Journal of Soils and Sediments

, Volume 19, Issue 10, pp 3499–3511 | Cite as

N2O production in the organic and mineral horizons of soil had different responses to increasing temperature

  • Lifei Sun
  • Changpeng Sang
  • Chao Wang
  • Zhenzhen Fan
  • Bo Peng
  • Ping Jiang
  • Zongwei XiaEmail author
Soils, Sec 2 • Global Change, Environ Risk Assess, Sustainable Land Use • Research Article



The responses of N2O emission to increasing temperature in different soil horizons are not clearly understood yet. Here, we investigated the effects of increasing temperature on sources of soil N2O emissions from organic (O) and mineral (A) horizons of a temperate forest soil.

Materials and methods

An incubation experiment using 15N as a tracer was conducted to investigate the sources of soil N2O emission and their responses to increasing temperature in the O and A horizon soils at controlled temperatures (5 °C, 15 °C, 25 °C, and 35 °C at 60% water holding capacity). The O horizon had higher total organic carbon, total nitrogen, and sand contents than the A horizon.

Results and discussion

The ratio of nitrification- to denitrification-derived N2O production decreased with increasing temperature in both soil horizons, perhaps due to the development of anaerobic volumes and the greater increase in nirS gene abundance. The nirS gene was much more abundant than the nirK gene and was more correlated to denitrification-derived N2O flux. No relationship was found between nitrification-derived N2O flux and amoA gene abundances of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) for either soil horizon. In general, nitrification dominated N2O production in the O horizon soil, while denitrification dominated N2O production in the A horizon soil. N2O emission was higher in the A horizon soil than in the O horizon soil, but the temperature sensitivity of N2O emission in the A horizon soil was lower. These differences might be explained by the higher initial anaerobic volume and higher carbon availability in the A horizon than in the O horizon.


Our results suggest that the denitrification process is more stimulated by increasing temperature compared to the nitrification process in both O and A horizons in our studied soil.


15Denitrification Nitrous oxide (N2O) emission Nitrification qPCR Temperature sensitivity (Q10



This work was financially supported by the National Natural Science Foundation of China (31400427 and 31770531).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11368_2019_2316_MOESM1_ESM.docx (847 kb)
ESM 1 (DOCX 846 kb)


