Abstract
Purpose
The responses of nitrification and denitrification are not well characterised at temperatures above 35 °C, which is the focus of our study.
Materials and methods
Soils collected from two dairy pastures (Victoria, Australia) were incubated at 10 to 45 °C in the dark for 5 to 10 days following amendment with 100 μg N g−1 either as NH4NO3, 14NH415NO3 or 15NH415NO3 (10 atom% 15N excess) at 50% water-filled pore space. To detect N2O from heterotrophic nitrification, acetylene (0.01% v/v) was used in a subset of samples amended with 15NH415NO3. Atom% 15N enrichments of NO3ˉ, N2O and N2 were measured during the experiment to evaluate the responses of nitrification and denitrification to temperature.
Results and discussion
N2O production from the two soils increased with rising temperature and peaked between 35 and 40 °C. N2O production from nitrification and denitrification both had similar thermal responses, which were different to N2 production. The N2O/N2 ratio decreased from > 4 at 35–40 °C to 0.5 at 45 °C, due to greater N2 than N2O production in the Dermosol. Heterotrophic nitrifiers oxidised NH4+ and released N2O at 35–40 °C, suggesting a role for heterotrophs in N cycling under warm climates. Topt for nitrification was between 35 and 40 °C, which is higher than reported previously. A short-term effect of high temperatures could provide NH4+ for the growth of crops but may also decrease soil C pools.
Conclusions
Increasing temperature above 35 °C altered the rates of nitrification, denitrification associated N2O and N2 production. Nitrification and denitrification peaked at 35–40 °C in the Chromosol and Dermosol. The production of N2 increased rapidly above 40 °C, which may be related to high soil respiration rates that likely decreased O2 availability, thus expanding the anaerobic microsites; such circumstances increased the reduction of N2O to N2 production from the Dermosol.
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References
Ambus P (2005) Relationship between gross nitrogen cycling and nitrous oxide emission in grass-clover pasture. Nutr Cycl Agroecosyst 72:189–199
Anderson OE, Boswell F, Harrison RM (1971) Variations in low temperature adaptability of nitrifiers in acid soils 1. Soil Sci Soc Am J 35:68–71
Avalakki U, Strong W, Saffigna P (1995) Measurement of gaseous emissions from denitrification of applied 15N2. Effects of temperature and added straw. Soil Res 33:89–99
Avrahami S, Liesack W, Conrad R (2003) Effects of temperature and fertilizer on activity and community structure of soil ammonia oxidizers. Environ Microbiol 5:691–705
Bateman E, Baggs E (2005) Contributions of nitrification and denitrification to N2O emissions from soils at different water-filled pore space. Biol Fertil Soils 41:379–388
Bremner JM (1997) Sources of nitrous oxide in soils. Nutr Cycl Agroecosyst 49:7–16
Bremner J, Blackmer A (1979) Effects of acetylene and soil water content on emission of nitrous oxide from soils. Nature 280:380–381
Breuer L, Butterbach-Bahl K (2005) Local temperature optimum of N2O production rates in tropical rain forest soils of Australia. Soil Res 43:689–694
Bronson KF, Sparling GP, Fillery IR (1999) Short-term N dynamics following application of 15N-labeled urine to a sandy soil in summer. Soil Biol Biochem 31:1049–1057
Brooks P, Stark JM, McInteer B, Preston T (1989) Diffusion method to prepare soil extracts for automated nitrogen-15 analysis. Soil Sci Soc Am J 53:1707–1711
Carter MS (2007) Contribution of nitrification and denitrification to N2O emissions from urine patches. Soil Biol Biochem 39:2091–2102
Chen D, Suter HC, Islam A, Edis R (2010) Influence of nitrification inhibitors on nitrification and nitrous oxide (N2O) emission from a clay loam soil fertilized with urea. Soil Biol Biochem 42:660–664
Cheng W, Tsuruta H, Chen G, Yagi K (2004) N2O and NO production in various Chinese agricultural soils by nitrification. Soil Biol Biochem 36:953–963
Cho C, Burton D, Chang C (1997) Kinetic formulation of oxygen consumption and denitrification processes in soil. Can J Soil Sci 77:253–260
Conant RT, Ryan MG, Ågren GI, Birge HE, Davidson EA, Eliasson PE, Evans SE, Frey SD, Giardina CP, Hopkins FM, Hyvönen R, Kirschbaum MUF, Lavallee JM, Leifeld J, Parton WJ, Megan Steinweg J, Wallenstein MD, Martin Wetterstedt JÅ, Bradford MA (2011) Temperature and soil organic matter decomposition rates–synthesis of current knowledge and a way forward. Glob Chang Biol 17:3392–3404
