Skip to main content
Log in

Stimulation of heterotrophic nitrification and N2O production, inhibition of autotrophic nitrification in soil by adding readily degradable carbon

  • Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

This study aimed to test the hypothesis that readily degradable Carbon (C) has contrasting effect on soil N autotrophic and heterotrophic nitrification, can stimulate nitrous oxide (N2O) emission. The knowledge can improve our understanding of the effect of readily degradable C on soil N nitrification and the related N2O emission.

Materials and methods

15N tracing technique along with acetylene inhibition was used to determine the effect of different doses of glucose-C addition on the rates of total nitrification (ntot), autotrophic nitrification (na), heterotrophic nitrification (nh), and N2O production in two soils. Soils were collected from Glenormiston (GN) and Terang (TR), Victoria, Australia and incubated at soil moisture content of 60% water-filled pore space (WFPS) and at 25 °C.

Results and discussion

The addition of mixed C and N substrates with wide C/N ratio (> 25) promoted heterotrophic nitrification by 2.84- to 3.33-folds but inhibited autotrophic nitrification by 30.4–54.8%, thereby resulting in high ntot and NO3 accumulation compared with the soil samples under the control treatment. The mechanism of glucose inhibition of na might be caused by increasing the microbial immobilization of NH4+ and not by affecting the gene copy numbers of ammonia-oxidizing archea and ammonia-oxidizing bacteria. The glucose addition stimulated N2O production in soil, which might be caused by promoting heterotrophic nitrification and denitrification.

Conclusions

The stimulating effect of degradable C application on the contribution of heterotrophic nitrification to total nitrification, NO3 accumulation, and N2O production should be considered, especially in soils with low pH and high organic C content.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ameloot N, Maenhout P, Neve SD, Sleutel S (2016) Biochar-induced N2O emission reductions after field incorporation in a loam soil. Geoderma 267:10–16

    CAS  Google Scholar 

  • Baggs EM (2011) Soil microbial sources of nitrous oxide: recent advances in knowledge, emerging challenges and future direction. Curr Opin Environ Sustain 3:321–327

    Google Scholar 

  • Beeckman F, Motte H, Beeckman T (2018) Nitrification in agricultural soils: impact, actors and mitigation. Curr Opin Biotechnol 50:166–173

    CAS  Google Scholar 

  • 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 Lond 368:20130122

    Google Scholar 

  • Cai YJ, Ding WX, Zhang XL, Yu HY, Wang LF (2010) Contribution of heterotrophic nitrification to nitrous oxide production in a long-term N-fertilized arable black soil. Commun Soil Sci Plant Anal 41:2264–2278

    CAS  Google Scholar 

  • Chen ZM, Xu YH, Fan JL, Yu HY, Ding WX (2017) Soil autotrophic and heterotrophic respiration in response to different N fertilization and environmental conditions from a cropland in Northeast China. Soil Biol Biochem 110:103–115

    CAS  Google Scholar 

  • Cheng Y, Cai ZC, Chang SX, Wang J, Zhang JB (2012) Wheat straw and its biochar have contrasting effects on inorganic N retention and N2O production in a cultivated Black Chernozem. Biol Fertil Soils 48:941–946

    CAS  Google Scholar 

  • Cheng Y, Zhang JB, Muller C, Wang SQ (2015) 15N tracing study to understand the N supply associated with organic amendments in a vineyard soil. Biol Fertil Soils 51:983–993

    CAS  Google Scholar 

  • Cheng Y, Xie W, Huang R, Yan X, Wang S (2017) Extremely high N2O but unexpectedly low NO emissions from a highly organic and chemical fertilized peach orchard system in China. Agric Ecosyst Environ 246:202–209

    CAS  Google Scholar 

  • Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, von Bergen M, Rattei T, Bendinger B, Nielsen PH, Wagner M (2015) Complete nitrification by nitrospirabacteria. Nature 528(7583):504–509

    CAS  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, Winefield CS, 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

    CAS  Google Scholar 

  • Emeterio LS, Canals RM, Herman DJ (2014) Combined effects of labile and recalcitrant carbon on short-term availability of nitrogen in intensified arable soil. Eur J Soil Sci 65:377–385

    Google Scholar 

  • Freppaz M, Williams BL, Edwards AC, Scalenghe R, Zanini E (2007) Labile nitrogen, carbon, and phosphorus pools and nitrogen mineralization and immobilization rates at low temperatures in seasonally snow-covered soils. Biol Fertil Soils 43:519–529

