Skip to main content

Advertisement

Log in

Effects of biochar on nitrification and denitrification-mediated N2O emissions and the associated microbial community in an agricultural soil

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Nitrous oxide (N2O) is a strong greenhouse gas, and it is of great significance for N2O reduction to study the effects of biochar on its production pathway. In this research, the contributions and mechanisms of biochar on autotrophic nitrification (ANF), heterotrophic nitrification (HNF), and denitrification (DF) to N2O emissions were studied by using 15N stable isotopes and high-throughput sequencing after laboratory incubation. The results showed that biochar addition at 2% (B2) significantly reduced the N2O emissions from the ANF by an average of 20.6%, while adding 5% biochar (B5) had no significant effect on the ANF. Both B2 and B5 significantly reduced the N2O emissions from the HNF by 15.7% and 13.2%, respectively, and reduced the N2O emissions from the DF by 40.9% and 11.7%, respectively. B2 enhanced the relative contribution rate of the ANF to N2O emissions by 6.3%, while B5 had little effect on it. Biochar addition significantly changed the copy numbers of the AOA and AOB, as well as the nirK, nirS, and nosZ genes, but it had no significant effect on the community composition of the AOA and had minimal effect on the AOB community. B2 significantly increased the abundance of the genus Rhodococcus of nirK type denitrifiers and had a significant effect on the relative abundance of Cupriavidus and Pseudomonas of the nosZ type denitrifiers. These results revealed that the inhibitory effects of biochar on N2O emissions from nitrification might be attributed to the direct immobilization and adsorption of inorganic N by biochar and to its promotion of the genus Rhodococcus of nirK-type denitrifiers and the genera Cupriavidus and Pseudomonas of the nosZ-type denitrifiers. The soil exchangeable NH4+-N and NO3-N concentrations were the primary factors affecting the N2O emission rates. These results help to elucidate the effects and mechanisms of biochar on N2O production pathways in agricultural soil.

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.

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

Similar content being viewed by others

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Azziz G, Monza J, Etchebehere C, Irisarri P (2017) nirS- and nirK-type denitrifier communities are differentially affected by soil type, rice cultivar and water management. Eur J Soil Biol 78:20–28

    CAS  Google Scholar 

  • Baggs EM (2008) A review of stable isotope techniques for N2O source partitioning in soils: recent progress, remaining challenges and future considerations. Rapid Commun Mass Sp 22:1664–1672

    CAS  Google Scholar 

  • Bateman EJ, Baggs EM (2005) Contributions of nitrification and denitrification to N2O emissions from soils at different water-filled pore space. Biol Fertil Soils 41:379–388

    CAS  Google Scholar 

  • Bi QF, Chen QH, Yang XR, Li H, Zheng BX, Zhou WW, Liu XX, Dai PB, Li KJ, Lin XY (2017) Effects of combined application of nitrogen fertilizer and biochar on the nitrification and ammonia oxidizers in an intensive vegetable soil. AMB Express 7:108

    Google Scholar 

  • Brassard P, Godbout S, Raghavan V (2016) Soil biochar amendment as a climate change mitigation tool: key parameters and mechanisms involved. J Environ Manag 181:484–497

    CAS  Google Scholar 

  • Buckingham S, Anthony S, Bellamy PH, Cardenas LM, Higgins S, Mcgeough K, Topp CFE (2014) Review and analysis of global agricultural N2O emissions relevant to the UK. Sci Total Environ 487:164–172

    CAS  Google Scholar 

  • Butterbachbahl 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

    Google Scholar 

  • Case SDC, Mcnamara NP, Reay DS, Stott AW, Grant HK, Whitaker J (2015) Biochar suppresses N2O emissions while maintaining N availability in a sandy loam soil. Soil Biol Biochem 81:178–185

    CAS  Google Scholar 

  • Case SDC, Uno H, Nakajima Y, Jensen LS, Akiyama H (2017) Bamboo biochar does not affect paddy soil N2O emissions or source following slurry or mineral fertilizer amendment-a 15N tracer study. J Plant Nutr Soil Sci 181:90–98

    Google Scholar 

  • Cayuela ML, Van Zwieten L, Singh BP, Jeffery S, Roig A, Sánchez-Monedero MA (2014) Biochar’s role in mitigating soil nitrous oxide emissions: a review and meta-analysis. Agric Ecosyst Environ 191:5–16