Crutzen P (1983) Atmospheric interactions. Homogeneous gas reactions of C, N, and S containing compounds. In: Bolin B, Cook R (eds) The major biogeochemical cycles and their interactions, vol SCOPE 21. Wiley, pp 67–114
Davidson EA (1991) Fluxes of nitrous oxide and nitric oxide from terrestrial ecosystems. In: Rogers JE, Whitman BW (eds) Microbial production and consumption of greenhouse gases: methane, nitrogen oxides and halomethanes. Am. Soc. Microbiol, Washington, DC, pp 219–235
Davidson E, Hart S, Shanks C, Firestone M (1991) Measuring gross nitrogen mineralization, and nitrification by 15N isotopic pool dilution in intact soil cores. J Soil Sci 42:335–349
Dobbie K, Smith K (2001) The effects of temperature, water-filled pore space and land use on N2O emissions from an imperfectly drained gleysol. Eur J Soil Sci 52:667–673
Duan P, Wu Z, Zhang Q, Fan C, Xiong Z (2018) Thermodynamic responses of ammonia-oxidizing archaea and bacteria explain N2O production from greenhouse vegetable soils. Soil Biol Biochem 120:37–47
Focht D (1974) The effect of temperature, pH, and aeration on the production of nitrous oxide and gaseous nitrogen—a zero-order kinetic model. Soil Sci 118:173–179
Frame CH, Casciotti K (2010) Biogeochemical controls and isotopic signatures of nitrous oxide production by a marine ammonia-oxidizing bacterium. Biogeosciences 7:2695–2709
Galbally IE, Meyer MC, Wang Y-P, Smith CJ, Weeks IA (2010) Nitrous oxide emissions from a legume pasture and the influences of liming and urine addition. Agric Ecosyst Environ 136:262–272
Garrido F, Hénault C, Gaillard H, Perez S, Germon J (2002) N2O and NO emissions by agricultural soils with low hydraulic potentials. Soil Biol Biochem 34:559–575
Gillam K, Zebarth B, Burton D (2008) Nitrous oxide emissions from denitrification and the partitioning of gaseous losses as affected by nitrate and carbon addition and soil aeration. Can J Soil Sci 88:133–143
Global Temperature (2018). In: Global Climate Change. NASA. Available via https://climate.nasa.gov/Global Temperature. Accessed 15 April 2018
Gödde M, Conrad R (1999) Immediate and adaptational temperature effects on nitric oxide production and nitrous oxide release from nitrification and denitrification in two soils. Biol Fertil Soils 30:33–40
Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research. Wiley, Hoboken
Goodroad L, Keeney D (1984) Nitrous oxide production in aerobic soils under varying pH, temperature and water content. Soil Biol Biochem 16:39–43
Groffman PM, Altabet MA, Böhlke JK, Butterbach-Bahl K, David MB, Firestone MK, Giblin AE, Kana TM, Nielsen LP, Voytek MA (2006) Methods for measuring denitrification: diverse approaches to a difficult problem. Ecol Appl 16:2091–2122
Haynes R (1986) Niitrification. In: Haynes R (ed) Mineral nitrogen in the plant-soil system. Academic, London, pp 127–165
Heil J, Liu S, Vereecken H, Brüggemann N (2015) Abiotic nitrous oxide production from hydroxylamine in soils and their dependence on soil properties. Soil Biol Biochem 84:107–115
Hink L, Gubry-Rangin C, Nicol GW, Prosser JI (2018) The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions. ISME J 12:1084
Ingwersen J, Butterbach-Bahl K, Gasche R, Papen H, Richter O (1999) Barometric process separation: new method for quantifying nitrification, denitrification, and nitrous oxide sources in soils. Soil Sci Soc Am J 63:117–128
Isbell R (1996) The Australian soil classification. In: Australian soil and land survey handbook, vol 4. CSIRO, Melbourne
Islam A, Chen D, White R (2007) Heterotrophic and autotrophic nitrification in two acid pasture soils. Soil Biol Biochem 39:972–975
Jones L, Peters B, Lezama J, Casciotti K, Fendorf S (2013) Emission of the greenhouse gas nitrous oxide resulting from ferrous iron disturbance of denitrification. In: AGU Fall Meeting Abstracts, p 0413
Kamphake L, Hannah S, Cohen J (1967) Automated analysis for nitrate by hydrazine reduction. Water Res 1:205–216
Kaplan A (1965) Standard methods of clinical chemistry. Academic, New York
Keeney D, Marx G, Fillery I (1979) Effect of temperature on the gaseous nitrogen products of denitrification in a silt loam soil. Soil Sci Soc Am J 43:1124–1128
