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Advances in understanding nitrogen flows and transformations: gaps and research pathways

Published online by Cambridge University Press:  19 September 2013

C. MÜLLER*
Affiliation:
School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland Department of Plant Ecology, Justus-Liebig-University Giessen, Heinrich-Buff-Ring 26, 35392 Giessen, Germany
T. J. CLOUGH
Affiliation:
Faculty of Agriculture and Life Sciences, Lincoln University, New Zealand
*
*To whom all correspondence should be addressed. Email: [email protected]

Summary

The nitrogen (N) cycle is one of the best studied elemental cycles. However, the N flows and transformations, in particular in aggregated soils, at small scales and in plant–soil systems are not yet fully understood. Analytical and molecular techniques are now available to address N dynamics at small scales. The methodological advances should go hand in hand with the development of suitable mathematical models addressing the small scale and the full complexity of the many interacting effects. The importance of denitrification within the N cycle is highlighted and used as an example of the progress achieved in recent times. Research gaps and possible research pathways are outlined.

Type
Nitrogen Workshop Special Issue Papers
Copyright
Copyright © Cambridge University Press 2013 

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References

Ackert, L. T. Jr. (2006). The role of microbes in agriculture: Sergei Vinogradskii's discovery and investigation of chemosynthesis, 1880–1910. Journal of the History of Biology 39, 373406.CrossRefGoogle Scholar
Andersen, K., Kjær, T. & Revsbech, N. P. (2001). An oxygen insensitive microsensor for nitrous oxide. Sensors and Actuators B: Chemical 81, 4248.CrossRefGoogle Scholar
Arah, J. & Smith, K. A. (1989). Steady-state denitrification in aggregated soils: a mathematical model. Journal of Soil Science 40, 139149.CrossRefGoogle Scholar
Arah, J. R. M. (1990 a). Diffusion–reaction models of denitrification in soil microsites. In Denitrification in Soil and Sediment (Eds Revsbech, N. P. & Sørensen, J.), pp. 245258. New York: Plenum Press.CrossRefGoogle Scholar
Arah, J. R. M. (1990 b). Modelling spatial and temporal variability of dentrification. Biology and Fertility of Soils 9, 7177.CrossRefGoogle Scholar
Aulie, R. P. (1970). Boussingault and the nitrogen cycle. Proceedings of the American Philosophical Society 114, 435479.Google Scholar
Barnard, R., Leadley, P. W., Lensi, R. & Barthes, L. (2005). Plant, soil microbial and soil inorganic nitrogen responses to elevated CO2: a study in microcosms of Holcus lanatus . Acta Oecologica 27, 171178.CrossRefGoogle Scholar
Barnosky, A. D., Hadly, E. A., Bascompte, J., Berlow, E. L., Brown, J. H., Fortelius, M., Getz, W. M., Harte, J., Hastings, A., Marquet, P. A., Martinez, N. D., Mooers, A., Roopnarine, P., Vermeij, G., Williams, J. W., Gillespie, R., Kitzes, J., Marshall, C., Matzke, N., Mindell, D. P., Revilla, E. & Smith, A. B. (2012). Approaching a state shift in Earth's biosphere. Nature 486, 5258.CrossRefGoogle ScholarPubMed
Beauchamp, E. G., Trevors, J. T. & Paul, J. W. (1989). Carbon sources for bacterial denitrification. Advances in Soil Science 10, 113142.CrossRefGoogle Scholar
Betlach, M. R. & Tiedje, J. M. (1981). Kinetic explanation for accumulation of nitrite, nitric oxide, and nitrous oxide during bacterial denitrification. Applied and Environmental Microbiology 42, 10741084.CrossRefGoogle ScholarPubMed
Bollmann, A. & Conrad, R. (1997). Acetylene blockage technique leads to underestimation of denitrification rates in oxic soils due to scavenging of intermediate nitric oxide. Soil Biology and Biochemistry 29, 10671077.CrossRefGoogle Scholar
