al.  N2O accumulation in estuarine and coastal sediments: The influence of H2S on dissimilatory nitrate reduction , 2006 .

[7]  D. Canfield,et al.  Anaerobic ammonium oxidation (anammox) in the marine environment. , 2005, Research in microbiology.

[8]  R. Glud,et al.  Denitrification and anammox activity in Arctic marine sediments , 2004 .

[9]  R. Glud,et al.  Anaerobic N2 production in Arctic sea ice , 2004 .

[10]  P. Visscher,et al.  Anaerobic Metabolism: Linkages to Trace Gases and Aerobic Processes , 2003 .

[11]  J. G. Kuenen,et al.  Anaerobic ammonium oxidation by marine and freshwater planctomycete-like bacteria , 2003, Applied Microbiology and Biotechnology.

[12]  R. E. Turner,et al.  Linking Landscape and Water Quality in the Mississippi River Basin for 200 Years , 2003 .

[13]  J. Zedler.  Wetlands at your service: reducing impacts of agriculture at the watershed scale , 2003 .

[14]  E. Davidson,et al.  A mechanism of abiotic immobilization of nitrate in forest ecosystems: the ferrous wheel hypothesis , 2003 .

[15]  M. Nguyen,et al.  Fate of 15N-nitrate in unplanted, planted and harvested riparian wetland soil microcosms , 2002 .

[16]  Wayne S Gardner,et al.  Dissimilatory nitrate reduction to ammonium (DNRA) as a nitrogen link, versus denitrification as a sink in a shallow estuary (Laguna Madre/Baffin Bay, Texas) , 2002 .

[17]  B. Jørgensen,et al.  Ecology of Thioploca spp.: Nitrate and Sulfur Storage in Relation to Chemical Microgradients and Influence ofThioploca spp. on the Sedimentary Nitrogen Cycle , 2001, Applied and Environmental Microbiology.

[18]  I. Anderson,et al.  Tracking the fate of a high concentration groundwater nitrate plume through a fringing marsh: A combined groundwater tracer and in situ isotope enrichment study , 2001 .

[19]  W. Silver,et al.  Dissimilatory nitrate reduction to ammonium in upland tropical forest soils , 2001 .

[20]  M. Bartoli,et al.  Denitrification in an intertidal seagrass meadow, a comparison of 15N-isotope and acetylene-block techniques: dissimilatory nitrate reduction to ammonia as a source of N2O? , 2001 .

[21]  M. Holmer,et al.  Sulphate reduction and sulphur cycling in lake sediments: a review , 2001 .

[22]  S. Hamilton,et al.  Control of Nitrogen Export from Watersheds by Headwater Streams , 2001, Science.

[23]  E. Roden,et al.  Microbially catalyzed nitrate-dependent oxidation of biogenic solid-phase Fe(II) compounds. , 2001, Environmental science & technology.

[24]  M. Jetten.  New pathways for ammonia conversion in soil and aquatic systems , 2001, Plant and Soil.

[25]  W. Wiseman,et al.  Hypoxia in the Gulf of Mexico. , 2001, Journal of environmental quality.

[26]  D. Kelly,et al.  Confirmation of Thiobacillus denitrificans as a species of the genus Thiobacillus, in the beta-subclass of the Proteobacteria, with strain NCIMB 9548 as the type strain. , 2000, International journal of systematic and evolutionary microbiology.

[27]  Gregory E. Schwarz,et al.  Effect of stream channel size on the delivery of nitrogen to the Gulf of Mexico , 2000, Nature.

[28]  L. Philippot,et al.  Dissimilatory nitrate reductases in bacteria. , 1999, Biochimica et biophysica acta.

[29]  Hans W. Paerl,et al.  Nitrogen, Carbon, and Sulfur Metabolism in NaturalThioploca Samples , 1999, Applied and Environmental Microbiology.

[30]  W. Kemp,et al.  Denitrification in coastal ecosystems: methods, environmental controls, and ecosystem level controls, a review , 1999, Aquatic Ecology.

