Abstract
This study evaluated the impacts of a nitrification inhibitor (3,4-dimethylpyrazole phosphate, DMPP) and herbicides (atrazine and glyphosate) on nitrification, gross nitrite, and nitrate (NO2−-N + NO3−-N) consumption rate, nitrous oxide (N2O) emission, and abundances of microbial functional genes related to nitrogen (N) cycling in an Australian sugarcane soil. The experiment included four treatments: blank control (CK), DMPP application (NI), atrazine application (ATR), and glyphosate application (GLY). All treatments received (NH4)2SO4 at 50 mg N kg−1 dry soil and KNO3 at 50 mg N kg−1 dry soil and were incubated initially at 55% of water holding capacity (WHC) for 7 days and subsequently at 75% WHC for another 7 days (K15NO3 with 5 atom% 15N added at the beginning of each stage). Compared with the CK treatment, DMPP application significantly decreased N2O emissions throughout the incubation, while atrazine or glyphosate application significantly inhibited N2O emissions only during the 4–7-day period. DMPP application also decreased ammonium-oxidizing bacteria (AOB) amoA gene abundances, gross NO2−-N + NO3−-N consumption rates at 55 and 75% WHC, and nirS and nirK gene abundances of denitrifiers at 75% WHC. The atrazine and glyphosate applications decreased the gross nitrification and NO2−-N + NO3−-N consumption rates, abundances of both ammonium-oxidizing archaea (AOA) and AOB amoA genes at 55 and 75% WHC, and abundances of functional genes related to different reactions of the denitrification during the incubation. These results suggested that DMPP, atrazine, and glyphosate could decrease soil gross nitrification and denitrification rates perhaps by inhibiting microbial functional gene abundances and that application of DMPP could effectively reduce N2O emissions in the sugarcane cropping soil.
Similar content being viewed by others
References
Allegrini M, Gomez EV, Zabaloy MC (2017) Repeated glyphosate exposure induces shifts in nitrifying communities and metabolism of phenylpropanoids. Soil Biol Biochem 105:206–215
Anjum T, Bajwa R (2007) Field appraisal of herbicide potential of sunflower leaf extract against Rumex dentatus. Field Crop Res 100:139–142
Bento CP, Yang X, Gort G, Xue S, van Dam R, Zomer P, Mol HG, Ritsema CJ, Geissen V (2016) Persistence of glyphosate and aminomethylphosphonic acid in loess soil under different combinations of temperature, soil moisture and light/darkness. Sci Total Environ 572:301–311
Bonfleur E, Tornisielo V, Regitano J, Lavorenti A (2015) The effects of glyphosate and atrazine mixture on soil microbial population and subsequent impacts on their fate in a tropical soil. Water Air Soil Pollut 226:21
Bonilla-Rosso G, Wittorf L, Jones CM, Hallin S (2016) Design and evaluation of primers targeting genes encoding NO-forming nitrite reductases: implications for ecological inference of denitrifying communities. Sci Rep 6:39208
Caffrey JM, Bano N, Kalanetra K, Hollibaugh JT (2007) Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J 1:660–662
Cai Y, Chang SX, Ma B, Bork EW (2016) Watering increased DOC concentration but decreased N2O emission from a mixed grassland soil under different defoliation regimes. Biol Fertil Soils 52:987–996
Chaves B, Opoku A, De Neve S, Boeckx P, Van Cleemput O, Hofman G (2006) Influence of DCD and DMPP on soil N dynamics after incorporation of vegetable crop residues. Biol Fertil Soils 43:62–68
Decock C (2014) Mitigating nitrous oxide emissions from corn cropping systems in the midwestern US: potential and data gaps. Environ Sci Technol 48:4247–4256
Duan YF, Kong XW, Schramm A, Labouriau R, Eriksen J, Petersen SO (2017) Microbial N transformations and N2O emission after simulated grassland cultivation: effects of the nitrification inhibitor 3, 4-dimethylpyrazole phosphate (DMPP). Appl Environ Microbiol 83:e02019–e02016
Fahad S, Hussain S, Saud S, Hassan S, Muhammad H, Shan D, Chen C, Wu C, Xiong D, Khan S (2014) Consequences of narrow crop row spacing and delayed Echinochloa colona and Trianthema portulacastrum emergence for weed growth and crop yield loss in maize. Weed Res 54:475–483
Florio A, Clark IM, Hirsch PR, Jhurreea D, Benedetti A (2014) Effects of the nitrification inhibitor 3, 4-dimethylpyrazole phosphate (DMPP) on abundance and activity of ammonia oxidizers in soil. Biol Fertil Soils 50:795–807
