Abstract
Purpose
Paddy fields are an important source of nitrous oxide (N2O) emission. The application of biochar or the nitrification inhibitor 3,4-dimethylpyrazole phosphate (DMPP) to paddy soils have been proposed as technologies to mitigate N2O emissions, but their mechanisms remain poorly understood.
Methods
An experiment was undertaken to study the combined and individual effects of biochar and DMPP on N2O emission from a paddy field. Changes in soil microbial community composition were investigated. Four fertilized treatments were established as follows: fertilizer only, biochar, DMPP, and biochar combined with DMPP; along with an unfertilized control.
Results
The application of biochar and/or DMPP decreased N2O emission by 18.9–39.6% compared with fertilizer only. The combination of biochar and DMPP exhibited higher efficiency at suppressing N2O emission than biochar alone but not as effective as DMPP alone. Biochar promoted the growth of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB), while DMPP suppressed AOB and increased AOA. Applying biochar with DMPP reduced the impact of DMPP on AOB. The nirS-/nirK- denitrifiers were decreased and nosZ-N2O reducers were increased by DMPP and the combination of DMPP and biochar. The abundance of the nirK gene was increased by biochar at the elongation and heading stages of rice development. Compared with fertilizer only, the application of biochar and/or DMPP promoted the abundance of nosZ genes.
Conclusion
These results suggest that applying biochar and/or DMPP to rice paddy fields is a promising strategy to reduce N2O emissions by regulating the dynamics of ammonia oxidizers and N2O reducers.
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References
Akiyama H, Yagi K, Yan XY (2005) Direct N2O emissions from rice paddy fields: summary of available data. Glob Biogeochem Cycles 19
Allen LH, Boote KJ, Jones JW, Jones PH, Valle RR, Acock B et al (1987) Response of vegetation to rising carbon dioxide: photosynthesis, biomass, and seed yield of soybean. Global Biogeochem Cy 1:1–14
Anderson CR, Condron LM, Clough TJ et al (2011) Biochar induced soil microbial community change: implications for biogeochemical cycling of carbon, nitrogen and phosphorus. Pedobiologia 54:309–320
Aulakh MS, Singh B (1997) Nitrogen losses and fertilizer N use efficiency in irrigated porous soils. Nutr Cycl Agroecosyst 7:1–16
Baggs EM, Smales CL, Bateman EJ (2010) Changing pH shifts the microbial source as well as the magnitude of N2O emission from soil. Biol Fertil Soils 46:793–805
Benckiser G, Christ E, Herbert T et al (2013) The nitrification inhibitor 3,4-dimethylpyrazole-phosphat (DMPP)-quantification and effects on soil metabolism. Plant Soil 371:257–266
Braker G, Fesefeldt A, Witzel KP (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 64:3769–3775
Cai ZC, Laughlin J (2001) Nitrous oxide and nitrogen emissions from soil under different water regimes and straw amendment. Chemosphere 42:11–19
Cayuela ML, van Zwieten L, Singh BP et al (2014) Biochar's role in mitigating soil nitrous oxide emissions: a review and meta-analysis. Agric Ecosyst Environ 191:5–16
Chen D, **ng W, Lan Z et al (2019) Direct and indirect effects of nitrogen enrichment on soil organisms and carbon and nitrogen mineralization in a semi-arid grassland. Funct Ecol 33:175–187
Conthe M, Wittorf L, Kuenen JG et al (2018) Growth yield and selection of nosZ clade II types in a continuous enrichment culture of N2O respiring bacteria. Environ Microbiol Rep 10:239–244
Di H, Cameron K, Shen JP et al (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624
Fan CH, Chen H, Li B et al (2017) Biochar reduces yield-scaled emissions of reactive nitrogen gases from vegetable soils across China. Biogeosciences 14:2851–2863
Fan X, Yin C, Chen H et al (2019) The efficacy of 3,4-dimethylpyrazole phosphate on N2O emissions is linked to niche differentiation of ammonia oxidizing archaea and bacteria across four arable soils. Soil Biol Biochem 130:82–93