    CAS  Google Scholar 

  • Chen J, Liu X, Zheng J, Zhang B, Lu H, Chi Z, Pan G, Li L, Zheng J, Zhang X, Wang J, Yu X (2013) Biochar soil amendment increased bacterial but decreased fungal gene abundance with shifts in community structure in a slightly acid rice paddy from southwest China. Appl Soil Ecol 71:33–44

    Google Scholar 

  • Cole JR, Wang Q, Fish JA, Chai BL, Mcgarrell DM, Sun YN, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633–D642

    CAS  Google Scholar 

  • Cui PY, Fan FL, Yin C, Song A, Huang PR, Tang YJ, Zhu P, Peng C, Li TQ, Wakeline SA, Liang YC (2016) Long–term organic and inorganic fertilization alters temperature sensitivity of potential N2O emissions and associated microbes. Soil Biol Biochem 93:131–141

    CAS  Google Scholar 

  • Davidson EA (2009) The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860. Nat Geosci 2:659–662

    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 

  • Domeignoz-Horta LA, Spor A, Bru D, Breuil MC, Bizouard F, Léonard J, Philippot L (2015) The diversity of the N2O reducers matters for the N2O:N2 denitrification end-product ratio across an annual and a perennial cropping system. Front Microbiol 6:971

    Google Scholar 

  • Duan P, Song Y, Li S, Xiong Z (2019a) Responses of N2O production pathways and related functional microbes to temperature across greenhouse vegetable field soils. Geoderma 355:113904

    CAS  Google Scholar 

  • Duan P, Zhou J, Feng L, Jansen-Willems AB, Xiong Z (2019b) Pathways and controls of N2O production in greenhouse vegetable production soils. Biol Fertil Soils 55:285–297

    CAS  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    CAS  Google Scholar 

  • Fan C, Chen H, Li B, Xiong Z (2017) Biochar reduces yield-scaled emissions of reactive nitrogen gases from vegetable soils across China. Biogeosciences 14:1–27

    Google Scholar 

  • Garrido JM, Fdz-Polanco M, Fdz-Polanco F (2013) Working with energy and mass balances: a conceptual framework to understand the limits of municipal wastewater treatment. Water Sci & Technol 67:2294–2301

    CAS  Google Scholar 

  • Gao D, Liu FQ, Xie Y, Liang H (2018) Temporal and spatial distribution of ammonia-oxidizing organisms of two types of wetlands in northeast China. Appl Microbiol Biotechnol 102:7195–7205

    CAS  Google Scholar 

  • Gill SR, Pop M, DeBoy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359

    CAS  Google Scholar 

  • Guo L, Wang X, Diao T, Ju X, Niu X, Zheng L, Zhang X, Han X (2018) N2O emission contributions by different pathways and associated microbial community dynamics in a typical calcareous vegetable soil. Environ Pollut 242:2005–2013

    CAS  Google Scholar 

  • Hallin S, Lindgren PE (1999) PCR detection of genes encoding nitrile reductase in denitrifying bacteria. Appl Environ Microbiol 65:1652–1657

    CAS  Google Scholar 

  • Harter J, Krause HM, Schuettler S, Ruser R, Fromme M, Scholten T, Kappler A, Behrens S (2014) Linking N2O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community. ISME J 8:660–674

    CAS  Google Scholar 

  • Harter J, Guzman-Bustamante I, Kuehfuss S, Ruser R, Well R, Spott O, Kappler A, Behrens S (2016) Gas entrapment and microbial N2O reduction reduce N2O emissions from a biochar-amended sandy clay loam soil. Sci Rep 6:39574

    CAS  Google Scholar 

  • Harter J, El-Hadid M, Huson DH, Kappler A, Behrens S (2017) Soil biochar amendment affects the diversity of nosZ transcripts: implications for N2O formation. Sci Rep 7:3338

    Google Scholar 

  • He JZ, Ge Y, Xu Z, Chen C (2009) Linking soil bacterial diversity to ecosystem multifunctionality using backward-elimination boosted trees analysis. J Soils Sediments 9:547–554

    CAS  Google Scholar 

  • 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 39:729–749

    CAS  Google Scholar 

  • Islam A, Chen D, White RE (2007) Heterotrophic and autotrophic nitrification in two acid pasture soils. Soil Biol Biochem 39:972–975

