Skip to main content
SpringerLink
Log in

The contributions of hydroxylamine and nitrite to NO and N2O production in alkaline and acidic vegetable soils

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

The contribution of hydroxylamine (NH2OH) and nitrite (NO2−) to nitric oxide (NO) and nitrous oxide (N2O) production remains unclear in vegetable production soils.

Materials and methods

Soils collected from six typical greenhouse vegetable fields were incubated for 48 h following amendment with 1 mM NaNO2, 10 μM NH2OH, or 1 mM NaNO2 + 10 μM NH2OH. The importance of abiotic processes on the NO and N2O formation from the NH2OH and NO2− were studied by irradiating the soil samples with γ-irradiation.

Results and discussion

NO2− amendment significantly stimulated NO production, while the NH2OH-dependent NO production was minimal. NH2OH stimulated more abiotic N2O production in alkaline soils than in acidic soils (p < 0.05), while NO2− stimulated more biotic N2O production in acidic soils than in alkaline soils (p < 0.05). The NH2OH- and NO2−-dependent sources produced biotic or abiotic N2O with site preference (SP) values of 27.4–36.5‰, which is similar to those from ammonia-oxidizing archaea (AOA) or ammonia-oxidizing bacteria (AOB) sources (25.1–34.2‰), indicating that abiotic N2O production were closely linked with biotic NH3 oxidation. The variability of NO2−+NH2OH-induced N2O production can be explained by the soil organic carbon and iron concentrations, whereas NO2−-induced NO production can be explained by the soil pH.

Conclusions

NO2− addition dominated NO production in all soils. Furthermore, NO2− addition increased biotic N2O production in acidic soils, while NH2OH addition increased abiotic N2O production in alkaline soils. The presence of NO2− could significantly stimulate the abiotic conversion of NH2OH to N2O in soils with low soil organic carbon and high iron concentrations. Thus, assessing the abundance of NH2OH and NO2− could provide crucial information for understanding NO and N2O production procedures in vegetable soils.

Highlights

• The chemical decomposition of NO2− dominated NO production in all soils.

• The NH2OH stimulated abiotic N2O production in alkaline soils.

• The NO2− stimulated biotic N2O production in acidic soils.

• The SP for abiotic NO2−-/NH2OH-related N2O were in the same range as AOB/AOA sources.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

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

    CAS  Google Scholar 

  • Breuillin-Sessoms F, Venterea RT, Sadowsky MJ, Coulter JA, Clough TJ, Wang P (2017) Nitrification gene ratio and free ammonia explain nitrite and nitrous oxide production in urea-amended soils. Soil Biol Biochem 111:143–153

    CAS  Google Scholar 

  • Bremner JM (1997) Sources of nitrous oxide in soils. Nutr Cycl Agroecosyst 49:7–16

    CAS  Google Scholar 

  • Denk TR, Mohn J, Decock C, Lewicka-Szczebak D, Harris E, Butterbach-Bahl K, Kiese R, Wolf B (2017) The nitrogen cycle: a review of isotope effects and isotope modeling approaches. Soil Biol Biochem 105:121–137

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Duan P, Zhang Q, Zhang X, Xiong Z (2019) Mechanisms of mitigating nitrous oxide emissions from vegetable soil varied with manure, biochar and nitrification inhibitors. Agric For Meteorol 278:107672

    Google Scholar 

  • Grabb KC, Buchwald C, Hansel CM, Wankel SD (2017) A dual nitrite isotopic investigation of chemodenitrification by mineral-associated Fe(II) and its production of nitrous oxide. Geochim Cosmochim Acta 196:388–402

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Heil J, Vereecken H, Brüggemann N (2016) A review of chemical reactions of nitrification intermediates and their role in nitrogen cycling and nitrogen trace gas formation in soil. Eur J Soil Sci 67:23–39

    CAS  Google Scholar 

  • Homyak PM, Kamiyama M, Sickman JO, Schimel JP (2017) Acidity and organic matter promote abiotic nitric oxide production in drying soils. Glob Chang Biol 23:1735–1747

    Google Scholar 

  • Hu W, Zhang Y, Huang B, Teng Y (2017) Soil environmental quality in greenhouse vegetable production systems in eastern China: current status and management strategies. Chemosphere 170:183–195

    CAS  Google Scholar 

  • Hu HW, He JZ (2017) Comammox—a newly discovered nitrification process in the terrestrial nitrogen cycle. J Soils Sediments 17:2709–2717

    CAS  Google Scholar 

  • Jones LC, Peters B, Lezama Pacheco JS, Casciotti KL, Fendorf S (2015) Stable isotopes and iron oxide mineral products as markers of chemodenitrification. Environ Sci Technol 49:3444–3452