Felber R, Leifeld J, Horak J et al (2014) Nitrous oxide emission reduction with greenwaste biochar: comparison of laboratory and field experiments. Eur J Soil Sci 65:128–138
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. Proceedings of the National Academy of Sciences of the United States of America 102:14683–14688
Granli T, Bøckman OC (1994) Nitrous oxide from agriculture. Norw J Agri Sci 12:1–128
Gregorutti VC, Caviglia OP (2017) Nitrous oxide emission after the addition of organic residues on soil surface. Agric Ecosyst Environ 246:234–242
Hallin S, Philippot L, Loffler FE et al (2018) Genomics and ecology of novel N2O-reducing microorganisms. Trends Microbiol 26:43–55
Harter J, Krause HM, Schuettler S et al (2014) Linking N2O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community. ISME J 8:660–674
Hatch D, Trindade H, Cardenas L et al (2005) Laboratory study of the effects of two nitrification inhibitors on greenhouse gas emissions from a slurry-treated arable soil: impact of diurnal temperature cycle. Biol Fertil Soils 41:225–232
He T, Liu D, Yuan J, Luo J et al (2018) Effects of application of inhibitors and biochar to fertilizer on gaseous nitrogen emissions from an intensively managed wheat field. Sci Total Environ 628-629:121–130
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
Hink L, Gubry-Rangin C, Nicol GW et al (2018) The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions. ISME J 12:1084–1093
Jacobson MZ (2005) Atmospheric pollution: history, science & regulation. Cambridge University Press, New York
Jia Z, Conard R (2009) Bacteria rather than Archaea dominate microbial ammoina oxidation in an agricultural soil. Environ Microbiol 11:1658–1671
Kleineidam K, Košmrlj K, Kublik S et al (2011) Infuence of the nitrification inibitor 3,4-dimethylpyrazolephosphate (DMPP) on ammonia-oxidizing bacteria and archaea in rhizosphere and bulk soil. Chemosphere 84:182–186
Knoblauch C, Maarifat AA, Pfeiffer EM et al (2011) Degradability of black carbon and its impact on trace gas fluxes and carbon turnover in paddy soils. Soil Biol Biochem 43:1768–1778
Levicnik-Hofferle S, Nicol GW, Ausec L et al (2012) Stimulation of thaumarchaeal ammonia oxidation by ammonia derived from organic nitrogen but not added inorganic nitrogen. FEMS Microbiol Ecol 80:114–123
Li XL, Zhang XY, Xu H et al (2009) Methane and nitrous oxide emissions from rice paddy soil as influenced by timing of application of hydroquinone and dicyandiamide. Nutr Cycl Agroecosyst 85:31–40
Li XL, Yuan WP, Xu H et al (2011) Effect of timing and duration of midseason aeration on CH4 and N2O emissions from irrigated lowland rice paddies in China. Nutr Cycl Agroecosyst 91:293–305
Li B, Fan CH, **ong ZQ et al (2015) The combined effects of nitrification inhibitor and biochar incorporation on yield-scaled N2O emissions from an intensively managed vegetable field in southeastern China. Biogeosciences 12:2003–2017
Lin Y, Ding W, Liu D et al (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
Ly P, Jensen L, Bruun T et al (2013) Methane (CH4) and nitrous oxide (N2O) emissions from the system of rice intensification (SRI) under a rain-fed lowland rice ecosystem in Cambodia. Nutr Cycl Agroecosyst 97:13–27
Ma J, Ma ED, Xu H et al (2009) Wheat straw management affects CH4 and N2O emissions from rice fields. Soil Biol Biochem 41:1022–1028
Maljanen M, Liikanen A, Silvola J et al (2003) Nitrous oxide emissions from boreal organic soil under different land-use. Soil Biol Biochem 35:689–700
Meng L, Ding W, Cai Z (2005) Long-term application of organic manure and nitrogen fertilizer on N2O emissions, soil quality and crop production in a sandy loam soil. Soil Biol Biochem 37:2037–2045
Pachauri RK, Allen MR, Barros VR et al (2014) Climate Change 2014: Synthesis Report. Contribution of Working Groups I. II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, IPCC, Geneva, Switzerland
Padhye LP (2017) Influence of surface chemistry of carbon materials on their interactions with inorganic nitrogen contaminants in soil and water. Chemosphere 184:532–547
