Skip to main content
Log in

Crop residue carbon-to-nitrogen ratio regulates denitrifier N2O production post flooding

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

The response of nitrifier and denitrifier populations and associated N2O emissions to different carbon-to-nitrogen (C/N = 17 or 45) straw amendments was monitored under flooding-drying and non-flooding conditions. A 10-week laboratory mesocosm study was conducted in two soils, (i) a paddy soil with a long history of managed flooding-drying (CN), and (ii) a wheat cropping soil with no previous history of flooding (UK). We measured N2O fluxes and the abundances of ammonia-oxidizing archaea (AOA) and bacteria (AOB), nitrite reductase (nirK and nirS) genes, and nitrous oxide reductase (nosZI and nosZII) genes during flooding (4 weeks) and post-flooding (6 weeks). Straw addition enhanced N2O emissions, with higher fluxes apparent after incorporation of narrow C/N residues. Moreover, the impact of crop amendment on N2O emission was exacerbated when soil was under flooding-drying conditions. The abundances of nirS and nosZI genes in CN soil and AOA gene in UK soil were increased by straw amendment, with highest in narrow C/N straw amendments. Structural equation modeling showed that the impact of denitrifier gene abundance on the N2O flux was stronger than that of nitrifier gene abundance in the two soils, and significant correlations were observed between N2O fluxes and the consumption of DOC and NO3, indicating that denitrification was the dominant N2O production pathway during the drying phase. The ratio of (nirS + nirK)/(nosZI + nosZII) in the narrow C/N amendment was greater than in the wide C/N treatment after flooding, suggesting that the straw C/N ratio had an effect on the capacity for N2O production via denitrification. We conclude that crop amendments with an appropriate C/N ratio could minimize N2O fluxes through regulating the denitrification process when soils are subjected to regular flooding and drying and also experiencing greater frequencies of flooding.

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
Fig. 6

Similar content being viewed by others

References

  • Abalos D, Sanz-Cobena A, Garcia-Torres L, Van Groenigen JW, Vallejo A (2013) Role of maize Stover incorporation on nitrogen oxide emissions in a non-irrigated Mediterranean barley field. Plant Soil 364:357–371

    CAS  Google Scholar 

  • Adair KL, Schwartz E (2008) Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of northern Arizona, USA. Microb Ecol 56:420–426

    CAS  PubMed  Google Scholar 

  • AHBD Agriculture & Horticulture Development Board Badagliacca G, Ruisi P, Rees RM, Saia S (2017) An assessment of factors controlling N2O and CO2 emissions from crop residues using different measurement approaches. Biol Fertil Soils 53:547–561

    Google Scholar 

  • Badagliacca G, Ruisi P, Rees RM, Saia S (2017) An assessment of factors controlling N2O and CO2 emissions from crop residues using different measurement approaches. Biol Fertil Soils 53(5):547–561

  • Barton L, Kiese R, Gatter D, Butterbach-Bahl K, Buck R, Hinz C, Murphy DV (2008) Nitrous oxide emissions from a cropped soil in a semi-arid climate. Glob Chang Biol 14:177–192

    Google Scholar 

  • Beniston M, Stephenson DB, Christensen OB, Ferro CA, Frei C, Goyette S, Halsnaes K, Holt T, Jylhä K, Koffi B (2007) Future extreme events in European climate: an exploration of regional climate model projections. Clim Chang 81:71–95

    Google Scholar 

  • Blake G, Hartge K (1986) Particle density Methods of soil analysis: part 1 physical and mineralogical methods. 5:377–382

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108:4516–4522

    CAS  PubMed  Google Scholar 

  • Chen H, Li X, Hu F, Shi W (2013) Soil nitrous oxide emissions following crop residue addition: a meta-analysis. Glob Chang Biol 19:2956–2964

    PubMed  Google Scholar 

  • Chen L, Zhang J, Zhao B, Yan P, Zhou G, Xin X (2014) Effects of straw amendment and moisture on microbial communities in Chinese fluvo-aquic soil. J Soils Sediments 14:1829–1840