    CAS  Google Scholar 

  • Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843

    CAS  Google Scholar 

  • Garrido F, Hénault C, Gaillard H, Pérez S, Germon JC (2002) N2O and NO emissions by agricultural soils with low hydraulic potentials. Soil Biol Biochem 34:559–575

    CAS  Google Scholar 

  • Hart SC, Stark JM, Davidson EA, Firestone MK (1994) Nitrogen mineralization, immobilization and nitrification. In: Weaver RW et al (eds) Methods of soil analysis, part 2. Microbiological and Biochemical Properties. Soil Science Society of America, Madison, pp 985–1018

    Google Scholar 

  • Hu HW, Zhang LM, Dai Y, Di HJ, He JZ (2013) pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing. J Soils Sediments 13:1439–1449

    Google Scholar 

  • 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 39:729–749

    CAS  Google Scholar 

  • Hu HW, He JZ (2017) Comammox—a newly discovered nitrification process in the terrestrial nitrogen cycle. J Soils Sediments 17:1–9

    Google Scholar 

  • Hanan EJ, Schimel JP, Dowdy K, D'Antonio CM (2016) Effects of substrate supply, pH, and char on net nitrogen mineralization and nitrification along a wildfire-structured age gradient in chaparral. Soil Biol Biochem 95:87–99

    CAS  Google Scholar 

  • Hink L, Nicol GW, Prosser JI (2017) Archaea produce lower yields of N2O than bacteria during aerobic ammonia oxidation in soil. Environ Microbiol 19:4829–4837

    CAS  Google Scholar 

  • Ilstedt U, Singh S (2005) Nitrogen and phosphorus limitations of microbial respiration in a tropical phosphorus-fixing acrisol (ultisol) compared with organic compost. Soil Biol Biochem 37:1407–1410

    CAS  Google Scholar 

  • Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143

    CAS  Google Scholar 

  • Kessel MAHJV, Speth DR, Albertsen M, Nielsen PH, Camp HJMOD, Kartal B et al (2015) Complete nitrification by a single microorganism. Nature 528(7583):555–559

    Google Scholar 

  • Lan T, Suter H, Liu R, Gao X, Chen D (2018) Nitrogen transformation rates and N2O producing pathways in two pasture soils. J Soils Sediments 18:2970–2979

    CAS  Google Scholar 

  • Li Y, Chapman SJ, Nicol GW, Yao H (2018) Nitrification and nitrifiers in acidic soils. Soil Biol Biochem 116:290–301

    CAS  Google Scholar 

  • Liu R, Suter H, Hayden H, He JZ, Chen DL (2015) Nitrate production is mainly heterotrophic in an acid dairy soil with high organic content in Australia. Biol Fertil Soils 51:891–896

    CAS  Google Scholar 

  • Liu SW, Lin F, Wu S, Ji C, Sun Y, Jin YG, Li SQ, Li ZF, Zou JW (2017) A meta-analysis of fertilizer-induced soil NO and combined N2O emissions. Glob Chang Biol 23:2520–2532

    Google Scholar 

  • Loick N (2016) Denitrification as a source of nitric oxide emissions from incubated soil cores from a UK grassland soil. Soil Biol Biochem 95:1–7

    CAS  Google Scholar 

  • Ma Q, Wu Z, Pan F, Wang J, Zhou H, Jiang C, Xu YG, Yu WT (2016) Effect of glucose addition on the fate of urea – 15N in fixed ammonium and soil microbial biomass N pools. Eur J Soil Biol 75:168–173

    CAS  Google Scholar 

  • Manzoni S, Porporato A, Schimel JP (2008) Soil heterogeneity in lumped mineralization–immobilization models. Soil Biol Biochem 40:1137–1148

    CAS  Google Scholar 

  • Mehnaz KR, Keitel C, Dijkstra FA (2018) Effects of carbon and phosphorus addition on microbial respiration, N2O emission, and gross nitrogen mineralization in a phosphorus-limited grassland soil. Biol Fertil Soils 54:481–493

    CAS  Google Scholar 

  • Mooshammer M, Wanek W, Hämmerle I, Fuchslueger L, Hofhansl F, Knoltsch A, Schnecker J, Takriti M, Watzka M, Wild B, Keiblinger KM, Zechmeister-Boltenstern S, Richter A (2014) Adjustment of microbial nitrogen use efficiency to carbon:nitrogen imbalances regulates soil nitrogen cycling. Nat Commun 5:3694

    CAS  Google Scholar 

  • Morley N, Baggs EM (2010) Carbon and oxygen controls on N2O and N2 production during nitrate reduction. Prog Theor Phys 121:671–686

