Abstract
Combined application of organic amendment with synthetic fertilizer is an emerging management technique for maximized agronomic benefits without drastic soil health effects. However, little attention has been paid to the environmental costs of such management as the primary focus has remained on agronomic outcomes. In present study, we investigated the impacts of three organic amendments including dairy cattle manure (20 t/ha), poultry manure (20 t/ha), and a biochar (30 t/ha) applied along with urea (55 kg-N/ha) on soil N2O fluxes and explored the mechanisms behind N2O emissions. Plots with urea-only application were used as a control. For source partitioning of soil-emitted N2O, we used isotopocule mapping approach. The results showed significantly higher N2O emission rates from manure-treated plots compared with biochar or control treatments plots. The cumulative N2O emissions rates for 125 days from control, biochar, dairy cattle, and poultry treatments were 0.76, 0.70, 0.96, and 1.05 kg N2O-N/ha, respectively. Isotopocule mapping approach revealed that bacterial denitrification was the dominant pathway for temporal high N2O emission events as the fractions of bacterial denitrification ranged between 0.5 and 0.9 among treatments. Soil DNA-based Q-PCR assays showed significant increase in abundance of NO2− reducing denitrifiers in dairy cattle and poultry treated plots suggesting acceleration in N2O emissions was due to shift in the molecular ratios of (nirS + nirK)/nosZ denitrifying bacterial community. In contrast to manure treatments, the combined application of biochar along fertilizer significantly improved soil C contents with a slight decrease in N2O emission rates. Therefore, biochar appeared to be the best option to minimize soil quality loss without additional environmental cost.
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References
Akiyama H, Tsuruta H (2003) Nitrous oxide, nitric oxide, and nitrogen dioxide fluxes from soils after manure and urea application. J Environ Qual 32:423–431. https://doi.org/10.2134/jeq2003.4230
Asgedom H, Tenuta M, Flaten DN, Gao XP, Kebreab E (2014) Nitrous oxide emissions from a clay soil receiving granular urea formulations and dairy manure. Agron J 106:732–744. https://doi.org/10.2134/agronj2013.0096
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 Spectrom 22:1664–1672. https://doi.org/10.1002/rcm.3456
Borchard N, Schirrmann M, Cayuela ML, Kammann C, Wrage-Mönnig N, Estavillo JM, Fuertes-Mendizábal T, Sigua G, Spokas K, Ippolito JA, Novak J (2019) Biochar, soil and land-use interactions that reduce nitrate leaching and N2O emissions: a meta-analysis. Sci Total Environ 651:2354–2364. https://doi.org/10.1016/j.scitotenv.2018.10.060
Bowen H, Maul JE, Poffenbarger H, Mirsky S, Cavigelli M, Yarwood S (2018) Spatial patterns of microbial denitrification genes change in response to poultry litter placement and cover crop species in an agricultural soil. Biol Fertil Soils 54:769–781. https://doi.org/10.1007/s00374-018-1301
Buchen C, Lewicka-Szczebak D, Flessa H, Well R (2018) Estimating N2O processes during grassland renewal and grassland conversion to maize cropping using N2O isotopocules. Rapid Commun Mass Spectrom 32:1053–1067. https://doi.org/10.1002/rcm.8132
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 Ser B Biol Sci 368:20130122. https://doi.org/10.1098/rstb.2013.0122
Cai ZJ, Wang BR, Xu MG, Zhang HM, He XH, Zhang L, Gao SD (2015) Intensified soil acidification from chemical N fertilization and prevention by manure in an 18-year field experiment in the red soil of southern China. J Soils Sediments 15:260–270. https://doi.org/10.1007/s11368-014-0989
Castellano-Hinojosa A, González-López J, Bedmar EJ (2018) Distinct effect of nitrogen fertilisation and soil depth on nitrous oxide emissions and nitrifiers and denitrifiers abundance. Biol Fertil Soils 54:829–840. https://doi.org/10.1007/s00374-018-1310-9