    CAS  Google Scholar 

  • Cheng Y, Wang J, Wang J, Chang SX, Wang S (2017) The quality and quantity of exogenous organic carbon input control microbial NO3 immobilization: a meta-analysis. Soil Biol Biochem:357–363

  • Congreves K, Wagner-Riddle C, Si B, Clough T (2018) Nitrous oxide emissions and biogeochemical responses to soil freezing-thawing and drying-wetting. Soil Biol Biochem 117:5–15

    CAS  Google Scholar 

  • Datta R, Vranová V, Pavelka M, Rejšek K, Formánek P (2014) Effect of soil sieving on respiration induced by low-molecular-weight substrates. Int Agrophys 28:119–124

    CAS  Google Scholar 

  • Dobbie KE, Smith KA (2003) Nitrous oxide emission factors for agricultural soils in Great Britain: the impact of soil water-filled pore space and other controlling variables. Glob Chang Biol 9:204–218

    Google Scholar 

  • FAO (2015) World reference base for soil resources 2014. World soil resources reports 106 Food and Agriculture Organization of the United Nations, Rome

  • 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 102:14683–14688

    CAS  PubMed  Google Scholar 

  • Frimpong KA, Baggs E (2010) Do combined applications of crop residues and inorganic fertilizer lower emission of N2O from soil? Soil Use Manag 26:412–424

    Google Scholar 

  • Gao J, Xie Y, Jin H, Liu Y, Bai X, Ma D, Zhu Y, Wang C, Guo T (2016) Nitrous oxide emission and denitrifier abundance in two agricultural soils amended with crop residues and urea in the North China Plain. PLoS One 11:e0154773

    PubMed  PubMed Central  Google Scholar 

  • Hai B, Diallo NH, Sall S, Haesler F, Schauss K, Bonzi M, Assigbetse K, Chotte J-L, Munch JC, Schloter M (2009) Quantification of key genes steering the microbial nitrogen cycle in the rhizosphere of sorghum cultivars in tropical agroecosystems. Appl Environ Microbiol 75:4993–5000

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison-Kirk T, Beare M, Meenken E, Condron L (2013) Soil organic matter and texture affect responses to dry/wet cycles: effects on carbon dioxide and nitrous oxide emissions. Soil Biol Biochem 57:43–55

    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

    CAS  PubMed  Google Scholar 

  • Hartmann M, Frey B, Mayer J, Mäder P, Widmer F (2015) Distinct soil microbial diversity under long-term organic and conventional farming. ISME J 9:1177

    PubMed  Google Scholar 

  • Henry S, Baudoin E, López-Gutiérrez JC, Martin-Laurent F, Brauman A, Philippot L (2004) Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J Microbiol Methods 59:327–335

    CAS  PubMed  Google Scholar 

  • Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72:5181–5189

    CAS  PubMed  PubMed Central  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  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • IPCC (2013) Climate change 2013: the physical science basis. Cambridge University Press, Cambridge

    Google Scholar 

  • Jones CM, Graf DR, Bru D, Philippot L, Hallin S (2013) The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J 7:417–426

    CAS  PubMed  Google Scholar 

  • Kettler T, Doran JW, Gilbert T (2001) Simplified method for soil particle-size determination to accompany soil-quality analyses. Soil Sci Soc Am J 65:849–852

    CAS  Google Scholar 

  • Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529

    CAS  PubMed  Google Scholar 

  • Li X, Hu F, Shi W (2013) Plant material addition affects soil nitrous oxide production differently between aerobic and oxygen-limited conditions. Appl Soil Ecol 64:91–98

    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 

  • Macdonald CA, Clark IM, Hirsch PR, Zhao F-J, McGrath SP (2011) Development of a real-time PCR assay for detection and quantification of Rhizobium leguminosarum bacteria and discrimination between different biovars in zinc-contaminated soil. Appl Environ Microbiol 77:4626–4633