[31]  J. G. Kuenen,et al.  The anaerobic oxidation of ammonium. , 1998, FEMS microbiology reviews.

[32]  K. Straub,et al.  Enumeration and Detection of Anaerobic Ferrous Iron-Oxidizing, Nitrate-Reducing Bacteria from Diverse European Sediments , 1998, Applied and Environmental Microbiology.

[33]  R. Laughlin,et al.  Dissimilatory nitrate reduction in anaerobic sediments leading to river nitrite accumulation , 1997, Applied and environmental microbiology.

[34]  S. Gerards,et al.  Effects of Nitrate Availability and the Presence of Glyceria maxima on the Composition and Activity of the Dissimilatory Nitrate-Reducing Bacterial Community , 1997, Applied and environmental microbiology.

[35]  L. J. Garcia-Gil,et al.  Sulfide-induced dissimilatory nitrate reduction to ammonia in anaerobic freshwater sediments , 1996 .

[36]  N. Risgaard-Petersen,et al.  Nitrification, denitrification, and nitrate ammonification in sediments of two coastal lagoons in Southern France , 1996, Hydrobiologia.

[37]  Dennis P. Swaney,et al.  Regional nitrogen budgets and riverine N & P fluxes for the drainages to the North Atlantic Ocean: Natural and human influences , 1996 .

[38]  H. Cypionka,et al.  Oxidation of H2, organic compounds and inorganic sulfur compounds coupled to reduction of O2 or nitrate by sulfate-reducing bacteria , 1992, Archives of Microbiology.

[39]  D. Postma,et al.  Nitrate Reduction in an Unconfined Sandy Aquifer: Water Chemistry, Reduction Processes, and Geochemical Modeling , 1991 .

[40]  H. Schmidt,et al.  Using isotope fractionation of nitrate-nitrogen and nitrate-oxygen for evaluation of microbial denitrification in a sandy aquifer , 1990 .

[41]  A. Zehnder.  Biology of anaerobic microorganisms , 1988 .

[42]  S. Seitzinger.  Denitrification in freshwater and coastal marine ecosystems: Ecological and geochemical significance , 1988 .

[43]  Jørgensen Bb.  Ecology of the bacteria of the sulphur cycle with special reference to anoxic-oxic interface environments. , 1982 .

[44]  R. Knowles.  Denitrification , 1982, Microbiological reviews.

[45]  E. Roden,et al.  Anaerobic redox cycling of iron by freshwater sediment microorganisms. , 2006, Environmental microbiology.

[46]  A. T. Hoor.  Cell yield and bioenergetics of Thiomicrospira denitrificans compared with Thiobacillus denitrificans , 2004, Antonie van Leeuwenhoek.

[47]  J. A. Robinson,et al.  Denitrification: ecological niches, competition and survival , 2004, Antonie van Leeuwenhoek.

[48]  Robin L. Dennis,et al.  Atmospheric deposition of nitrogen: Implications for nutrient over-enrichment of coastal waters , 2002 .

[49]  E. Davidson,et al.  Rapid abiotic transformation of nitrate in an acid forest soil , 2001 .

[50]  H. N. Schulz,et al.  Big bacteria. , 2001, Annual review of microbiology.

[51]  P. Bonin.  Anaerobic nitrate reduction to ammonium in two strains isolated from coastal marine sediment: A dissimilatory pathway , 1996 .

[52]  D. Canfield,et al.  Concentration and transport of nitrate by the mat-forming sulphur bacterium Thioploca , 1995, Nature.

[53]  I. Brettar,et al.  Denitrification in the Central Baltic: evidence for H2S-oxidation as motor of denitrification at the oxic-anoxic interface , 1991 .

[54]  W. Schlesinger.  Biogeochemistry: An Analysis of Global Change , 1991 .

[55]  B. Jørgensen.  Ecology of the bacteria of the sulphur cycle with special reference to anoxic-oxic interface environments. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[56]  A. Timer-ten Hoor.  Cell yield and bioenergetics of Thiomicrospira denitrificans compared with Thiobacillus denitrificans. , 1981, Antonie van Leeuwenhoek.