Bouldin, D. R. (1961). Mathematical description of diffusion processes in the soil–plant system. Soil Science Society of America Journal 25, 476480.CrossRefGoogle Scholar
Bowman, R. A. & Focht, D. D. (1974). The influence of glucose and nitrate concentrations upon denitrification rates in sandy soils. Soil Biology and Biochemistry 6, 297301.CrossRefGoogle Scholar
Braker, G. & Conrad, R. (2011). Diversity, structure, and size of N2O-producing microbial communities in soils – What matters for their functioning? Advances in Applied Microbiology 75, 3370.CrossRefGoogle Scholar
Braker, G., Zhou, J., Wu, L., Devol, A. H. & Tiedje, J. M. (2000). Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in Pacific Northwest Marine Sediment Communities. Applied and Environmental Microbiology 66, 20962104.CrossRefGoogle ScholarPubMed
Bréal, E. (1892). De la prèsence, dans la paille, d'un ferment aérobie, réducteur des nitrates. Comptes Rendus hebdomadaires des Séance de l'Academie des Sciences (Paris) 114, 681684.Google Scholar
Brock, T. D. (1967). The ecosystem and the steady state. BioScience 17, 166169.CrossRefGoogle Scholar
Burford, J. R. & Bremner, J. M. (1975). Relationships between the denitrification capacities of soils and total, water-soluble and readily decomposable soil organic matter. Soil Biology and Biochemistry 7, 389394.CrossRefGoogle Scholar
Burford, J. R. & Stefanson, R. C. (1973). Measurements of gaseous losses of nitrogen from soils. Soil Biology and Biochemistry 5, 133141.CrossRefGoogle Scholar
Burger, M. & Jackson, L. E. (2005). Plant and microbial use and turnover: rapid conversion of nitrate to ammonium in soil with roots. Plant and Soil 266, 289301.CrossRefGoogle Scholar
Cabrera, M. L., Kissel, D. E. & Vigil, M. F. (2005). Nitrogen mineralization from organic residues: research opportunities. Journal of Environmental Quality 34, 7579.CrossRefGoogle ScholarPubMed
Cavigelli, M. A. & Robertson, G. P. (2000). The functional significance of denitrifier community composition in a terrestrial ecosystem. Ecology 81, 14021414.CrossRefGoogle Scholar
Chalk, P. M. & Smith, C. J. (1983). Chemodenitrification. In Gaseous Loss of Nitrogen from Plant Soil Systems (Eds Freney, J. R. & Simpson, J. R.), pp. 6589. Developments in Plant and Soil Sciences 9. Dordrecht: Martinus Nijhoff and Dr W Junk.CrossRefGoogle Scholar
Clément, J.-C., Shrestha, J., Ehrenfeld, J. G. & Jaffé, P. R. (2005). Ammonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils. Soil Biology and Biochemistry 37, 23232328.CrossRefGoogle Scholar
Clode, P. L., Kilburn, M. R., Jones, D. L., Stockdale, E. A., Cliff, J. B. III, Herrmann, A. M. & Murphy, D. V. (2009). In situ mapping of nutrient uptake in the rhizosphere using nanoscale secondary ion mass spectrometry. Plant Physiology 151, 17511757.CrossRefGoogle ScholarPubMed
Dassonville, F. & Renault, P. (2002). Interactions between microbial processes and geochemical transformations under anaerobic conditions: a review. Agronomie 22, 5168.CrossRefGoogle Scholar
Davidson, E. A. & Seitzinger, S. (2006). The enigma of progress in dentrification research. Ecological Applications 16, 20572063.CrossRefGoogle Scholar
Deangelis, K. M., Lindow, S. E. & Firestone, M. K. (2008). Bacterial quorum sensing and nitrogen cycling in rhizosphere soil. FEMS Microbiology Ecology 66, 197207.CrossRefGoogle ScholarPubMed
Dendooven, L. & Anderson, J. M. (1994). Dynamics of reduction enzymes involved in the denitrification process in pasture soil. Soil Biology and Biochemistry 26, 15011506.CrossRefGoogle Scholar
Dendooven, L., Splatt, P., Anderson, J. M. & Scholefield, D. (1994). Kinetics of the denitrification process in a soil under permanent pasture. Soil Biology and Biochemistry 26, 361370.CrossRefGoogle Scholar