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. https://doi.org/10.1016/j.agee.2013.10.009
Dai Z, Li Y, Zhang X, Wu J, Luo Y, Kuzyakov Y, Brookes PC, Xu J (2019) Easily mineralizable carbon in manure-based biochar added to a soil influences N2O emissions and microbial-N cycling genes land. Degrad Dev 30:406–416. https://doi.org/10.1002/ldr.3230
Davidson EA (2009) The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860. Nat Geosci 2:659–662. https://doi.org/10.1038/Ngeo608
Decock C, Six J (2013) How reliable is the intramolecular distribution of 15N in N2O to source partition N2O emitted from soil? Soil Biol Biochem 65:114–127. https://doi.org/10.1016/j.soilbio.2013.05.012
Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN, Reis S, Sheppard LJ, Jenkins A, Grizzetti B, Galloway JN, Vitousek P, Leach A, Bouwman AF, Butterbach-Bahl K, Dentener F, Stevenson D, Amann M, Voss M (2013) The global nitrogen cycle in the twenty-first century. Philos Trans R Soc Lond B Biol Sci 368:20130164. https://doi.org/10.1098/rstb.2013.0164
Fungo B, Lehmann J, Kalbitz K, Thionģo M, Tenywa M, Okeyo I, Neufeldt H (2019) Ammonia and nitrous oxide emissions from a field ultisol amended with tithonia green manure, urea, and biochar. Biol Fertil Soils 55:135–148. https://doi.org/10.1007/s00374-018-01338-3
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. https://doi.org/10.1371/journal.pone.0154773
Gil J, Perez T, Boering K, Martikainen PJ, Biasi C (2017) Mechanisms responsible for high N2O emissions from subarctic permafrost peatlands studied via stable isotope techniques. Glob Biogeochem Cycles 31:172–189. https://doi.org/10.1002/2015gb005370
Giles ME, Daniell TJ, Baggs EM (2017) Compound driven differences in N2 and N2O emission from soil; the role of substrate use efficiency and the microbial community. Soil Biol Biochem 106:90–98. https://doi.org/10.1016/j.soilbio.2016.11.028
Groffman P (2012) Terrestrial denitrification: challenges and opportunities. Ecol Process 1:11. https://doi.org/10.1186/2192-1709-1-11
Henault C, Grossel A, Mary B, Roussel M, Leonard J (2012) Nitrous oxide emission by agricultural soils: a review of spatial and temporal variability for mitigation pedosphere 22:426–433. https://doi.org/10.1016/S1002-0160(12)60029-0
Henry S, Baudoin E, Lopez-Gutierrez 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. https://doi.org/10.1016/j.mimet.2004.07.002
IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge
Jha N, Saggar S, Giltrap D, Tillman R, Deslippe J (2017) Soil properties impacting denitrifier community size, structure, and activity in New Zealand dairy-grazed pasture. Biogeosciences 14:4243–4253. https://doi.org/10.5194/bg-14-4243-2017
Kamewada K (2007) Vertical distribution of denitrification activity in an Andisol upland field and its relationship with dissolved organic carbon: effect of long-term organic matter application. J Soil Sci Plant Nutr 53:401–412. https://doi.org/10.1111/j.1747-0765.2007.00148.x
Kong AY, Hristova K, Scow KM, Six J (2010) Impacts of different N management regimes on nitrifier and denitrifier communities and N cycling in soil microenvironments. Soil Biol Biochem 42:1523–1533. https://doi.org/10.1016/j.soilbio.2010.05.021
Koster JR, Well R, Dittert K, Giesemann A, Lewicka-Szczebak D, Muhling KH, Herrmann A, Lammel J, Senbayram M (2013) Soil denitrification potential and its influence on N2O reduction and N2O isotopomer ratios rapid. Commun Mass Spectrom 27:2363–2373. https://doi.org/10.1002/rcm.6699
Kuang W, Gao X, Tenuta M, Gui D, Zeng F (2019) Relationship between soil profile accumulation and surface emission of N2O: effects of soil moisture and fertilizer nitrogen. Biol Fertil Soils 55:97–107. https://doi.org/10.1007/s00374-018-01337-4
Kuppusamy S, Thavamani P, Megharaj M, Venkateswarlu K, Naidu R (2016) Agronomic and remedial benefits and risks of applying biochar to soil: current knowledge and future research directions. Environ Int 87:1–12. https://doi.org/10.1016/j.envint.2015.10.018