    CAS  PubMed  PubMed Central  Google Scholar 

  • MacKenzie A, Fan M, Cadrin F (1998) Nitrous oxide emission in three years as affected by tillage, corn-soybean-alfalfa rotations, and nitrogen fertilization. J Environ Qual 27:698–703

    CAS  Google Scholar 

  • Marsden KA, Jones DL, Chadwick DR (2017) DMPP is ineffective at mitigating N2O emissions from sheep urine patches in a UK grassland under summer conditions. Agric Ecosyst Environ 246:1–11

    CAS  Google Scholar 

  • Martins CS, Nazaries L, Macdonald CA, Anderson IC, Singh BK (2015) Water availability and abundance of microbial groups are key determinants of greenhouse gas fluxes in a dryland forest ecosystem. Soil Biol Biochem 86:5–16

    CAS  Google Scholar 

  • Miller M, Zebarth B, Dandie C, Burton D, Goyer C, Trevors J (2008) Crop residue influence on denitrification, N2O emissions and denitrifier community abundance in soil. Soil Biol Biochem 40:2553–2562

    CAS  Google Scholar 

  • Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5:62–71

    CAS  PubMed  Google Scholar 

  • Nannipieri P, Penton C, Purahong W, Schloter M, van Elsas J (2019) Recommendations for soil microbiome analyses. Biol Fertil Soils 55:765–766

    Google Scholar 

  • Nguyen TT, Marschner P (2016) Soil respiration, microbial biomass and nutrient availability in soil after repeated addition of low and high C/N plant residues. Biol Fertil Soils 52:165–176

    CAS  Google Scholar 

  • Qin H, Tang Y, Shen J, Wang C, Chen C, Yang J, Liu Y, Chen X, Li Y, Hou H (2018) Abundance of transcripts of functional gene reflects the inverse relationship between CH4 and N2O emissions during mid-season drainage in acidic paddy soil. Biol Fertil Soils 54:885–895

    Google Scholar 

  • Rasmussen R (2001) Quantification on the LightCycler. Rapid cycle real-time PCR. Springer, Berlin, pp 21–34

    Google Scholar 

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

    CAS  PubMed  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  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Rodríguez AR, Hill PW, Chadwick DR, Jones DL (2017) Crop residues exacerbate the negative effects of extreme flooding on soil quality. Biol Fertil Soils 53:751–765

    PubMed  PubMed Central  Google Scholar 

  • Sánchez-Rodríguez AR, Chadwick DR, Tatton GS, Hill PW, Jones DL (2018) Comparative effects of prolonged freshwater and saline flooding on nitrogen cycling in an agricultural soil. Appl Soil Ecol 125:56–70

    Google Scholar 

  • Sánchez-Rodríguez AR, Nie C, Hill PW, Chadwick DR, Jones DL (2019) Extreme flood events at higher temperatures exacerbate the loss of soil functionality and trace gas emissions in grassland. Soil Biol Biochem 130:227–236

    Google Scholar 

  • Schiermeier Q (2011) Increased flood risk linked to global warming. Nature Publishing Group, City, State

    Google Scholar 

  • Senbayram M, Chen R, Mühling KH, Dittert K (2009) Contribution of nitrification and denitrification to nitrous oxide emissions from soils after application of biogas waste and other fertilizers. Rapid Commun Mass Spectrom 23:2489–2498

    CAS  PubMed  Google Scholar 

  • Sengupta A, Dick WA (2015) Bacterial community diversity in soil under two tillage practices as determined by pyrosequencing. Microb Ecol 70:853–859

    PubMed  Google Scholar 

  • Song K, Lee SH, Mitsch WJ, Kang H (2010) Different responses of denitrification rates and denitrifying bacterial communities to hydrologic pulsing in created wetlands. Soil Biol Biochem 42:1721–1727

    CAS  Google Scholar 

  • Sun X, Han X, Ping F, Zhang L, Zhang K, Chen M, Wu W (2018) Effect of rice-straw biochar on nitrous oxide emissions from paddy soils under elevated CO2 and temperature. Sci Total Environ 628:1009–1016