Firestone, M. K. & Davidson, E. A. (1989). Microbiological basis of NO and N2O production and consumption in soil. In Exchange of Trace Gases between Terrestrial Ecosystems and the Atmosphere (Eds Andreae, M. O. & Schimel, D. S.), pp. 721. New York: John Wiley & Sons.Google Scholar
Focht, D. D. (1974). The effect of temperature, pH, and aeration on the production of nitrous oxide and gaseous nitrogen – a zero order kinetic model. Soil Science 118, 173179.CrossRefGoogle Scholar
Focht, D. D. & Verstraete, E. (1977). Biochemical ecology of nitrification and denitrification. In Advances in Microbial Ecology (Ed. Alexander, M.), pp. 135214. New York: Plenum Press.Google Scholar
Galloway, J. N. & Cowling, E. B. (2002). Reactive nitrogen and the world: 200 years of change. Ambio 31, 6471.CrossRefGoogle ScholarPubMed
Galloway, J. N., Dentener, F. J., Capone, D. G., Boyer, E. W., Howarth, R. W., Seitzinger, S. P., Asner, G. P., Cleveland, C. C., Green, P. A., Holland, E. A., Karl, D. M., Michaels, A. F., Porter, J. H., Townsend, A. R. & Vörösmarty, C. J. (2004). Nitrogen cycles: past, present, and future. Biogeochemistry 70, 153226.CrossRefGoogle Scholar
Galloway, J. N., Townsend, A. R., Erisman, J. W., Bekunda, M., Cai, Z., Freney, J. R., Martinelli, L. A., Seitzinger, S. P. & Sutton, M. A. (2008). Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889893.CrossRefGoogle ScholarPubMed
Greenwood, D. J. & Goodman, D. (1964). Oxygen diffusion and aerobic respiration in soil spheres. Journal of the Science of Food and Agriculture 15, 579588.CrossRefGoogle Scholar
Groffman, P. M. (1991). Ecology of nitrification and denitrification in soil evaluated at scales relevant to atmospheric chemistry. In Microbial Production and Consumption of Greenhouse Gases: Methane, Nitrogen Oxides and Halomethanes (Eds Rogers, J. E. & Whitman, W. B.), pp. 201217. Washington, DC: American Society for Microbiology.Google Scholar
Groffman, P. M., Tiedje, J. M., Robertson, G. P. & Christensen, S. (1988). Denitrification at different temporal and geographical scales: proximal and distal controls. In Advances in Nitrogen Cycling in Agricultural Ecosystems (Ed. Wilson, J. R.), pp. 174192. Wallingford: CAB International.Google Scholar
Groffman, P. M., Altabet, M. A., Böhlke, J. K., Butterbach-Bahl, K., David, M. B., Firestone, M. K., Giblin, A. E., Kana, T. M., Nielsen, L. P. & Voytek, M. A. (2006). Methods for measuring denitrification diverse approaches to a difficult problem. Ecological Applications 16, 20912122.CrossRefGoogle ScholarPubMed
Hall, E. K., Maixner, F., Franklin, O., Daims, H., Richter, A. & Battin, T. (2011). Linking microbial and ecosystem ecology using ecological stoichiometry: a synthesis of conceptual and empirical approaches. Ecosystems 14, 261273.CrossRefGoogle Scholar
Herrmann, A. M., Ritz, K., Nunan, N., Clode, P. L., Pett-Ridge, J., Kilburn, M. R., Murphy, D. V., O'donnell, A. G. & Stockdale, E. A. (2007). Nano-scale secondary ion mass spectrometry – a new analytical tool in biogeochemistry and soil ecology: a review article. Soil Biology and Biochemistry 39, 18351850.CrossRefGoogle Scholar
Inselsbacher, E., Öhlund, J., Jämtgard, S., Huss-Danell, K. & Näsholm, T. (2011). The potential of microdialysis to monitor organic and inorganic nitrogen compounds in soil. Soil Biology and Biochemistry 43, 13211332.CrossRefGoogle Scholar
Inselsbacher, E., Wanek, W., Strauss, J., Zechmeister-Boltenstern, S. & Müller, C. (2013). A novel 15N tracer model reveals: plant nitrate uptake governs nitrogen transformation rates in agricultural soils. Soil Biology and Biochemistry 57, 301310.CrossRefGoogle Scholar