French E, Kozlowski JA, Mukherjee M, Bullerjahn G, Bollmann A (2012) Ecophysiological characterization of ammonia-oxidizing archaea and bacteria from freshwater. Appl Environ Microbiol 78:5773–5780
Gómez-Rey MX, González-Prieto SJ (2015) Soil gross N transformation rates after a wildfire and straw mulch application for burned soil emergency stabilisation. Biol Fertil Soils 51:493–505
Haney R, Senseman S, Krutz L, Hons F (2002) Soil carbon and nitrogen mineralization as affected by atrazine and glyphosate. Biol Fertil Soils 35:35–40
Hatzenpichler R (2012) Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microbiol 78:7501–7510
Hayden HL, Drake J, Imhof M, Oxley AP, Norng S, Mele PM (2010) The abundance of nitrogen cycle genes amoA and nifH depends on land-uses and soil types in South-Eastern Australia. Soil Biol Biochem 42:1774–1783
He J, Shen J, Zhang L, Zhu Y, Zheng Y, Xu M, Di H (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9:2364–2374
Jia Z, Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671
Jiang J, Chen L, Sun Q, Sang M, Huang Y (2015) Application of herbicides is likely to reduce greenhouse gas (N2O and CH4) emissions from rice-wheat cropping systems. Atmos Environ 107:62–69
Kaur N, Bhullar M, Gill G (2016) Weed management in sugarcane-canola intercropping systems in northern India. Field Crop Res 188:1–9
Kleineidam K, Košmrlj K, Kublik S, Palmer I, Pfab H, Ruser R, Fiedler S, Schloter M (2011) Influence of the nitrification inhibitor 3, 4-dimethylpyrazole phosphate (DMPP) on ammonia-oxidizing bacteria and archaea in rhizosphere and bulk soil. Chemosphere 84:182–186
Kong X, Duan Y, Schramm A, Eriksen J, Petersen SO (2016) 3, 4-Dimethylpyrazole phosphate (DMPP) reduces activity of ammonia oxidizers without adverse effects on non-target soil microorganisms and functions. Appl Soil Ecol 105:67–75
Kroon FJ, Thorburn P, Schaffelke B, Whitten S (2016) Towards protecting the great barrier reef from land-based pollution. Glob Chang Biol 22:1985–2002
Lan T, Han Y, Roelcke M, Nieder R, Cai Z (2013) Processes leading to N2O and NO emissions from two different Chinese soils under different soil moisture contents. Plant Soil 371:611–627
Liu X, Chen C, Wang W, Hughes J, Lewis HE, Shen J (2013) Soil environmental factors rather than denitrification gene abundance control N2O fluxes in a wet sclerophyll forest with different burning frequency. Soil Biol Biochem 57:292–300
Liu R, Hayden H, Suter H, He J, Chen D (2015) The effect of nitrification inhibitors in reducing nitrification and the ammonia oxidizer population in three contrasting soils. J Soils Sediments 15:1113–1118
MacGregor A (1972) Gaseous losses of nitrogen from freshly wetted desert soils. Soil Sci Soc Am J 36:594–596
Mahía J, Cabaneiro A, Carballas T, Díaz-Raviña M (2008) Microbial biomass and C mineralization in agricultural soils as affected by atrazine addition. Biol Fertil Soils 45:99–105
Mahía J, González-Prieto SJ, Martín A, Bååth E, Díaz-Raviña M (2011) Biochemical properties and microbial community structure of five different soils after atrazine addition. Biol Fertil Soils 47:577–589
Martens-Habbena W, Berube PM, Urakawa H, José R, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–979
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
Mary B, Recous S, Robin D (1998) A model for calculating nitrogen fluxes in soil using 15N tracing. Soil Biol Biochem 30:1963–1979
Menéndez S, Barrena I, Setien I, González-Murua C, Estavillo JM (2012) Efficiency of nitrification inhibitor DMPP to reduce nitrous oxide emissions under different temperature and moisture conditions. Soil Biol Biochem 53:82–89
Nachimuthu G, Halpin NV, Bell MJ (2016) Effect of sugarcane cropping systems on herbicide losses in surface runoff. Sci Total Environ 557:773–784
Nguyen DB, Rose MT, Rose TJ, Morris SG, Van Zwieten L (2016) Impact of glyphosate on soil microbial biomass and respiration: a meta-analysis. Soil Biol Biochem 92:50–57
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
Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531
Rayment GE, Lyons DJ (2010) Soil chemical methods—Australasia. CSIRO Publishing, Melbourne, p 520
Sabba F, Picioreanu C, Pérez J, Nerenberg R (2015) Hydroxylamine diffusion can enhance N2O emissions in nitrifying biofilms: a modeling study. Environ Sci Technol 49:1486–1494