    PubMed  Google Scholar 

  • Thomson AJ, Giannopoulos G, Pretty J, Baggs EM, Richardson DJ (2012) Biological sources and sinks of nitrous oxide and strategies to mitigate emissions. R Soc

  • Throbäck IN, Enwall K, Jarvis Å, Hallin S (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol Ecol 49:401–417

    PubMed  Google Scholar 

  • Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart—how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484

    Google Scholar 

  • Wagg C, Bender SF, Widmer F, van der Heijden MG (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci 111:5266–5270

    CAS  PubMed  Google Scholar 

  • Whelan JA, Russell NB, Whelan MA (2003) A method for the absolute quantification of cDNA using real-time PCR. J Immunol Methods 278:261–269

    CAS  PubMed  Google Scholar 

  • Wilson J, Baldwin D, Rees G, Wilson B (2011) The effects of short-term inundation on carbon dynamics, microbial community structure and microbial activity in floodplain soil. River Res Appl 27:213–225

    Google Scholar 

  • Xu X, Ran Y, Li Y, Zhang Q, Liu Y, Pan H, Guan X, Li J, Shi J, Dong L (2016) Warmer and drier conditions alter the nitrifier and denitrifier communities and reduce N2O emissions in fertilized vegetable soils. Agric Ecosyst Environ 231:133–142

    CAS  Google Scholar 

  • Yang L, Zhang X, Ju X (2017) Linkage between N2O emission and functional gene abundance in an intensively managed calcareous fluvo-aquic soil. Sci Rep 7:43283

    PubMed  PubMed Central  Google Scholar 

  • Yuan Y, Dai X, Xu M, Wang H, Fu X, Yang F (2015) Responses of microbial community structure to land-use conversion and fertilization in southern China. Eur J Soil Biol 70:1–6

    Google Scholar 

  • Zhang W, Liang C, Kao-Kniffin J, He H, Xie H, Zhang X (2017) Effects of drying and wetting cycles on the transformations of extraneous inorganic N to soil microbial residues. Sci Rep 7:9477

    PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Ding H, Zheng X, Cai Z, Misselbrook T, Carswell A, Müller C, Zhang J (2018) Soil N transformation mechanisms can effectively conserve N in soil under saturated conditions compared to unsaturated conditions in subtropical China. Biol Fertil Soils 54:495–507

    CAS  Google Scholar 

  • Zhao B, Zhang J, Yu Y, Karlen DL, Hao X (2016) Crop residue management and fertilization effects on soil organic matter and associated biological properties. Environ Sci Pollut Res 23:17581–17591

    CAS  Google Scholar 

  • Zhong L, Du R, Ding K, Kang X, Li FY, Bowatte S, Hoogendoorn CJ, Wang Y, Rui Y, Jiang L, Wang S (2014) Effects of grazing on N2O production potential and abundance of nitrifying and denitrifying microbial communities in meadow-steppe grassland in northern China. Soil Biol Biochem:1–10

  • Zhou W, Lin S, Wu L, Zhao JS, Wang ML, Zhu B, Mo YL, Hu RG, Chadwick D, Shaaban M (2017) Substantial N2O emission during the initial period of the wheat season due to the conversion of winter-flooded paddy to rice-wheat rotation. Atmos Environ 170:269–278

    CAS  Google Scholar 

Download references

Acknowledgments

This study was financed by UK-China Virtual Joint Centre for Agricultural Nitrogen (CINAg) funded by the Newton Fund via UK BBSRC/NERC (BB/N013468/1). We would like to thank the Bangor University, Rothamsted Research, and China Scholarship Council which supported the research in the UK.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ronggui Hu.

Additional information

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 142 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, W., Jones, D.L., Hu, R. et al. Crop residue carbon-to-nitrogen ratio regulates denitrifier N2O production post flooding. Biol Fertil Soils 56, 825–838 (2020). https://doi.org/10.1007/s00374-020-01462-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-020-01462-z

Keywords

Navigation