Jones, D. L., Shannon, D., Murphy, D. V. & Farrar, J. (2004). Role of dissolved organic nitrogen (DON) in soil N cycling in grassland soils. Soil Biology and Biochemistry 36, 749756.CrossRefGoogle Scholar
Jørgensen, C. J., Struwe, S. & Elberling, B. (2012). Temporal trends in N2O flux dynamics in a Danish wetland – effects of plant-mediated gas transport of N2O and O2 following changes in water level and soil mineral-N availability. Global Change Biology 18, 210222.CrossRefGoogle Scholar
Knops, J. M. H., Bradley, K. L. & Wedin, D. A. (2002). Mechanisms of plant-species impacts on ecosystem nitrogen cycling. Ecology Letters 5, 454466.CrossRefGoogle Scholar
Knowles, R. (1982). Denitrification. Microbiological Reviews 46, 4370.CrossRefGoogle ScholarPubMed
Kool, D. M., Dolfing, J., Wrage, N. & Van Groenigen, J. W. (2011). Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil. Soil Biology and Biochemistry 43, 174178.CrossRefGoogle Scholar
Laudelout, H., Germain, L., Chabalier, P. F. & Chiang, C. N. (1977). Computer simulation of loss of fertilizer nitrogen through chemical decomposition of nitrite. Journal of Soil Science 28, 329339.CrossRefGoogle Scholar
Laughlin, R. J. & Stevens, R. J. (2002). Evidence for fungal dominance of denitrification and codenitrification in a grassland soil. Soil Science Society of America Journal 66, 15401548.CrossRefGoogle Scholar
Li, C., Frolking, S. & Frolking, T. A. (1992). A model of nitrous oxide evolution from soil driven by rainfall events: 1. model structure and sensitivity. Journal of Geophysical Research: Atmospheres 97, 97599776.CrossRefGoogle Scholar
Liu, B., Mørkved, P. T., Frostegård, Å. & Bakken, L. R. (2010). Denitrification gene pools, transcription and kinetics of NO, N2O and N2 productions affected by soil pH. FEMS Microbiology Ecology 72, 407417.CrossRefGoogle ScholarPubMed
Manzoni, S., Jackson, R. B., Trofymow, J. A. & Porporato, A. (2008). The global stoichiometry of litter nitrogen mineralization. Science 321, 684686.CrossRefGoogle ScholarPubMed
Mccarty, G. W. & Bremner, J. M. (1993). Factors affecting the availabiltiy of organic carbon for denitrification of nitrate in subsoils. Biology and Fertility of Soils 15, 132136.CrossRefGoogle Scholar
Mcconnaughey, P. K. & Bouldin, D. R. (1985). Transient microsite models of denitrification. I. Model development. Soil Science Society of America Journal 49, 886891.CrossRefGoogle Scholar
Mcelwain, D. L. S. (1978). A re-examination of oxygen diffusion in a spherical cell with Michaelis–Menten oxygen uptake kinetics. Journal of Theoretical Biology 71, 255263.CrossRefGoogle Scholar
Mclaren, A. D. (1970). Temporal and vectorial reactions of nitrogen in soil: a review. Canadian Journal of Soil Science 50, 97109.CrossRefGoogle Scholar
Meyer, R. L., Kjær, T. & Revsbech, N. P. (2002). Nitrification and denitrification near a soil–manure interface studied with a nitrate–nitrite biosensor. Soil Science Society of America Journal 66, 498506.CrossRefGoogle Scholar
Miller, M. N., Zebarth, B. J., Dandie, C. E., Burton, D. L., Goyer, C. & Trevors, J. T. (2009). Denitrifier community dynamics in soil aggregates under permanent grassland and arable cropping systems. Soil Science Society of America Journal 73, 18431851.CrossRefGoogle Scholar
Misra, C., Nielsen, D. R. & Biggar, J. W. (1974). Nitrogen transformations in soil during leaching. I. Theoretical considerations. Soil Science Society of America Proceedings 38, 289293.CrossRefGoogle Scholar
Molina, J. A. E., Clapp, C. E., Shaffer, M. J., Chichester, F. W. & Larson, W. E. (1983). NCSOIL, A model of nitrogen and carbon transformations in soil: description, calibration, and behavior. Soil Science Society of America Journal 47, 8591.CrossRefGoogle Scholar