  1. Abdalla M, Jones M, Smith P, Williams M (2009) Nitrous oxide fluxes and denitrification sensitivity to temperature in Irish pasture soils. Soil Use Manag 25:376–388CrossRefGoogle Scholar
  2. 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 11:1399–1407CrossRefGoogle Scholar
  3. Baggs EM (2011) Soil microbial sources of nitrous oxide: recent advances in knowledge, emerging challenges and future direction. Curr Opin Environ Sustain 3:321–327CrossRefGoogle Scholar
  4. Bai E, Li W, Li S, Sun J, Peng B, Dai W, Jiang P, Han S (2014) Pulse increase of soil N2O emission in response to N addition in a temperate forest on Mt Changbai, Northeast China. PLoS One 9:e102765CrossRefGoogle Scholar
  5. Belser LW (1979) Population ecology of nitrifying bacteria. Annu Rev Microbiol 33:309–333CrossRefGoogle Scholar
  6. Bing H, Wu Y, Zhou J, Sun H, Luo J, Wang J, Yu D (2015) Stoichiometric variation of carbon, nitrogen, and phosphorus in soils and its implication for nutrient limitation in alpine ecosystem of eastern Tibetan plateau. J Soils Sediments 16:405–416CrossRefGoogle Scholar
  7. Blagodatskaya Е, Zheng X, Blagodatsky S, Wiegl R, Dannenmann M, Butterbach-Bahl K (2014) Oxygen and substrate availability interactively control the temperature sensitivity of CO2 and N2O emission from soil. Biol Fertil Soils 50:775–783CrossRefGoogle Scholar
  8. Bosatta E, Ågren GI (1999) Soil organic matter quality interpreted thermodynamically. Soil Biol Biochem 31:1889–1891CrossRefGoogle Scholar
  9. Braker G, Fesefeldt A, Witzel K-P (1998) Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microbiol 64:3769–3775Google Scholar
  10. Braker G, Schwarz J, Conrad R (2010) Influence of temperature on the composition and activity of denitrifying soil communities. FEMS Microbiol Ecol 73:134–148Google Scholar
  11. 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 53:1707–1711CrossRefGoogle Scholar
  12. Burford J, Bremner J (1975) Relationships between the denitrification capacities of soils and total, water-soluble and readily decomposable soil organic matter. Soil Biol Biochem 7:389–394CrossRefGoogle Scholar
  13. 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 T Roy Soc B 368:20130122CrossRefGoogle Scholar
  14. Castaldi S (2000) Responses of nitrous oxide, dinitrogen and carbon dioxide production and oxygen consumption to temperature in forest and agricultural light-textured soils determined by model experiment. Biol Fertil Soils 32:67–72CrossRefGoogle Scholar
  15. Chen D, Li Y, Grace P, Mosier AR (2008) N2O emissions from agricultural lands: a synthesis of simulation approaches. Plant Soil 309:169–189CrossRefGoogle Scholar
  16. Chen Y, Chen G, Robinson D, Yang Z, Guo J, Xie J, Fu S, Zhou L, Yang Y (2016) Large amounts of easily decomposable carbon stored in subtropical forest subsoil are associated with r-strategy-dominated soil microbes. Soil Biol Biochem 95:233–242CrossRefGoogle Scholar
  17. Cheng Y, Wang J, Wang SQ, Zhang JB, Cai ZC (2014a) Effects of soil moisture on gross N transformations and N2O emission in acid subtropical forest soils. Biol Fertil Soils 50:1099–1108CrossRefGoogle Scholar
  18. Cheng Y, Zhang JB, Müller C, Wang SQ (2014b) 15N tracing study to understand the N supply associated with organic amendments in a vineyard soil. Biol Fertil Soils 51:983–993CrossRefGoogle Scholar
  19. Cui P, Fan F, Yin C, Song A, Huang P, Tang Y, Zhu P, Peng C, Li T, Wakelin SA, Liang Y (2016) Long-term organic and inorganic fertilization alters temperature sensitivity of potential N2O emissions and associated microbes. Soil Biol Biochem 93:131–141CrossRefGoogle Scholar
  20. Davidson EA, Janssens IA, Luo Y (2006) On the variability of respiration in terrestrial ecosystems: moving beyond Q10. Glob Chang Biol 12:154–164CrossRefGoogle Scholar
  21. 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 52:667–673CrossRefGoogle Scholar