    CAS  Google Scholar 

  • Jung M, Well R, Min D, Giesemann A, Park S, Kim J, Kim S, Rhee S (2014) Isotopic signatures of N2O produced by ammonia-oxidizing archaea from soils. The ISME Journal 8:1115–1125

    CAS  Google Scholar 

  • Jung MY, Gwak JH, Rohe L, Giesemann A, Kim JG, Well R, Madsen EL, Herbold CW, Wagner M, Rhee SK (2019) Indications for enzymatic denitrification to N2O at low pH in an ammonia–oxidizing archaeon. The ISME Journal 13:2633–2638

    CAS  Google Scholar 

  • Kits KD, Jung MY, Vierheilig J, Pjevac P, Sedlacek CJ, Liu S, Herbold C, Stein LY, Richter A, Wissel H, Brüggemann N, Wagner M, Daims H (2019) Low yield and abiotic origin of N2O formed by the complete nitrifier Nitrospira inopinata. Nat Commun 10:1836

    Google Scholar 

  • Kozlowski JA, Stieglmeier M, Schleper C, Klotz MG, Stein LY (2016) Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota. The ISME Journal 10:1836–1845

    CAS  Google Scholar 

  • Li C, Hu HW, Chen QL, Chen D, He JZ (2020) Growth of comammox Nitrospira is inhibited by nitrification inhibitors in agricultural soils. J Soils Sediments 20:621–628

    CAS  Google Scholar 

  • Liu S, Berns AE, Vereecken H, Wu D, Brüggemann N (2017a) Interactive effects of MnO2, organic matter and pH on abiotic formation of N2O from hydroxylamine in artificial soil mixtures. Sci Rep 7:39590

    CAS  Google Scholar 

  • Liu S, Han P, Hink L, Prosser JI, Wagner M, Brüggemann N (2017b) Abiotic conversion of extracellular NH2OH contributes to N2O emission during ammonia oxidation. Environ Sci Technol 51:13122–13132

    CAS  Google Scholar 

  • Liu S, Herbst M, Bol R, Gottselig N, Pütz T, Weymann D, Wiekenkamp I, Vereecken H, Brüggemann N (2016) The contribution of hydroxylamine content to spatial variability of N2O formation in soil of a Norway spruce forest. Geochim Cosmochim Acta 178:76–86

    CAS  Google Scholar 

  • Liu S, Lin F, Wu S, Cheng J, Sun Y, Jin Y, Li S, Li Z, Zou J (2017c) A meta-analysis of fertilizer-induced soil NO and combined with N2O emissions. Glob Chang Biol 23:2520–2532

    Google Scholar 

  • Liu S, Schloter M, Brüggemann N (2018) Accumulation of NO2− during periods of drying stimulates soil N2O emissions during subsequent rewetting. Eur J Soil Sci 69:936–946

    CAS  Google Scholar 

  • Liu S, Vereecken H, Brüggemann N (2014) A highly sensitive method for the determination of hydroxylamine in soils. Geoderma 232:117–122

    Google Scholar 

  • Loescher CR, Kock A, Koenneke M, Laroche J (2012) Production of oceanic nitrous oxide by ammonia-oxidizing archaea. Biogeosciences 9:2419–2429

    CAS  Google Scholar 

  • Medinets S, Skiba U, Rennenberg H, Butterbach-Bahl K (2015) A review of soil NO transformation: associated processes and possible physiological significance on organisms. Soil Biol Biochem 80:92–117

    CAS  Google Scholar 

  • Mothapo NV, Chen H, Cubeta MA, Shi W (2013) Nitrous oxide producing activity of diverse fungi from distinct agroecosystems. Soil Biol Biochem 66:94–101

    CAS  Google Scholar 

  • Norton JM, Stark JM (2011) Regulation and measurement of nitrification in terrestrial systems. Methods Enzymol 486:343–368

    CAS  Google Scholar 

  • Oikawa PY, Ge C, Wang J, Eberwein JR, Liang LL, Allsman LA, Grantz DA, Jenerette GD (2015) Unusually high soil nitrogen oxide emissions influence air quality in a high-temperature agricultural region. Nat Commun 6:8753

    CAS  Google Scholar 

  • Pilegaard K (2013) Processes regulating nitric oxide emissions from soils. Philosophical Transactions of the Royal Society B: Biological Sciences 368:20130126

    Google Scholar 

  • Spott O, Russow R, Stange CF (2011) Formation of hybrid N2O and hybrid N2 due to codenitrification: first review of a barely considered process of microbially mediated N-nitrosation. Soil Biol Biochem 43:1995–2011

