Abstract
In recent years, identification of the microbial sources responsible for soil N2O production has substantially advanced with the development of isotope enrichment techniques, selective inhibitors, mathematical models and the discoveries of specific N-cycling functional genes. However, little information is available to effectively quantify the N2O produced from different microbial pathways (e.g. nitrification and denitrification). Here, a 15N-tracing incubation experiment was conducted under controlled laboratory conditions (50, 70 and 85% water-filled pore space (WFPS) at 25 and 35 °C). Nitrification was the main contributor to N2O production. At 50, 70 and 85% WFPS, nitrification contributed 87, 80 and 53% of total N2O production, respectively, at 25 °C, and 86, 74 and 33% at 35 °C. The proportion of nitrified N as N2O (P N2O) increased with temperature and moisture, except for 85% WFPS, when P N2O was lower at 35 °C than at 25 °C. Ammonia-oxidizing archaea (AOA) were the dominant ammonia oxidizers, but both AOA and ammonia-oxidizing bacteria (AOB) were related to N2O emitted from nitrification. AOA and AOB abundance was significantly influenced by soil moisture, more so than temperature, and decreased with increasing moisture content. These findings can be used to develop better models for simulating N2O from nitrification to inform soil management practises for improving N use efficiency.
Similar content being viewed by others
References
Akiyama H, Morimoto S, Tago K, Hoshino YT, Nagaoka K, Yamasaki M, Karasawa T, Takenaka M, Hayatsu M (2014) Relationships between ammonia oxidizers and N2O and CH4 fluxes in agricultural fields with different soil types. Soil Sci Plant Nutri 60:520–529
Allen D, Kingston G, Rennenberg H, Dalal RC, Schmidt S (2010) Effect of nitrogen fertilizer management and waterlogging on nitrous oxide emission from subtropical sugarcane soils. Agric Ecosyst Environ 136:209–217
Andert J, Wessén E, Börjesson G, Hallin S (2011) Temporal changes in abundance and composition of ammonia-oxidizing bacterial and archaeal communities in a drained peat soil in relation to N2O emissions. J Soils Sediments 11:1399–1407
Avrahami S, Bohannan BJM (2009) N2O emission rates in a California meadow soil are influenced by fertilizer level, soil moisture and the community structure of ammonia-oxidizing bacteria. Glob Chang Biol 15:643–655
Barraclough D, Puri G (1995) The use of 15N pool dilution and enrichment to separate the heterotrophic and autotrophic pathways of nitrification. Soil Biol Biochem 27:17–22
Bateman EJ, Baggs EM (2005) Contributions of nitrification and denitrification to N2O emission from soils at different water-filled pore space. Biol Fertil Soils 41:379–388
Belser LW (1979) Population ecology of nitrifying bacteria. Annu Rev Microbiol 33:309–333
Braker G, Conrad R (2011) Diversity, structure, and size of N2O producing microbial communities in soils—what matters for their functioning? Adv Appl Microbiol 75:33–70
Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic crenarchaeota: proposal for a third archaeal phylum, the thaumarchaeota. Nat Rev Microbiol 6:245–252
Butterbach-Bahl K, Baggs EM, Dannenmann M, Kiese R, Zechmeister-Boltenstern S (2013) Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philos Trans R Soc B 368:20130122
Cheng Y, Wang J, Wang SQ, Zhang JB, Cai ZC (2014) Effects of soil moisture on gross N transformations and N2O emission in acid subtropical forest soils. Biol Fertil Soils 50:1099–1108
Ciarlo E, Conti M, Bartoloni N, Rubio G (2008) Soil N2O emissions and N2O/(N2O + N2) ratio as affected by different fertilization practices and soil moisture. Biol Fertil Soils 44:991–995
Colbourn P, Dowdell RJ (1984) Dnitrification in field soils. Plant Soil 76:213–226