Morley, N. & Baggs, E. M. (2010). Carbon and oxygen controls on N2O and N2 production during nitrate reduction. Soil Biology and Biochemistry 42, 18641871.CrossRefGoogle Scholar
Morozkina, E. V. & Kurakov, A. V. (2007). Dissimilatory nitrate reduction in fungi under conditions of hypoxia and anoxia: a review. Applied Biochemistry and Microbiology 43, 544549.CrossRefGoogle ScholarPubMed
Müller, C., Martin, M., Stevens, R. J., Laughlin, R. J., Kammann, C., Ottow, J. C. G. & Jäger, H.-J. (2002). Processes leading to N2O emissions in grassland soil during freezing and thawing. Soil Biology and Biochemistry 34, 13251331.CrossRefGoogle Scholar
Myrold, D. D. & Tiedje, J. M. (1985 a). Diffusional constraints on denitrification in soil. Soil Science Society of America Journal 49, 651657.CrossRefGoogle Scholar
Myrold, D. D. & Tiedje, J. M. (1985 b). Establishment of denitrification capacity in soil: effects of carbon, nitrate and moisture. Soil Biology and Biochemistry 17, 819822.CrossRefGoogle Scholar
Neumann, G., George, T. S. & Plassard, C. (2009). Strategies and methods for studying the rhizosphere – the plant science toolbox. Plant and Soil 321, 431456.CrossRefGoogle Scholar
Nõmmik, H. (1956). Investigations on denitrification in soil. Acta Agriculturae Scandinavica 6, 195228.CrossRefGoogle Scholar
Nunan, N., Wu, K., Young, I. M., Crawford, J. W. & Ritz, K. (2002). In situ spatial patterns of soil bacterial populations, mapped at multiple scales, in an arable soil. Microbial Ecology 44, 296305.CrossRefGoogle Scholar
Osler, G. H. R. & Sommerkorn, M. (2007). Toward a complete soil C and N cycle: incorporating the soil fauna. Ecology 88, 16111621.CrossRefGoogle Scholar
Parkin, T. B. (1987). Soil microsites as a source of denitrification variability. Soil Science Society of America Journal 51, 11941199.CrossRefGoogle Scholar
Parton, W., Silver, W. L., Burke, I. C., Grassens, L., Harmon, M. E., Currie, W. S., King, J. Y., Adair, E. C., Brandt, L. A., Hart, S. C. & Fasth, B. (2007). Global-scale similarities in nitrogen release patterns during long-term decomposition. Science 315, 361364.CrossRefGoogle ScholarPubMed
Parton, W. J., Schimel, D. S., Cole, C. V. & Ojima, D. S. (1987). Analysis of factors controlling soil organic matter levels in great plains grasslands. Soil Science Society of America Journal 51, 11731179.CrossRefGoogle Scholar
Philippot, L. (2005). Tracking nitrate reducers and denitrifiers in the environment. Biochemical Society Transactions 33, 200204.CrossRefGoogle ScholarPubMed
Philippot, L., Čuhel, J., Saby, N. P. A., Chèneby, D., Chroňáková, A., Bru, D., Arrouays, D., Martin-Laurent, F. & Šimek, M. (2009). Mapping field-scale spatial patterns of size and activity of the denitrifier community. Environmental Microbiology 11, 15181526.CrossRefGoogle ScholarPubMed
Philippot, L., Andert, J., Jones, C. M., Bru, D. & Hallin, S. (2011). Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil. Global Change Biology 17, 14971504.CrossRefGoogle Scholar
Rastetter, E. B., Ågren, G. I. & Shaver, G. R. (1997). Responses of N-limited ecosystems to increased CO2: a balanced-nutrition, coupled-element-cycles model. Ecological Applications 7, 444460.Google Scholar
Robertson, L. A. & Kuenen, J. G. (1990). Physiological and ecological aspects of aerobic denitrification. In Denitrification in Soil and Sediment (Eds Revsbech, N. P. & Sørensen, J.), pp. 91104. New York: Plenum Press.CrossRefGoogle Scholar
Rütting, T. & Müller, C. (2008). Process-specific analysis of nitrite dynamics in a permanent grassland soil by using a Monte Carlo sampling technique. European Journal of Soil Science 59, 208215.CrossRefGoogle Scholar