Lee S-H, Kang H (2016) The activity and community structure of total bacteria and denitrifying bacteria across soil depths and biological gradients in estuary ecosystem. Appl Microbiol Biotechnol 100:1999–2010. https://doi.org/10.1007/s00253-015-7111-2
Lewicka-Szczebak D, Augustin J, Giesemann A, Well R (2017) Quantifying N2O reduction to N2 based on N2O isotopocules – validation with independent methods (helium incubation and 15N gas flux method). Biogeosciences 14:711–732. https://doi.org/10.5194/bg-14-711-2017
Liu X, Tiquia SM, Holguin G, Wu L, Nold SC, Devol AH, Luo K, Palumbo AV, Tiedje JM, Zhou J (2003) Molecular diversity of denitrifying genes in continental margin sediments within the oxygen-deficient zone off the Pacific coast of Mexico. Appl Environ Microbiol 69:3549–3560. https://doi.org/10.1128/aem.69.6.3549-3560.2003
Malghani S, Kim J, Lee SH, Yoo GY, Kang H (2018) Application of two contrasting rice-residue-based biochars triggered gaseous loss of nitrogen under denitrification-favoring conditions: a short-term study based on acetylene inhibition technique. Appl Soil Ecol 127:112–119. https://doi.org/10.1016/j.apsoil.2018.03.011
Norton JM, Stark JM (2011) Regulation and measurement of nitrification in terrestrial systems. In: Martin GK (ed) Methods in enzymology, vol volume 486. Academic Press, pp 343–368. https://doi.org/10.1016/B978-0-12-381294-0.00015-8
Ostrom NE, Sutka R, Ostrom PH, Grandy AS, Huizinga KM, Gandhi H, von Fischer JC, Robertson GP (2010) Isotopologue data reveal bacterial denitrification as the primary source of N2O during a high flux event following cultivation of a native temperate grassland soil. Biol Biochem 42:499–506. https://doi.org/10.1016/j.soilbio.2009.12.003
Ouyang Y, Norton JM, Stark JM, Reeve JR, Habteselassie MY (2016) Ammonia-oxidizing bacteria are more responsive than archaea to nitrogen source in an agricultural soil. Soil Biol Biochem 96:4–15. https://doi.org/10.1016/j.soilbio.2016.01.012
Park S, Pérez T, Boering KA, Trumbore SE, Gil J, Marquina S, Tyler SC (2011) Can N2O stable isotopes and isotopomers be useful tools to characterize sources and microbial pathways of N2O production and consumption in tropical soils? Global Biogeochem Cycles 25:n/a-n/a https://doi.org/10.1029/2009GB003615
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. https://doi.org/10.1007/s00374-015-1004-5
Philippot L, Cuhel J, Saby NP, Cheneby D, Chronakova A, Bru D, Arrouays D, Martin-Laurent F, Simek M (2009) Mapping field-scale spatial patterns of size and activity of the denitrifier community. Environ Microbiol 11:1518–1526. https://doi.org/10.1111/j.1462-2920.2009.01879.x
Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125. https://doi.org/10.1126/science.1176985
Rich JJ, Heichen RS, Bottomley PJ, Cromack K Jr, Myrold DD (2003) Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Appl Environ Microbiol 69:5974–5982. https://doi.org/10.1128/aem.69.10.5974-5982.2003
Rockmann T, Kaiser J, Brenninkmeijer CA, Brand WA (2003) Gas chromatography/isotope-ratio mass spectrometry method for high-precision position-dependent 15N and 18O measurements of atmospheric nitrous oxide rapid. Commun Mass Spectrom 17:1897–1908. https://doi.org/10.1002/rcm.1132
Rohe L (2014) Nitrous oxide from fungal denitrification - Pure culture and soil studies using stable isotope and microbial inhibitor approaches. PhD thesis. Georg-August-Universität Göttingen Germany
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
Sánchez-García M, Roig A, Sanchez-Monedero MA, Cayuela ML (2014) Biochar increases soil N2O emissions produced by nitrification-mediated pathways front. Environ Sci 2. https://doi.org/10.3389/fenvs.2014.00025
Seufert V, Ramankutty N, Foley JA (2012) Comparing the yields of organic and conventional agriculture. Nature 485:229–232. https://doi.org/10.1038/nature11069