Khalil K, Mary B, Renault P (2004) Nitrous oxide production by nitrification and denitrification in soil aggregates as affected by O2 concentration. Soil Biol Biochem 36:687–699
Kirkham D, Bartholomew W (1954) Equations for following nutrient transformations in soil, utilizing tracer data. Soil Sci Soc Am J 18:33–34
Kirschbaum MU (1993) A modelling study of the effects of changes in atmospheric CO2 concentration, temperature and atmospheric nitrogen input on soil organic carbon storage. Tellus Ser B Chem Phys Meteorol 45:321–334
Kirschbaum MU (1995) The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic C storage. Soil Biol Biochem 27:753–760
Klemedtsson L, Svensson B, Rosswall T (1988) A method of selective inhibition to distinguish between nitrification and denitrification as sources of nitrous oxide in soil. Biol Fertil Soils 6:112–119
Knowles R (1990) Acetylene inhibition technique: development, advantages, and potential problems. In: Denitrification in soil and sediment. Springer, Berlin, pp 151–166
Lai TV, Denton MD (2018) N2O and N2 emissions from denitrification respond differently to temperature and nitrogen supply. J Soils Sediments 18:1548–1557
Liu R, Suter H, He J, Hayden H, Chen D (2015) Influence of temperature and moisture on the relative contributions of heterotrophic and autotrophic nitrification to gross nitrification in an acid cropping soil. J Soils Sediments 15:2304–2309
Liu R et al (2016) The effect of temperature and moisture on the source of N2O and contributions from ammonia oxidizers in an agricultural soil. Biol Fertil Soils 53:141–152
Maag M, Vinther FP (1996) Nitrous oxide emission by nitrification and denitrification in different soil types and at different soil moisture contents and temperatures. Appl Soil Ecol 4:5–14
Malhi S, McGill W (1982) Nitrification in three Alberta soils: effect of temperature, moisture and substrate concentration. Soil Biol Biochem 14:393–399
Malhi S, McGill W, Nyborg M (1990) Nitrate losses in soils: effect of temperature, moisture and substrate concentration. Soil Biol Biochem 22:733–737
Malone J, Stevens R, Laughlin R (1998) Combining the 15N and acetylene inhibition techniques to examine the effect of acetylene on denitrification. Soil Biol Biochem 30:31–37
Martikainen PJ, Lehtonen M, Lång K, De Boer W, Ferm A (1993) Nitrification and nitrous oxide production potentials in aerobic soil samples from the soil profile of a Finnish coniferous site receiving high ammonium deposition. FEMS Microbiol Ecol 13:113–121
Mathieu O, Hénault C, Lévêque J, Baujard E, Milloux M-J, Andreux F (2006) Quantifying the contribution of nitrification and denitrification to the nitrous oxide flux using 15N tracers. Environ Pollut 144:933–940
Mørkved PT, Dörsch P, Henriksen TM, Bakken LR (2006) N2O emissions and product ratios of nitrification and denitrification as affected by freezing and thawing. Soil Biol Biochem 38:3411–3420
Mørkved PT, Dörsch P, Bakken LR (2007) The N2O product ratio of nitrification and its dependence on long-term changes in soil pH. Soil Biol Biochem 39:2048–2057
Mosier A (1980) Acetylene inhibition of ammonium oxidation in soil. Soil Biol Biochem 12:443–444
Myers R (1975) Temperature effects on ammonification and nitrification in a tropical soil. Soil Biol Biochem 7:83–86
Ouyang Y, Norton JM, Stark JM (2017) Ammonium availability and temperature control contributions of ammonia oxidizing bacteria and archaea to nitrification in an agricultural soil. Soil Biol Biochem 113:161–172
Parton W et al (2001) Generalized model for NOx and N2O emissions from soils. J Geophys Res-Atmos 106:17403–17419
Pierzynski GM, Vance GF, Sims JT (2005) Soils and environmental quality. CRC Press, Taylor & Francis Group
Powlson D, Saffigna P, Kragt-Cottaar M (1988) Denitrification at sub-optimal temperatures in soils from different climatic zones. Soil Biol Biochem 20:719–723
Ravishankara A, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125
Rudaz A, Wälti E, Kyburz G, Lehmann P, Fuhrer J (1999) Temporal variation in N2O and N2 fluxes from a permanent pasture in Switzerland in relation to management, soil water content and soil temperature. Agric Ecosyst Environ 73:83–91