Paranychianakis NV, Tsiknia M, Giannakis G et al (2013) Nitrogen cycling and relationships between ammonia oxidizers and denitrifiers in a clay-loam soil. Appl Microbiol Biotechnol 97:5507–5515
Rejesus RM, Mohanty S, Balatas JV (2012) Forecasting global rice consumption. http://www.agecon.purdue.edu/staff/balagtas/rice_timeseries_v6.pdf. Accessed 01 Mar 2014
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
Sarkhot DV, Berhe AA, Ghezzehei T (2012) Impact of biochar enriched with dairy manure effluent on carbon and nitrogen dynamics. J Environ Qual 41:1107–1114
Shcherbak I, Millar N, Robertson GP (2014) Global meta-analysis of the nonlinear response of soil nitrous oxide (N2O) emissions to fertilizer nitrogen. Proc Natl Acad Sci U S A 111:9199–9204
Shen J, Li R, Zhang F, Tang C, Rengel Z et al (2004) Crop yields, soil fertility and phosphorus fractions in response to long-term fertilization under the rice monoculture system on a calcareous soil. Field Crop Res 86:225–238
Shen T, Stieglmeier M, Dai J et al (2013) Responses of the terrestrial ammonia-oxidizing archaeon Ca. Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformis to nitrification inhibitors. FEMS Microbiol Lett 344:121–129
Shi XZ, Hu HW, Zhu-Barker X et al (2017) Nitrifier-induced denitrification is an important source of soil nitrous oxide and can be inhibited by a nitrification inhibitor 3,4-dimethylpyrazole phosphate. Environ Microbiol 19:4851–4865
Shin YK, Yun SH, Park ME et al (1996) Mitigation options for methane emission from rice fields in Korea. Ambio 25:289–291
Spokas KA, Cantrell KB, Novak JM et al (2012) Biochar: a synthesis of its agronomic impact beyond carbon sequestration. J Environ Qual 41:973–989
Steinbeiss S, Gleixner G, Antonietti M (2009) Effect of biochar amendment on soil carbon balance and soil microbial activity. Soil Biol Biochem 41:1301–1310
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
Wang C, Lu HH, Dong D et al (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
Wells NS, Baggs EM (2014) Char amendments impact soil nitrous oxide production during ammonia oxidation. Soil Sci Soc Am J 78:1656–1660
Wu YC, Lu L, Wang BZ et al (2011) Long-term field fertilization significantly alters community structure of ammonia-oxidizing bacteria rather than archaea in a paddy soil. Soil Sci Soc Am J 75:1431–1439
Wu KK, Gong P, Zhang LL et al (2019) Yield-scaled N2O and CH4 emissions as affected by combined application of stabilized nitrogen fertilizer and pig manure in rice fields. Plant Soil Environ 65:497–502
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
Yu L, Tang J, Zhang R et al (2013) Effects of biochar application on soil methane emission at different soil moisture levels. Biol Fertil Soils 49:119–128
Zhang AF, Bian RJ, Pan GX et al (2012) Effects of biochar amendment on soil quality, crop yield and greenhouse gas emission in a Chinese rice paddy: a field study of 2 consecutive rice growing cycles. Field Crop Res 127:153–160
Zhang K, Chen L, Li Y et al (2017) The effects of combinations of biochar, lime, and organic fertilizer on nitrification and nitrifiers. Biol Fertil Soils 53:77–87
Zheng J, Chen J, Pan G et al (2016) Biochar decreased microbial metabolic quotient and shifted community composition four years after a single incorporation in a slightly acid rice paddy from southwest China. Sci Total Environ 571:206–217
Funding
This study was financially supported by the National Natural Science Foundation of China (Nos. 41807107), the National Key Research and Development Program of China (Nos. 2017YFD0200708, 2018YFD0200200).
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Jie Li and Shuai Wang contributed to the work equally and should be regarded as co-first authors.
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Li, J., Wang, S., Luo, J. et al. Effects of biochar and 3,4-dimethylpyrazole phosphate (DMPP) on soil ammonia-oxidizing bacteria and nosZ-N2O reducers in the mitigation of N2O emissions from paddy soils. J Soils Sediments 21, 1089–1098 (2021). https://doi.org/10.1007/s11368-020-02811-z
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DOI: https://doi.org/10.1007/s11368-020-02811-z