Smith DW, Mukhtar S (2015) Estimation and attribution of nitrous oxide emissions following subsurface application of animal manure: a review. Trans Asabe 58:429–438. https://doi.org/10.13031/trans.58.11065
Stein LY (2011) Surveying N2O-producing pathways in bacteria. In: Martin GK (ed) Methods in enzymology, volume 486. Academic Press, London, pp 131–152. https://doi.org/10.1016/B978-0-12-381294-0.00006-7
Stieglmeier M, Mooshammer M, Kitzler B, Wanek W, Zechmeister-Boltenstern S, Richter A, Schleper C (2014) Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. ISME J 8:1135–1146. https://doi.org/10.1038/ismej.2013.220
Toyoda S, Yoshida N, Koba K (2017) Isotopocule analysis of biologically produced nitrous oxide in various environments. Mass Spectrom Rev 36:135–160. https://doi.org/10.1002/mas.21459
Ussiri D, Lal R (2013) Soil emission of nitrous oxide and its mitigation. Springer, Heidelberg
Verhoeven E, Barthel M, Yu LF, Celi L, Said-Pullicino D, Sleutel S, Lewicka-Szczebak D, Six J, Decock C (2019) Early season N2O emissions under variable water management in rice systems: source-partitioning emissions using isotope ratios along a depth profile. Biogeosciences 16:383–408. https://doi.org/10.5194/bg-16-383-2019
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. https://doi.org/10.1007/s00374-017-1191-3
Vilain G, Garnier J, Decuq C, Lugnot M (2014) Nitrous oxide production from soil experiments: denitrification prevails over nitrification. Nutr Cycl Agroecosyst 98:169–186. https://doi.org/10.1007/s10705-014-9604-2
Watanabe A, Ikeya K, Kanazaki N, Makabe S, Sugiura Y, Shibata A (2014) Five crop seasons records of greenhouse gas fluxes from upland fields with repetitive applications of biochar and cattle manure. J Environ Manag 144:168–175. https://doi.org/10.1016/j.jenvman.2014.05.032
Wei WL, Yan Y, Cao J, Christie P, Zhang FS, Fan MS (2016) Effects of combined application of organic amendments and fertilizers on crop yield and soil organic matter: An integrated analysis of long-term experiments. Agric Ecosyst Environ 225:86–92. https://doi.org/10.1016/j.agee.2016.04.004
Wrage-Monnig N, Horn MA, Well R, Muller C, Velthof G, Oenema O (2018) The role of nitrifier denitrification in the production of nitrous oxide revisited. Soil Biol Biochem 123:A3–A16. https://doi.org/10.1016/j.soilbio.2018.03.020
Yamamoto A, Uchida Y, Akiyama H, Nakajima Y (2014) Continuous and unattended measurements of the site preference of nitrous oxide emitted from an agricultural soil using quantum cascade laser spectrometry with intercomparison with isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 28:1444–1452. https://doi.org/10.1002/rcm.6916
Yan ZF, Liu CX, Todd-Brown KE, Liu YY, Bond-Lamberty B, Bailey VL (2016) Pore-scale investigation on the response of heterotrophic respiration to moisture conditions in heterogeneous soils. Biogeochemistry 131:121–134. https://doi.org/10.1007/s10533-016-0270-0
Yano M, Toyoda S, Tokida T, Hayashi K, Hasegawa T, Makabe A, KobaK, Yoshida N (2014) Isotopomer analysis of production, consumption and soil-to-atmosphere emission processes of N2O at the beginning of paddy field irrigation. Soil Biol Biochem 70:66–78 https://doi.org/10.1016/j.soilbio.2013.11.026
Zaady E, Groffman PM, Standing D, Shachak M (2013) High N2O emissions in dry ecosystems. Eur J Soil Biol 59:1–7. https://doi.org/10.1016/j.ejsobi.2013.08.004
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This work was supported by the Korea Research Fellowship Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (KRF project).
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Malghani, S., Yoo, Gy., Giesemann, A. et al. Combined application of organic manure with urea does not alter the dominant biochemical pathway producing N2O from urea treated soil. Biol Fertil Soils 56, 331–343 (2020). https://doi.org/10.1007/s00374-019-01420-4
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DOI: https://doi.org/10.1007/s00374-019-01420-4