    CAS  Google Scholar 

  • Jones CM, Spor A, Brennan FP, Breuil MC, Bru D, Lemanceau P, Griffiths B, Hallin S, Philippot L (2014) Recently identified microbial guild mediates soil N2O sink capacity. Nat Clim Chang 4:801–805

    CAS  Google Scholar 

  • Kloos K, Mergel A, Rösch C, Bothe H (2001) Denitrification within the genus Azospirillum and other associative bacteria. Funct Plant Biol 28:991–998

    Google Scholar 

  • Krause HM, Hüppi R, Leifeld J, El-Hadidi M, Harter J, Kappler A, Hartmanne M, Behrensf S, Mäder P, Gattinger A (2018) Biochar affects community composition of nitrous oxide reducers in a field experiment. Soil Biol Biochem 119:143–151

    CAS  Google Scholar 

  • Levy-Booth DJ, Prescott CE, Grayston SJ (2014) Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems. Soil Biol Biochem 75:11–25

    CAS  Google Scholar 

  • Li S, Song L, Jin Y, Liu S, Shen Q, Zou J (2016) Linking N2O emission from biochar-amended composting process to the abundance of denitrify (nirK and nosZ) bacteria community. AMB Express 6:37

    CAS  Google Scholar 

  • Li W, Sun Y, Li G, Liu Z, Wang H, Zhang D (2017) Contributions of nitrification and denitrification to N2O emissions from aged refuse bioreactor at different feeding loads of ammonia substrates. Waste Manag 68:319–328

    CAS  Google Scholar 

  • Lin Y, Ding W, Liu D, He T, Yoo G, Yuan J, Chen Z, Fan J (2017) Wheat straw-derived biochar amendment stimulated N2O emissions from rice paddy soils by regulating the amoA genes of ammonia-oxidizing bacteria. Soil Biol Biochem 113:89–98

    CAS  Google Scholar 

  • Liu B, Frostegard A, Bakken LR (2014) Impaired reduction of N2O to N2 in acid soils is due to a posttranscriptional interference with the expression of nosZ. mBio 5:e01383–e01314

    Google Scholar 

  • Liu XR, Ren JQ, Zhang QW, Liu C (2019) Long-term effects of biochar addition and straw return on N2O fluxes and the related functional genes abundances under wheat-maize rotation system in the North China Plain. Appl Soil Ecol 135:44–55

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Müller C, Laughlin RJ, Spott O, Rütting T (2014) Quantification of N2O emission pathways via a 15N tracing model. Soil Boil Biochem 72:44–54

    Google Scholar 

  • Németh DD, Wagner-Riddle C, Dunfield KE (2014) Abundance and gene expression in nitrifier and denitrifier communities associated with a field scale spring thaw N2O flux event. Soil Biol Biochem 73:1–9

    Google Scholar 

  • Nguyen DH, Scheer C, Rowlings DW, Grace PR (2016) Rice husk biochar and crop residue amendment in subtropical cropping soils: effect on biomass production, nitrogen use efficiency and greenhouse gas emissions. Biol Fertil Soils 52:261–270

    Google Scholar 

  • Orellana LH, Rodriguezr LM, Higgins S, Cheesanford JC, Sanford RA, Ritalahti KM, Löffler FE, Konstantinidis KT (2014) Detecting nitrous oxide reductase (nosZ) genes in soil metagenomes: method development and implications for the nitrogen cycle. mBio 5:01193–01114

    Google Scholar 

  • Park SJ, Park BJ, Rhee SK (2008) Comparative analysis of archaeal 16S rRNA and amoA genes to estimate the abundance and diversity of ammonia-oxidizing archaea inmarine sediments. Extremophiles 12:605–615

    CAS  Google Scholar 

  • Pereira EIP, Suddick EC, Mansour I, Mukome FND, Parikh SJ, Scow K, Six J (2015) Biochar alters nitrogen transformations but has minimal effects on nitrous oxide emissions in an organically managed lettuce mesocosm. Biol Fertil Soils 51:573–582

    CAS  Google Scholar 

  • Qin S, Hu C, Clough TJ, Luo J, Oenema O, Zhou S (2017) Irrigation of DOC-rich liquid promotes potential denitrification rate and decreases N2O/(N2O+N2) product ratio in a 0–2 m soil profile. Soil Biol Biochem 106:1–8