Sabey BR, Frederick LR, Bartholomew WV (1959) The formation of nitrate from ammounium in soils. III. Influence of temperature and initial population of nitrifying organisms on the maximum rate and delay period. Proc Soil Sci Soc Am 23
Schimel JP, Firestone MK, Killham KS (1984) Identification of heterotrophic nitrification in a Sierran forest soil. Appl Environ Microbiol 48:802–806
Schlesinger WH, Andrews JA (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20
Schmidt EL (1982) Nitrification in soil. In: Stevenson F (ed) Nitrogen in agricultural soil, vol 22. American Soc. Agronomy, Madison, pp 253–267
Schmidt I (2009) Chemoorganoheterotrophic growth of Nitrosomonas europaea and Nitrosomonas eutropha. Curr Microbiol 59:130–138
Sierra J, Marban L (2000) Nitrogen mineralization pattern of an oxisol of Guadeloupe, French West Indies. Soil Sci Soc Am J 64:2002–2010
Stark JM (1996) Modeling the temperature response of nitrification. Biogeochemistry 35:433–445
Stark JM, Firestone MK (1996) Kinetic characteristics of ammonium-oxidizer communities in a California oak woodland-annual grassland. Soil Biol Biochem 28:1307–1317
Stevens R, Laughlin R (1998) Measurement of nitrous oxide and di-nitrogen emissions from agricultural soils. Nutr Cycl Agroecosyst 52:131–139
Stevens R, Laughlin R, Atkins G, Prosser S (1993) Automated determination of nitrogen-15-labeled dinitrogen and nitrous oxide by mass spectrometry. Soil Sci Soc Am J 57:981–988
Strong D, Fillery I (2002) Denitrification response to nitrate concentrations in sandy soils. Soil Biol Biochem 34:945–954
Taylor AE, Giguere AT, Zoebelein CM, Myrold DD, Bottomley PJ (2017) Modeling of soil nitrification responses to temperature reveals thermodynamic differences between ammonia-oxidizing activity of archaea and bacteria. ISME J 11:896–908
Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (ed) Environmental microbiology of anaerobes, vol 717. Wiley, New York, pp 179–244
Tortoso AC, Hutchinson G (1990) Contributions of autotrophic and heterotrophic nitrifiers to soil NO and N2O emissions. Appl Environ Microbiol 56:1799–1805
Wrage N, Velthof G, Van Beusichem M, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33:1723–1732
Wrage N, Groenigen JW, Oenema O, Baggs E (2005) A novel dual-isotope labelling method for distinguishing between soil sources of N2O. Rapid Commun Mass Spectrom 19:3298–3306
Yoshinari T, Hynes R, Knowles R (1977) Acetylene inhibition of nitrous oxide reduction and measurement of denitrification and nitrogen fixation in soil. Soil Biol Biochem 9:177–183
Yu K, Seo DC, DeLaune RD (2010a) Incomplete acetylene inhibition of nitrous oxide reduction in potential denitrification assay as revealed by using 15N-nitrate tracer. Commun Soil Sci Plant Anal 41:2201–2210
Yu R, Kampschreur MJ, MCv L, Chandran K (2010b) Mechanisms and specific directionality of autotrophic nitrous oxide and nitric oxide generation during transient anoxia. Environ Sci Technol 44:1313–1319
Zaman M, Chang S (2004) Substrate type, temperature, and moisture content affect gross and net N mineralization and nitrification rates in agroforestry systems. Biol Fertil Soils 39:269–279
Zhu X, Burger M, Doane TA, Horwath WR (2013) Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability. Proc Natl Acad Sci 110:6328–6333
Acknowledgements
This study was assisted through funding from the Vietnam International Education Development (VIED), The University of Adelaide and Tim Healy Memorial Scholarship (Future Farm Industries CRC). We acknowledge the assistance of Murray Unkovich (University of Adelaide), Nanthi Bolan (University of Newcastle) in assistance with methods, Kevin Kelly (Department of Economic Development, VIC, Australia) in providing site access for soil collection and environmental data, Nigel Charman for assistance with soil sampling and Ann McNeill and Nang Nguyen for technical assistance with mineral nitrogen analysis and soil physical measurements.
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Lai, T.V., Farquharson, R. & Denton, M.D. High soil temperatures alter the rates of nitrification, denitrification and associated N2O emissions. J Soils Sediments 19, 2176–2189 (2019). https://doi.org/10.1007/s11368-018-02238-7
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DOI: https://doi.org/10.1007/s11368-018-02238-7