Santos A, Flores M (1995) Effects of glyphosate on nitrogen fixation of free-living heterotrophic bacteria. Lett Appl Microbiol 20:349–352
Scheer C, Rowlings DW, Firrel M, Deuter P, Morris S, Grace PR (2014) Impact of nitrification inhibitor (DMPP) on soil nitrous oxide emissions from an intensive broccoli production system in sub-tropical Australia. Soil Biol Biochem 77:243–251
Soares JR, Cantarella H, de Campos Menegale ML (2012) Ammonia volatilization losses from surface-applied urea with urease and nitrification inhibitors. Soil Biol Biochem 52:82–89
Thorburn PJ, Biggs JS, Collins K, Probert ME (2010) Using the APSIM model to estimate nitrous oxide emissions from diverse Australian sugarcane production systems. Agric Ecosyst Environ 136:343–350
Wang W (2016) Effects of polymer-and nitrification inhibitor-coated urea on N2O emission, productivity and profitability in a wet tropical sugarcane crop in Australia. In ‘Proceedings of the International Nitrogen Initiative Conference, Melbourne, Australia’. http://www.ini2016.com/pdf-papers/INI2016_Wang_Weijin.pdf
Wang W, Dalal RC, Reeves SH, Bntterbach-Bahl K, Kiese R (2011) Greenhouse gas fluxes from an Australian subtropical cropland under long-term contrasting management regimes. Glob Chang Biol 17:3089–3101
Wang Q, Zhang LM, Shen JP, Du S, Han LL, He JZ (2016a) Nitrogen fertiliser-induced changes in N2O emissions are attributed more to ammonia-oxidising bacteria rather than archaea as revealed using 1-octyne and acetylene inhibitors in two arable soils. Biol Fertil Soils 52:1163–1171
Wang W, Reeves S, Salter B, Moody P, Dalal R (2016b) Effects of urea formulations, application rates and crop residue retention on N2O emissions from sugarcane fields in Australia. Agric Ecosyst Environ 216:137–146
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
Weiske A, Benckiser G, Herbert T, Ottow J (2001) Influence of the nitrification inhibitor 3, 4-dimethylpyrazole phosphate (DMPP) in comparison to dicyandiamide (DCD) on nitrous oxide emissions, carbon dioxide fluxes and methane oxidation during 3 years of repeated application in field experiments. Biol Fertil Soils 34:109–117
Wu X, Liu H, Fu B, Wang Q, Xu M, Wang H, Yang F, Liu G (2017) Effects of land-use change and fertilization on N2O and NO fluxes, the abundance of nitrifying and denitrifying microbial communities in a hilly red soil region of southern China. Appl Soil Ecol 120:111–120
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
Yu Q, Chen Y, Ye X, Tian G, Zhang Z (2007) Influence of the DMPP (3, 4-dimethyl pyrazole phosphate) on nitrogen transformation and leaching in multi-layer soil columns. Chemosphere 69:825–831
Zerulla W, Barth T, Dressel J, Erhardt K, von Locquenghien KH, Pasda G, Rädle M, Wissemeier A (2001) 3, 4-Dimethylpyrazole phosphate (DMPP)—a new nitrification inhibitor for agriculture and horticulture. Biol Fertil Soils 34:79–84
Zhang MY, Xu ZH, Teng Y, Christie P, Wang J, Ren WJ, Luo YM, Li ZG (2016) Non-target effects of repeated chlorothalonil application on soil nitrogen cycling: the key functional gene study. Sci Total Environ 543:636–643
Zhang MY, Wang WJ, Bai SH, Zhou X, Teng Y, Xu ZH (2018) Antagonistic effects of nitrification inhibitor 3, 4-dimethylpyrazole phosphate and fungicide iprodione on net nitrification in an agricultural soil. Soil Biol Biochem 116:167–170
Acknowledgments
Manyun Zhang was awarded a Griffith University Ph.D. scholarship for international students. The authors sincerely thank Geoffrey Lambert for his patient and detailed guidance in the determination of gross nitrification/denitrification rates, Linfeng Li for his support in the path analysis, and Dr. Xiuzhen Shi from the University of Melbourne for her help in the qPCR.
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
ESM 1
(DOCX 317 kb)
Rights and permissions
About this article
Cite this article
Zhang, M., Wang, W., Tang, L. et al. Effects of nitrification inhibitor and herbicides on nitrification, nitrite and nitrate consumptions and nitrous oxide emission in an Australian sugarcane soil. Biol Fertil Soils 54, 697–706 (2018). https://doi.org/10.1007/s00374-018-1293-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-018-1293-6