    CAS  Google Scholar 

  • Qin S, Hu C, Clough TJ, Luo J, Oenema O, Zhou S (2019) Electrodes donate electrons for nitrate reduction in a soil matrix via DNRA and denitrification. Environ Sci Technol 53:2002–2012

    CAS  Google Scholar 

  • Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125

    CAS  Google Scholar 

  • Robertson WD (2010) Nitrate removal rates in woodchip media of varying age. Ecol Eng 36:1581–1587

    Google Scholar 

  • 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. Appl Environ Microbiol 63:4704–4712

    CAS  Google Scholar 

  • Saarenheimo J, Rissanen AJ, Arvola L, Nykänen H, Lehmann MF, Tiirola M (2015) Genetic and environmental controls on nitrous oxide accumulation in lakes. PLoS One 10:e0121201

    Google Scholar 

  • Sánchez-García M, Roig A, Sánchez-Monedero MA, Cayuela ML (2014) Biochar increases soil N2O emissions produced by nitrification-mediated pathways. Front Environ Sci 2:25

    Google Scholar 

  • Shi YL, Liu XR, Zhang QW (2019) Effects of combined biochar and organic fertilizer on nitrous oxide fluxes and the related nitrifier and denitrifier communities in a saline-alkali soil. Sci Total Environ 686:199–211

    CAS  Google Scholar 

  • Shi YL, Liu XR, Zhang QW, Gao PL, Ren JQ (2020) Biochar and organic fertilizer changed the ammonia-oxidizing bacteria and archaea community structure of saline-alkali soil in the North China Plain. J Soils Sediments 20:12–23

    CAS  Google Scholar 

  • Snider D, Thompson K, Wagner-Riddle C, Spoelstra J, Dunfield K (2015) Molecular techniques and stable isotope ratios at natural abundance give complementary inferences about N2O production pathways in an agricultural soil following a rainfall event. Soil Biol Biochem 88:197–213

    CAS  Google Scholar 

  • Stevens RJ, Laughlin RJ, Atkins GJ, Prosser SJ (1993) Automated determination of nitrogen-15-labeled dinitrogen and nitrous oxide by mass spectrometry. Soil Sci Soc Am J 57:981–988

    CAS  Google Scholar 

  • Suddick EC, Six J (2013) An estimation of annual nitrous oxide emissions and soil quality following the amendment of high temperature walnut shell biochar and compost to a small scale vegetable crop rotation. Sci Total Environ 465:298–307

    CAS  Google Scholar 

  • Tan G, Wang H, Xu N, Liu H, Zhai L (2018) Biochar amendment with fertilizers increases peanut N uptake, alleviates soil N2O emissions without affecting NH3 volatilization in field experiments. Environ Sci Pollut Res 25:1–10

    Google Scholar 

  • Tao R, Wakelin SA, Liang YC, Hu BW, Chu GX (2018) Nitrous oxide emission and denitrifier communities in drip–irrigated calcareous soil as affected by chemical and organic fertilizers. Sci Total Environ 612:739–749

    CAS  Google Scholar 

  • Uchida Y, Rein I, Akiyama H, Yagi K (2013) Contribution of nitrification and denitrification to nitrous oxide emissions in andosol and from fluvisol after coated urea application. Soil Sci Plant Nutr 59:46–55

    CAS  Google Scholar 

  • Wang C, Lu HH, Dong D, Deng H, Strong PJ, Wang HL, Wu WX (2013) Insight into the effects of biochar on manure composting: evidence supporting the relationship between N2O emission and denitrifying community. Environ Sci Technol 47:7341–7349

    CAS  Google Scholar 

  • Wang XJ, Jia MS, Zhang H, Pan SQ, Kao CM, Chen SH (2016) Quantifying N2O emissions and production pathways from fresh waste during the initial stage of disposal to a landfill. Waste Manag 63:3–10

    Google Scholar 

  • Wang W, Liu W, Wang S, Wang M, Long XE, Zhu G (2019) Abundance, contribution, and possible driver of ammonia-oxidizing archaea (AOA) in various types of aquatic ecosystems. J. Soils Sediments 19:2114–2125

    CAS  Google Scholar 

  • Webster FA, Hopkins DW (1996) Contributions from different microbial processes to N2O emission from soil under different moisture regimes. Biol Fertil Soils 22:331–335