    Google Scholar 

  • Müller C, Stevens RJ, Laughlin RJ (2004) A 15N tracing model to analyse N transformations in old grassland soil. Soil Biol Biochem 36:619–632

    Google Scholar 

  • Nelissen V, Rütting T, Huygens D, Staelens J, Ruysschaert G, Boeckx P (2012) Maize biochars accelerate short-term soil nitrogen dynamics in a loamy sand soil. Soil Biol Biochem 55:20–27

    CAS  Google Scholar 

  • Papen H, Vonberg R, Hinkel I, Thoene B, Rennenberg H (1989) Heterotrophic nitrification by Alcaligenes-Faecalis: NO2 , NO3 , N2O, and NO production in exponentially growing cultures. Appl Environ Microbiol 55:2068–2072

    CAS  Google Scholar 

  • Poeplau C, Don A (2013) Sensitivity of soil organic carbon stocks and fractions to different land-use changes across Europe. Geoderma 192:189–201

    CAS  Google Scholar 

  • Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531

    CAS  Google Scholar 

  • 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 Nutr 24:1745–1762

    CAS  Google Scholar 

  • Sahrawat KL (2008) Factors affecting nitrification in soils. Commun Soil Sci Plant Anal 39:1436–1446

    CAS  Google Scholar 

  • Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563

    CAS  Google Scholar 

  • Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol Lett16:930–939

    Google Scholar 

  • Stein LY, Klotz MG (2016) The nitrogen cycle. Curr Biol 26:94–98

    Google Scholar 

  • Wang L, Cai Z, Yang L, Meng L (2005) Effects of disturbance and glucose addition on nitrous oxide and carbon dioxide emissions from a paddy soil. Soil Tillage Res 82:185–194

    Google Scholar 

  • Yao H, Campbell CD, Qiao X (2011) Soil pH controls nitrification and carbon substrate utilization more than urea or charcoal in some highly acidic soils. Biol Fertil Soils 47:515–522

    CAS  Google Scholar 

  • Yokoyama K, Kai H, Naklang K (1992) Heterotrophic nitrification by sodium chloride-tolerant fungi in soils added with sodium-chloride. Soil Sci Plant Nutr 38:757–762

    CAS  Google Scholar 

  • Yu WT, Pan FF, Ma Q, Wang J, Zhou H, Jiang CM, Xu YG (2016) Alterations of pathways in fertilizer N conservation and supply in soils treated with dicyandiamide, hydroquinone and glucose. Appl Soil Ecol 108:108–117

    Google Scholar 

  • Zhang JB, Cai ZC, Zhu TB (2011) N2O production pathways in the subtropical acid forest soils in China. Environ Res 111(5):643–649

    CAS  Google Scholar 

  • Zhang J, Sun W, Zhong W, Cai Z (2014) The substrate is an important factor in controlling the significance of heterotrophic nitrification in acidic forest soils. Soil Biol Biochem 76:143–148

    CAS  Google Scholar 

  • Zhang JB, Muller C, Cai ZC (2015) Heterotrophic nitrification of organic N and its contribution to nitrous oxide emissions in soils. Soil Biol Biochem 84:199–209

    CAS  Google Scholar 

  • Zhao Y, Zhang JB, Muller C, Cai ZC (2018) Temporal variations of crop residue effects on soil N transformation depend on soil properties as well as residue qualities. Biol Fertil Soils 54:659–669

    CAS  Google Scholar 

  • Zhu T, Meng T, Zhang J, Zhong W, Mueller C, Cai Z (2015) Fungi-dominant heterotrophic nitrification in a subtropical forest soil of China. J Soils Sediments 15:705–709

    CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to the internal reviewers and editors for their comments on the draft manuscript.

Funding

The authors are grateful for the funding provided by the Ministry of Science and Technology of China, National Key Research and Development Plan (2017YFD0200100), by the Institute of Soil Science, Chinese Academy of Sciences, National Key Laboratory Opening Funding (Y20160031), Incitec Pivot Limited, the Australian Government Department of Agriculture through Grains Research (DE150100870), and the Australian Research Council (LP160101134).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ting Lan.

Additional information

Responsible editor: Huaiying Yao

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lan, T., Liu, R., Suter, H. et al. Stimulation of heterotrophic nitrification and N2O production, inhibition of autotrophic nitrification in soil by adding readily degradable carbon. J Soils Sediments 20, 81–90 (2020). https://doi.org/10.1007/s11368-019-02417-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-019-02417-0

Keywords

Navigation