Dalal RC, Wang W, Robertson GP, Parton WJ (2003) Nitrous oxide emission from Australian agricultural lands and mitigation options: a review. Soil Res 41:165–195
Davidson EA (1992) Sources of nitric oxide and nitrous oxide following wetting of dry soil. Soil Sci Soc Am J 56:95–102
Di HJ, Cameron KC, Shen JP, Winefield C, O’Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624
Di HJ, Cameron KC, Sherlock RR, Shen JP, He JZ, Winefield C (2010) Nitrous oxide emissions from grazed grassland as affected by a nitrification inhibitor, dicyandiamide, and relationships with ammonia-oxidizing bacteria and archaea. J Soils Sediments 10:943–954
Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci U S A 102:14683–14688
Friedl J, Scheer C, Rowlings DW, McIntosh HV, Strazzabosco A, Warner DI, Grace PR (2016) Denitrification losses from an intensively managed sub-tropical pasture—impact of soil moisture on the partitioning of N2 and N2O emissions. Soil Biol Biochem 92:58–66
Garrido F, Henault C, Gaillard H, Perez S, Germon JC (2002) N2O and NO emissions by agricultural soils with low hydraulic potentials. Soil Biol Biochem 34:559–575
Godde 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
Goodroad L, Keeney D (1984) Nitrous oxide production in aerobic soils under varying pH, temperature and water content. Soil Biol Biochem 16:39–43
Granli T, Bøeckman OC (1994) Nitrous oxide from agriculture. Nor J Agric Sci 12:128
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9
Harris RH, Officer SJ, Hill PA, Armstrong RD, Fogarty KM, Zollinger RP, Phelan AJ, Partington DL (2013) Can nitrogen fertiliser and nitrification inhibitor management influence N2O losses from high rainfall cropping systems in South Eastern Australia? Nutri Cycl Agroecosyst 95:269–285
Hastings R, Butler C, Singleton I, Saunders J, McCarthy A (2000) Analysis of ammonia-oxidizing bacteria populations in acidic forest soil during conditions of moisture limitation. Lett Appl Microbiol 30:14–18
Haynes R (1986) Nitrification. In: Haynes RS (ed) Mineral nitrogen in the plant-soil system. Academic Press, London, pp. 127–165
Hermansson A, Lindgren PE (2001) Quantification of ammonia-oxidizing bacteria in arable soil by real-time PCR. Appl Environ Microbiol 67:972–976
Hink L, Nicol GW, Prosser JI (2016) Archaea produce lower yields of N2O than bacteria during aerobic ammonia oxidation in soil. Environ Microbiol. doi:10.1111/1462-2920.13282
Hofstra N, Bouwman AF (2005) Denitrification in agricultural soils: summarizing published data and estimating global annual rates. Nutri Cycl Agroecosyst 72:267–278
Horz HP, Barbrook A, Field CB, Bohannan BJM (2004) Ammonia-oxidizing bacteria respond to multifactorial global change. Proc Natl Acad Sci U S A 101:15136–15141
Hu HW, Macdonald CA, Trivedi P (2014) Water addition regulates the metabolic activity of ammonia oxidizers responding to environmental perturbations in dry sub-humid ecosystems. Environ Microbiol 17:444–461
Hu HW, Chen DL, He JZ (2015) Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiol Rev. doi:10.1093/femsre/fuv021
Huang Y, Zou J, Zheng X, Wang Y, Xu X (2004) Nitrous oxide emissions as influenced by amendment of plant residues with different C:N ratios. Soil Biol Biochem 36:973–981
Huang T, Gao B, Hu XK (2014) Ammonia-oxidation as an engine to generate nitrous oxide in an intensively managed calcareous Fluvo-aquic soil. Sci Rep 4:3950
IPCC (2007) Climate change 2007: the physical science basis. In: Solomon S, Qin D, Manning M (eds) Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
Isbell RF (1996) The Australian Soil Classification, Revised Ed (CSIRO Publishing: Melbourne) http://www.publish.csiro.au/pid/3529.htm
Jia Z, Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671
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 WV (1954) Equations for following nutrient transformations in soil utilizing tracer data. Soil Sci Soc Am J 18:33–34