  22. Dowdell R, Smith K (1974) Field studies of the soil atmosphere II. Occurrence of nitrous oxide. J Soil Sci 25:231–238CrossRefGoogle Scholar
  23. Dungait JAJ, Hopkins DW, Gregory AS, Whitmore AP (2012) Soil organic matter turnover is governed by accessibility not recalcitrance. Glob Chang Biol 18:1781–1796CrossRefGoogle Scholar
  24. Durán J, Morse JL, Rodríguez A, Campbell JL, Christenson LM, Driscoll CT, Fahey TJ, Fisk MC, Mitchell MJ, Templer PH, Groffman PM (2017) Differential sensitivity to climate change of C and N cycling processes across soil horizons in a northern hardwood forest. Soil Biol Biochem 107:77–84CrossRefGoogle Scholar
  25. Gee GW, Bauder JW (1986) Particle-size analysis. Methods of soil analysis: part 1—physical and mineralogical methods. American Society of Agronomy, Madison, 383–411Google Scholar
  26. He JZ, Shen JP, Zhang LM, Di HJ (2012) A review of ammonia-oxidizing bacteria and archaea in Chinese soils. Front Microbiol 3:296Google Scholar
  27. Hu HW, Macdonald CA, Trivedi P, Anderson IC, Zheng Y, Holmes B, Bodrossy L, Wang JT, He JZ, Singh BK (2016a) Effects of climate warming and elevated CO2 on autotrophic nitrification and nitrifiers in dryland ecosystems. Soil Biol Biochem 92:1–15CrossRefGoogle Scholar
  28. Hu HW, Chen D, He JZ (2015) Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiol Rev 39:729–749CrossRefGoogle Scholar
  29. Hu X, Liu L, Zhu B, Du E, Hu X, Li P, Zhou Z, Ji C, Zhu J, Shen H, Fang J (2016) Asynchronous responses of soil carbon dioxide, nitrous oxide emissions and net nitrogen mineralization to enhanced fine root input. Soil Biol Biochem 92:67–78CrossRefGoogle Scholar
  30. Kirkham D, Bartholomew WV (1954) Equations for following nutrient transformations in soil, utilizing tracer data. Soil Sci Soc Am J 18:33–34CrossRefGoogle Scholar
  31. Li X, Sørensen P, Olesen JE, Petersen SO (2016) Evidence for denitrification as main source of N2O emission from residue-amended soil. Soil Biol Biochem 92:153–160CrossRefGoogle Scholar
  32. Liu R, Hayden HL, Suter H, Hu H, Lam SK, He J, Mele PM, Chen D (2016a) The effect of temperature and moisture on the source of N2O and contributions from ammonia oxidizers in an agricultural soil. Biol Fertil Soils 53:141–152CrossRefGoogle Scholar
  33. Liu R, Hu H, Suter H, Hayden HL, He J, Mele P, Chen D (2016b) Nitrification is a primary driver of nitrous oxide production in laboratory microcosms from different land-use soils. Front Microbiol 7:1373Google Scholar
  34. Liu Y, He N, Wen X, Yu G, Gao Y, Jia Y (2016c) Patterns and regulating mechanisms of soil nitrogen mineralization and temperature sensitivity in Chinese terrestrial ecosystems. Agric Ecosyst Environ 215:40–46CrossRefGoogle Scholar
  35. 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 4:5–14CrossRefGoogle Scholar
  36. Myrstener M, Jonsson A, Bergstrom AK (2016) The effects of temperature and resource availability on denitrification and relative N2O production in boreal lake sediments. J Environ Sci-China 47:82–90CrossRefGoogle Scholar
  37. Nagano H, Sugihara S, Matsushima M, Okitsu S, Prikhodko VE, Manakhova E, Zdanovich GB, Manakhov DV, Ivanov IV, Funakawa S, Kawahigashi M, Inubushi K (2012) Carbon and nitrogen contents and greenhouse gas fluxes of the Eurasian steppe soils with different land-use histories located in the Arkaim museum reserve of South Ural, Russia. Soil Sci Plant Nutr 58:238–244CrossRefGoogle Scholar
  38. Purkhold U, Pommerening-Röser A, Juretschko S, Schmid MC, Koops H-P, Wagner M (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 66:5368–5382CrossRefGoogle Scholar
  39. Remde A, Conrad R (1990) Production of nitric oxide in Nitrosomonas europaea by reduction of nitrite. Arch Microbiol 154:187–191CrossRefGoogle Scholar
  40. Rütting T, Clough TJ, Müller C, Lieffering M, Newton PCD (2010) Ten years of elevated atmospheric carbon dioxide alters soil nitrogen transformations in a sheep-grazed pasture. Glob Chang Biol 16:2530–2542CrossRefGoogle Scholar