    CAS  Google Scholar 

  • Terada A, Sugawara S, Hojo K, Takeuchi Y, Riya S, Harper WF Jr, Yamamoto T, Kuroiwa M, Isobe K, Katsuyama C (2017) Hybrid nitrous oxide production from a partial nitrifying bioreactor: hydroxylamine interactions with nitrite. Environ Sci Technol 51:2748–2756

    CAS  Google Scholar 

  • Tian H, Yang J, Xu R, Lu C, Canadell JG, Davidson EA, Jackson RB, Arneth A, Chang J, Ciais P, Gerber S, Ito A, Joos F, Lienert S, Messina P, Olin S, Pan S, Peng C, Saikawa E, Thompson RL, Vuichard N, Winiwarter W, Zaehle S, Zhang B (2019) Global soil nitrous oxide emissions since the preindustrial era estimated by an ensemble of terrestrial biosphere models: magnitude, attribution, and uncertainty. Glob Chang Biol 25:640–659

    Google Scholar 

  • Tierling J, Kuhlmann H (2018) Emissions of nitrous oxide (N2O) affected by pH-related nitrite accumulation during nitrification of N fertilizers. Geoderma 310:12–21

    CAS  Google Scholar 

  • Toyoda S, Mutobe H, Yamagishi H, Yoshida N, Tanji Y (2005) Fractionation of N2O isotopomers during production by denitrifier. Soil Biol Biochem 37:1535–1545

    CAS  Google Scholar 

  • Venterea RT, Rolston DEE, Cardon ZG (2005) Effects of soil moisture, physical, and chemical characteristics on abiotic nitric oxide production. Nutr Cycl Agroecosyst 72:27–40

    CAS  Google Scholar 

  • Wang X, Zou C, Gao X, Guan X, Zhang W, Zhang Y, Shi X, Chen X (2018) Nitrous oxide emissions in Chinese vegetable systems: a meta-analysis. Environ Pollut 239:375–383

    CAS  Google Scholar 

  • Wei J, Ibraim E, Brüggemann N, Vereecken H, Mohn J (2019) First real-time isotopic characterisation of N2O from chemodenitrification. Geochim Cosmochim Acta 267:17–32

    CAS  Google Scholar 

  • Wei W, Isobe K, Shiratori Y, Nishizawa T, Ohte N, Otsuka S, Senoo K (2014) N2O emission from cropland field soil through fungal denitrification after surface applications of organic fertilizer. Soil Biol Biochem 69:157–167

    CAS  Google Scholar 

  • Weiss RF, Price BA (1980) Nitrous oxide solubility in water and seawater. Mar Chem 8:347–359

    CAS  Google Scholar 

  • Wrage-Mönnig N, Horn MA, Well R, Müller C, Velthof G, Oenema O (2018) The role of nitrifier denitrification in the production of nitrous oxide revisited. Soil Biol Biochem 123:3–16

    Google Scholar 

  • Yamazaki T, Hozuki T, Arai K, Toyoda S, Koba K, Fujiwara T, Yoshida N (2014) Isotopomeric characterization of nitrous oxide produced by reaction of enzymes extracted from nitrifying and denitrifying bacteria. Biogeosciences 11:2679–2689

    CAS  Google Scholar 

  • Zacharia IG, Deen WM (2005) Diffusivity and solubility of nitric oxide in water and saline. Ann Biomed Eng 33:214–222

    Google Scholar 

Download references

Acknowledgments

We sincerely appreciate the anonymous reviewers and editors for their critical and valuable comments to help improve this manuscript.

Funding

This work was jointly supported by the National Natural Science Foundation of China (41977078, 41425005), the Special Fund for Agro-Scientific Research in the Public Interest (201503106), and the Postgraduate Research & Practice Innovation Program of Jiangsu Province, China (KYCX18_0678).

Author information

Authors and Affiliations

  1. Jiangsu Key Laboratory of Low Carbon Agriculture and GHGs Mitigation, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China

    Pengpeng Duan, Haojie Shen, Xueyang Jiang & Zhengqin Xiong

  2. Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, Hunan, China

    Pengpeng Duan

  3. State Key Lab of Soil and Sustainable Agriculture, Institute of Soil Sciences, Chinese Academy of Sciences, Nanjing, 210008, China

    Xiaoyuan Yan

Authors
  1. Pengpeng Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haojie Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xueyang Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaoyuan Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhengqin Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhengqin Xiong.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Hang-Wei Hu

Publisher’s note

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

Electronic supplementary material

ESM 1

(PDF 735 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Duan, P., Shen, H., Jiang, X. et al. The contributions of hydroxylamine and nitrite to NO and N2O production in alkaline and acidic vegetable soils. J Soils Sediments 20, 2903–2911 (2020). https://doi.org/10.1007/s11368-020-02645-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-020-02645-9

Keywords

Search

Navigation