Kool DM, Wrage N, Zechmeister-Boltenstern S (2010) Nitrifier denitrification can be a source of N2O from soil: a revised approach to the dual-isotope labelling method. Eur J Soil Sci 61:759–772
Kool DM, Dolfing J, Wrage N (2011) Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil. Soil Biol Biochem 43:174–178
Lan T, Han Y, Roelcke M, Nieder R, Cai ZC (2013) Processes leading to N2O and NO emissions from two different Chinese soils under different soil moisture contents. Plant Soil 371:611–627
Lang M, Cai Z, Chang SX (2011) Effects of land use type and incubation temperature on greenhouse gas emissions from Chinese and Canadian soils. J Soils Sediments 11:15–24
Leininger S, Urich T, Schloter M, Schwzrk L, Qi J, Nicol G, Prosser J, Schuster S, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809
Li P, Lang M (2014) Gross nitrogen transformations and related N2O emissions in uncultivated and cultivated black soil. Biol Fertil Soils 50:197–206
Li C, Aber J, Stange F, Butterbach-Bahl K, Papen H (2000) A process-oriented model of N2O and NO emissions from forest soils: 1. Model development J Geophys Res 105:4369–4384
Liu R, Hu HW, Suter H, Hayden HL, He JZ, Mele P, Chen DL (2016) Nitrification is a primary driver of nitrous oxide production in laboratory microcosms from different land-use soils. Front Microbiol 7:1373
Livesley S, Kiese R, Graham J, Weston C, Butterbach-Bahl K, Arndt S (2008) Trace gas flux and the influence of short-term soil water and temperature dynamics in Australian sheep grazed pastures of differing productivity. Plant Soil 309:89–103
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
Mathieu O, Hénault C, Lévêque J, Baujard E, Milloux MJ, Andreux F (2006) Quantifying the contribution of nitrification and denitrification to the nitrous oxide flux using 15N tracers. Environ Pollut 144:933–940
Mendum T, Sockett R, Hirsch P (1999) Use of molecular and isotopic techniques to monitor the response of autotrophic ammonia-oxidizing populations of the beta subdivision of the class proteobacteria in arable soils to nitrogen fertilizer. Appl Environ Microbiol 65:4155–4162
Mertens J, Broos K, Wakelin SA, Kowalchuk GA, Springael D, Smolders E (2009) Bacteria, not archaea, restore nitrification in a zinc-contaminated soil. ISME J 3:916–923
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
Müller C, Laughlin RJ, Spott O, Rütting T (2014) Quantification of N2O emission pathways via a 15N tracing model. Soil Biol Biochem 72:44–54
Niklaus PA, Kandeler E, Leadley PW, Schmid B, Tscherko D, Korner C (2001) A link between plant diversity, elevated CO2 and soil nitrate. Oecologia 127:540–548
Officer J, Phillips F, Armstrong R, Kelly K (2008) Nitrous oxide emissions from dry-land wheat in south-eastern Australia. In: Proceedings of the 14th Australian Agronomy Conference. Australian Society of Agronomy, Adelaide http://www.survey.regional.org.au/au/asa/
Officer S, Kearney G, Kelly K, Graham J (2012) Large nitrous oxide emissions after conversion from pasture to cropping in temperate south eastern Australia. Paper presented at the SSA-NZSSS Conference, Hobart, pp 2–7 December
Offre P, Prosser JI, Nicol GW (2009) Growth of ammonia-oxidizing archaea in soil microcosms is inhibited by acetylene. FEMS Microbiol Ecol 70:99–108
Okano Y, Hristova KR, Leutenegger CM, Jackson LE, Denison RF, Gebreyesus B, Lebauer D, Scow KM (2004) Appl Environ Microbiol 70:1008–1016
Purkhold U, Pommerening-Roser A, Juretschko S (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66:5368–5382
Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Environ Microbiol 63:4704–4712
Rudaz AO, Walti E, 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
Ru-Jerez BE, White RE, Roger ball P (1994) Long-term measurement of denitrification in three contrasting pastures grazed by sheep. Soil Biol Biochem 26:29–39