  41. Smith K (1997) The potential for feedback effects induced by global warming on emissions of nitrous oxide by soils. Glob Chang Biol 3:327–338CrossRefGoogle Scholar
  42. Smith K, Thomson P, Clayton H, McTaggart I, Conen F (1998) Effects of temperature, water content and nitrogen fertilisation on emissions of nitrous oxide by soils. Atmos Environ 32:3301–3309CrossRefGoogle Scholar
  43. Starr RC, Gillham RW (1993) Denitrification and organic carbon availability in two aquifers. Ground Water 31:934–947CrossRefGoogle Scholar
  44. Stevens R, Laughlin R, Burns L, Arah J, Hood R (1997) Measuring the contributions of nitrification and denitrification to the flux of nitrous oxide from soil. Soil Biol Biochem 29:139–151CrossRefGoogle Scholar
  45. Stottlemyer R, Toczydlowski D (1999) Nitrogen mineralization in a mature boreal forest, Isle Royale, Michigan. J Environ Qual 28:709–720CrossRefGoogle Scholar
  46. Szukics U, Abell GC, 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 72:395–406CrossRefGoogle Scholar
  47. Tu Y, Fang Y, Liu D, Pan Y (2016) Modifications to the azide method for nitrate isotope analysis. Rapid Commun Mass Sp 30:1213–1222CrossRefGoogle Scholar
  48. Wang J, Zhang J, Müller C, Cai Z (2016) Temperature sensitivity of gross N transformation rates in an alpine meadow on the Qinghai–Tibetan plateau. J Soils Sediments 17:423–431CrossRefGoogle Scholar
  49. Warneke S, Schipper LA, Matiasek MG, Scow KM, Cameron S, Bruesewitz DA, McDonald IR (2011) Nitrate removal, communities of denitrifiers and adverse effects in different carbon substrates for use in denitrification beds. Water Res 45:5463–5475CrossRefGoogle Scholar
  50. Weier K, Doran J, Power J, Walters D (1993) Denitrification and the dinitrogen/nitrous oxide ratio as affected by soil water, available carbon, and nitrate. Soil Sci Soc Am J 57:66–72CrossRefGoogle Scholar
  51. Xia Z, Xu H, Chen G, Dong D, Bai E, Luo L (2013) Soil N2O production and the δ15N–N2O value: their relationship with nitrifying/denitrifying bacteria and archaea during a growing season of soybean in Northeast China. Eur J Soil Biol 58:73–80CrossRefGoogle Scholar
  52. Xu W, Li W, Jiang P, Wang H, Bai E (2014) Distinct temperature sensitivity of soil carbon decomposition in forest organic layer and mineral soil. Sci Rep 4:6512CrossRefGoogle Scholar
  53. Yao H, Gao Y, Nicol GW, Campbell CD, Prosser JI, Zhang L, Han W, Singh BK (2011) Links between ammonia oxidier community structure, abundance and nitrification potential in acidic soils. Appl Environ Microbiol 77:4618–4625CrossRefGoogle Scholar
  54. Yin C, Fan F, Song A, Fan X, Ding H, Ran W, Qiu H, Liang Y (2017) The response patterns of community traits of N2O emission-related functional guilds to temperature across different arable soils under inorganic fertilization. Soil Biol Biochem 108:65–77CrossRefGoogle Scholar
  55. Zhang J, Cai Z, Zhu T (2011a) N2O production pathways in the subtropical acid forest soils in China. Environ Res 111:643–649CrossRefGoogle Scholar
  56. Zhang J, Zhu T, Cai Z, Müller C (2011b) Nitrogen cycling in forest soils across climate gradients in eastern China. Plant Soil 342:419–432CrossRefGoogle Scholar
  57. Zhang J, Müller C, Cai Z (2015) Heterotrophic nitrification of organic N and its contribution to nitrous oxide emissions in soils. Soil Biol Biochem 84:199–209CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Lifei Sun
    • 1
    • 2
  • Changpeng Sang
    • 1
    • 2
  • Chao Wang
    • 1
  • Zhenzhen Fan
    • 1
    • 2
  • Bo Peng
    • 1
    • 2
  • Ping Jiang
    • 1
  • Zongwei Xia
    • 1
    Email author
  1. 1.CAS Key Laboratory of Forest Ecology and Management, Institute of Applied EcologyChinese Academy of SciencesShenyangChina
  2. 2.University of Chinese Academy of SciencesBeijingChina

Personalised recommendations