Rütting, T., Boeckx, P., Müller, C. & Klemedtsson, L. (2011). Assessment of the importance of dissimilatory nitrate reduction to ammonium for the terrestrial nitrogen cycle. Biogeosciences 8, 17791791.CrossRefGoogle Scholar
Sanderman, J. & Amundson, R. (2003). Biogeochemistry of decomposition and detrital processing. In Biogeochemistry (Ed. Schlesinger, W. H.), pp. 249316. Treatise on Geochemistry vol. 8. Amsterdam: Elsevier.Google Scholar
Schimel, J. P. & Bennett, J. (2004). Nitrogen mineralization: challenges of a changing paradigm. Ecology 85, 591602.CrossRefGoogle Scholar
Sexstone, A. J., Revsbech, N. P., Parkin, T. B. & Tiedje, J. M. (1985). Direct measurement of oxygen profiles and denitrification rates in soil aggregates. Soil Science Society of America Journal 49, 645651.CrossRefGoogle Scholar
Šimek, M. & Cooper, J. E. (2002). The influence of soil pH on denitrification: progress towards the understanding of this interaction over the last 50 years. European Journal of Soil Science 53, 345354.CrossRefGoogle Scholar
Spott, O., Russow, R. & Stange, C. F. (2011). Formation of hybrid N2O and hybrid N2 due to codenitrification: first review of a barely considered process of microbially mediated N-nitrosation. Soil Biology and Biochemistry 43, 19952011.CrossRefGoogle Scholar
Stevens, R. J., Laughlin, R. J. & Malone, J. P. (1998). Soil pH affects the processes reducing nitrate to nitrous oxide and di-nitrogen. Soil Biology and Biochemistry 30, 11191126.CrossRefGoogle Scholar
Stockmann, U., Adams, M. A., Crawford, J. W., Field, D. J., Henakaarchchia, N., Jenkins, M., Minasny, B., Mcbratney, A. B., De Remy De Courcelles, V., Singh, K., Wheeler, I., Abbott, L., Angers, D. A., Baldock, J., Bird, M., Brookes, B. C., Chenu, C., Jastrow, J. D., Lal, R., Lehmann, J., O'donnell, A. G., Parton, W. J., Whitehead, D. & Zimmermann, M. (2013). The knowns, known unknowns and unknowns of sequestration of soil organic carbon. Agriculture, Ecosystems and Environment 164, 8099.CrossRefGoogle Scholar
Tiedje, J. M. (1988). Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In Biology of Anaerobic Microorganisms (Ed. Zehnder, A. J. B.), pp. 179244. New York: John Wiley & Sons.Google Scholar
Uchida, Y., Clough, T. J., Kelliher, F. M., Hunt, J. E. & Sherlock, R. R. (2011). Effects of bovine urine, plants and temperature on N2O and CO2 emissions from a sub-tropical soil. Plant and Soil 345, 171186.CrossRefGoogle Scholar
Van Der Ploeg, R. R., Böhm, W. & Kirkham, M. B. (1999). On the origin of the theory of mineral nutrition of plants and the law of the minimum. Soil Science Society of America Journal 63, 10551062.CrossRefGoogle Scholar
Van Kessel, C., Clough, T. J. & Van Groenigen, J. W. (2009). Dissolved organic nitrogen: an overlooked pathway of nitrogen loss from agricultural systems? Journal of Environmental Quality 38, 393401.CrossRefGoogle ScholarPubMed
Vogel, H.-J., Weller, U. & Schlüter, S. (2010). Quantification of soil structure based on Minkowski functions. Computers and Geosciences 36, 12361245.CrossRefGoogle Scholar
Wildenschild, D., Hopmans, J. W., Vaz, C. M. P., Rivers, M. L., Rikard, D. & Christensen, B. S. B. (2002). Using X-ray computed tomography in hydrology: systems, resolutions, and limitations. Journal of Hydrology 267, 285297.CrossRefGoogle Scholar
Wrage, N., Velthof, G. L., Van Beusichem, M. L. & Oenema, O. (2001). Role of nitrifier denitrification in the production of nitrous oxide. Soil Biology and Biochemistry 33, 17231732.CrossRefGoogle Scholar
Zak, D. R., Holmes, W. E., White, D. C., Peacock, A. D. & Tilman, D. (2003). Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84, 20422050.CrossRefGoogle Scholar
Zumft, W. G. (1997). Cell biology and molecular basis of denitrification. Microbiology and Molecular Biology Reviews 61, 533616.Google ScholarPubMed