Saggar S, Jha N, Deslippe J, Bolan NS, Luo J, Giltrap DL, Kim DG, Zaman M, Tillman RW (2013) Denitrification and N2O:N2 production in temperate grasslands: processes, measurements, modelling and mitigating negative impacts. Sci Total Environ 465:173–195
Saghir NS, Mulvancy RL, Azam F (1993) Determination of nitrogen by microdiffusion in mason jars. I. Inorganic nitrogen in soil extracts. Commun Soil Sci Plant Anal 24:1745–1762
Schauss K, Focks A, Leininger S, Kotzerke A, Heuer H, Thiele-Bruhn S, Sharma S, Berndt-Michael W, Michael M, Smalla K, Munch JC, Amelung W, Kaupenjohann M, Schloter M, Schleper C (2009) Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environ Microbiol 11:446–456
Schleper C, Jurgens G, Jonuscheit M (2005) Genomic studies of uncultivated archaea. Nat Rev Microbiol 3:479–488
Stevens RJ, Laughlin RJ, Burns LC, Arah JRM, Hood RC (1997) Measuring the contributions of nitrification and denitrification to the flux of nitrous oxide from soil. Soil Biol Biochem 29:139–151
Stieglmeier M, Mooshammer M, Kitzler B (2014) Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. ISME 8:1135–1146
Szukics U, Abell GCJ, Hodl V, Mitter B, Sessitsch A, Hackl E, Zechmeister-Boltenstern S (2010) Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. FEMS Microbiol Ecol 72:395–406
Tortoso AC, Hutchinson GL (1990) Contributions of autotrophic and heterotrophic nitrifiers to soil NO and N2O emissions. Appl Environm Microbiol 56:1799–1805
Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10:1357–1364
Watanabe T, Lee CG, Murase J, Asakawa S, Kimura M (2011) Carbon flow into ammonia-oxidizing bacteria and archaea during decomposition of 13C-labeled plant residues in soil. Soil Sci Plant Nutri 57:775–785
Webster EA, Hopkins DW (1996) Contributions from different microbial processes to N2O emission from soil under different moisture regimes. Biol Fertil Soils 22:331–335
Weier K, Doran J, Power J, Walters DT (1993) Denitrification and the dinitrogen/nitrous oxide ratio as affected by soil water, available carbon, and nitrate. Soil Sci Soc Am J 57:66–72
Well R, Flessa H, Lu X (2008) Isotopologue ratios of N2O emitted from microcosms with NH4 + fertilized arable soils under conditions favoring nitrification. Soil Biol Biochem 40:2416–2426
Wrage N, Groenigen JW, Oenema O, Baggs EM (2005) A novel dual-isotope labelling method for distinguishing between soil sources of N2O. Rapid Commun Mass Spectrom 19:3298–3306
Yamamoto A, Akiyama H, Naokawa T, Miyazaki Y, Honda Y, Sano Y, Nakajima Y, Yagi K (2014) Lime-nitrogen application affects nitrification, denitrification, and N2O emission in an acidic tea soil. Biol Fertil Soils 50:53–62
Zak DR, Pregitzer KS, Curtis PS, Holmes WE (2000) Atmospheric CO2 and the composition and function of soil microbial communities. Ecol Appl 10:47–59
Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045
Zheng X, Wang M, Wang Y, Shen R, Ji G, Li J, Jin J, Li L (2000) Impacts of soil moisture on nitrous oxide emission from croplands: a case study on the rice-based agro-ecosystem in Southeast China. Chemosphere-Glob Chang Sci 2:207–224
Zhu TB, Zhang JB, Cai ZC (2011) The contribution of nitrogen transformation processes to total N2O emissions from soils used for intensive vegetable cultivation. Plant Soil 343:313–327
Acknowledgements
The authors would like to acknowledge the financial support by Incitec Pivot, the 424 Australian Government Department of Agriculture through the Grains Research and 425 Development Corporation, and Australian Research Council (DE150100870, DP160101028).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Liu, R., Hayden, H.L., Suter, H. et al. 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 (2017). https://doi.org/10.1007/s00374-016-1167-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-016-1167-8