    CAS  Google Scholar 

  • Wei W, Isobe K, Nishizawa T, Zhu L, Shiratori Y, Ohte N, Koba K, Otsuka S, Senoo K (2015) Higher diversity and abundance of denitrifying microorganisms in environments than considered previously. ISME J 9:1954–1965

    CAS  Google Scholar 

  • Wu H, Zeng G, Liang J, Chen J, Xu J, Dai J, Li X, Chen M, Xu P, Zhou Y, Li F, Hu L, Wan J (2016) Responses of bacterial community and functional marker genes of nitrogen cycling to biochar, compost and combined amendments in soil. Appl Microbiol Biotechnol 100:8583–8591

    CAS  Google Scholar 

  • Xu HJ, Wang XH, Li H, Yao HY, Su JQ, Zhu YG (2014) Biochar impacts soil microbial community composition and nitrogen cycling in an acidic soil planted with rape. Environ Sci Technol 48:9391–9399

    CAS  Google Scholar 

  • Xu X, Liu X, LiY RY, Liu Y, Zhang Q, Li Z, He Y, Xu J, Di H (2017) High temperatures inhibited the growth of soil bacteria and archaea but not that of fungi and altered nitrous oxide production mechanisms from different nitrogen sources in an acidic soil. Soil Biol Biochem 107:168–179

    CAS  Google Scholar 

  • Yanai Y, Toyota K, Okazaki M (2007) Effects of charcoal addition on N2O emissions from soil resulting from rewetting air-dried soil in short-term laboratory experiments. Soil Sci Plant Nutr 53:181–188

    CAS  Google Scholar 

  • Yang Y, Hu Y, Wang Z, Zeng Z (2018) Variations of the nirS-, nirK-, and nosZ-denitrifying bacterial communities in a northern Chinese soil as affected by different long-term irrigation regimes. Environ Sci Pollut Res 25:14057–14067

    CAS  Google Scholar 

  • Yao Y, Gao B, Zhang M, Inyang M, Zimmerman AR (2012) Effect of biochar amendment on sorption and leaching of nitrate, ammonium, and phosphate in a sandy soil. Chemosphere 89:1467–1471

    CAS  Google Scholar 

  • Yin C, Fan FL, Song A, Li ZJ, Yu WT, Liang YC (2014) Different denitrification potential of aquic brown soil in Northeast China under inorganic and organic fertilization accompanied by distinct changes of nirS-and nirK-denitrifying bacterial community. Eur J Soil Biol 65:47–56

    CAS  Google Scholar 

  • Yoo G, Lee YO, Won TJ, Hyun JG, Ding W (2018) Variable effects of biochar application to soils on nitrification-mediated N2O emissions. Sci Total Environ 626:603–611

    CAS  Google Scholar 

  • Yuan H, Zhang Z, Li M, Clough T, Wrage-Mönnig N, Qin S, Ge T, Liao H, Zhou S (2019) Biochar’s role as an electron shuttle for mediating soil N2O emissions. Soil Biol Biochem 133:94–96

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Zhao S, Zhou J, Yuan D, Wang W, Zhou L, Pi Y, Zhu G (2020) NirS-type N2O-producers and nosZ II-type N2O-reducers determine the N2O emission potential in farmland rhizosphere soils. J. Soils Sediments 20:461–471

    Google Scholar 

  • Zhou ZF, Zheng YM, Shen JP, Zhang LM, He JZ (2011) Response of denitrification genes nirS, nirK, and nosZ to irrigation water quality in a Chinese agricultural soil. Environ Sci Pollut Res 18:1644–1652

    CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the National Natural Science Foundation of China (No. 41773090) for financial support.

Funding

The research was financially supported by the National Natural Science Foundation of China (No. 41773090).

Author information

Authors and Affiliations

Authors

Contributions

LXR planned and designed research; SYL and ZQW conducted experiments; SYL and LGC conducted chemical analysis; LXR and SYL conducted statistical analysis and wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Xingren Liu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Responsible editor: Zhihong Xu

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

Liu, X., Shi, Y., Zhang, Q. et al. Effects of biochar on nitrification and denitrification-mediated N2O emissions and the associated microbial community in an agricultural soil. Environ Sci Pollut Res 28, 6649–6663 (2021). https://doi.org/10.1007/s11356-020-10928-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-10928-4

Keywords

Navigation