Advertisement

Effects of 3,4-dimethylpyrazole phosphate (DMPP) on the abundance of ammonia oxidizers and denitrifiers in two different intensive vegetable cultivation soils

  • Jie Li
  • Yuanliang Shi
  • Jiafa Luo
  • Yan Li
  • Lingli Wang
  • Stuart Lindsey
Soils, Sec 2 • Global Change, Environ Risk Assess, Sustainable Land Use • Research Article
  • 17 Downloads

Abstract

Purpose

Nitrification and denitrification in the N cycle are affected by various ammonia oxidizers and denitrifying microbes in intensive vegetable cultivation soils, but our current understanding of the effect these microbes have on N2O emissions is limited. The nitrification inhibitor, 3,4-dimethylpyrazole phosphate (DMPP), acts by slowing nitrification and is used to improve fertilizer use efficiency and reduce N losses from agricultural systems; however, its effects on nitrifier and denitrifier activities in intensive vegetable cultivation soils are unknown.

Materials and methods

In this study, we measured the impacts of DMPP on N2O emissions, ammonia oxidizers, and denitrifying microbes in two intensive vegetable cultivation soils: one that had been cultivated for a short term (1 year) and one that had been cultivated over a longer term (29 years). The quantitative PCR technique was used in this study. Three treatments, including control (no fertilizer), urea alone, and urea with DMPP, were included for each soil. The application rates of urea and DMPP were 1800 kg ha−1 and 0.5% of the urea-N application rate.

Results and discussion

The application of N significantly increased N2O emissions in both soils. The abundance of ammonia-oxidizing bacteria (AOB) increased significantly with high rate of N fertilizer application in both soils. Conversely, there was no change in the growth rate of ammonia-oxidizing archaea (AOA) in response to the applied urea despite the presence of larger numbers of AOA in these soils. This suggests AOB may play a greater role than AOA in the nitrification process, and N2O emission in intensive vegetable cultivation soils. The application of DMPP significantly reduced soil NO3-N content and N2O emission, and delayed ammonia oxidation. It greatly reduced AOB abundance, but not AOA abundance. Moreover, the presence of DMPP was correlated with a significant decrease in the abundance of nitrite reductase (nirS and nirK) genes.

Conclusions

Long-term intensive vegetable cultivation with heavy N fertilization altered AOB and nirS abundance. In vegetable cultivation soils with high N levels, DMPP can be effective in mitigating N2O emissions by directly inhibiting both ammonia oxidizing and denitrifying microbes.

Keywords

AOA AOB DMPP nirnirVegetable cultivation soil 

Notes

Funding information

This study was financially supported by the National Key Research and Development Program of China (Nos. 2017YFD0200708, 2018YFD0200200, 2017YFD0200100, 2016YFD0200307, 2017YFD0800604), the National Natural Science Foundation of China (No. 41807107), a project from Liaoning province doctoral research start-up fund (20170520106), and the Shenyang science and technology project (17-156-6-00).

References

  1. Ai C, Liang G, Sun J, Wang X, He P, Zhou W (2013) Different roles of rhizosphere effect and long-term fertilization in the activity and community structure of ammonia oxidizers in a calcareous fluvo-aquic soil. Soil Biol Biochem 57:30–42CrossRefGoogle Scholar
  2. Bao Q, Ju X, Gao B, Qu Z, Christie P, Lu Y (2011) Response of nitrous oxide and corresponding bacteria to managements in an agricultural soil. Soil Sci Soc Am J 76:130–141CrossRefGoogle Scholar
  3. Benckiser G, Christ E, Herbert T, Weiske A, Blome J, Hardt M (2013) The nitrification inhibitor 3,4-dimethylpyrazole-phosphat (DMPP) - quantification and effects on soil metabolism. Plant Soil 371:257–266CrossRefGoogle Scholar
  4. 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 64:3769–3995Google Scholar
  5. Chen Z, Luo X, Hu R, Wu M, Wu J, Wei W (2010) Impact of long-term fertilization on the composition of denitrifier communities based on nitrite reductase analyses in a paddy soil. Microb Ecol 60:850–861CrossRefGoogle Scholar
  6. Chen Z, Liu J, Wu M, Xie X, Wu J, Wei W (2012) Differentiated response of denitrifying communities to fertilization regime in paddy soil. Microb Ecol 63:446–459CrossRefGoogle Scholar
  7. Dambreville C, Hallet S, Nguyen C, Morvan T, Germon JC, Philippot L (2006) Structure and activity of the denitrifying community in a maize-cropped field fertilized with composted pig manure or ammonium nitrate. FEMS Microbiol Ecol 56:119–131CrossRefGoogle Scholar
  8. Di HJ, Cameron KC (2011) Inhibition of ammonium oxidation by a liquid formulation of 3,4-dimethylpyrazole phosphate (DMPP) compared with a dicyandiamide (DCD) solution in six New Zealand grazed grassland soils. J Soils Sediments 11:1032–1039CrossRefGoogle Scholar
  9. Di HJ, Cameron KC (2012) How does the application of different nitrification inhibitors affect nitrous oxide emissions and nitrate leaching from cow urine in grazed pastures? Soil Use Manag 28:54–61CrossRefGoogle Scholar
  10. Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He J (2010) Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol 72:386–394CrossRefGoogle Scholar
  11. 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 50:795–807CrossRefGoogle Scholar
  12. 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 102:14683–14688CrossRefGoogle Scholar
  13. Garbeva P, Baggs EM, Prosser JI (2007) Phylogeny of nitrite reductase (nirK) and nitric oxide reductase (norB) genes from Nitrosospira species isolated from soil. FEMS Microbiol Lett 266:83–89CrossRefGoogle Scholar
  14. Gong P, Zhang L, Wu Z, Chen Z, Chen L (2013) Responses of ammonia-oxidizing bacteria and archaea in two agricultural soils to nitrification inhibitors DCD and DMPP: a pot experiment. Pedosphere 23:729–739CrossRefGoogle Scholar
  15. He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di HJ (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 9:2364–2374CrossRefGoogle Scholar
  16. Jackson ML (1958) Soil chemical analysis. Prentice-Hall, Englewood Cliffs, NJ, USAGoogle Scholar
  17. Jia Z, Conrad R (2009) Bacteria, rather than archaea, dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671CrossRefGoogle Scholar
  18. Kastl EM, Schloter-Hai B, Buegger F, Schloter M (2015) Impact of fertilization on the abundance of nitrifiers and denitrifiers at the root–soil interface of plants with different uptake strategies for nitrogen. Biol Fertil Soils 51:57–64CrossRefGoogle Scholar
  19. 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 84:182–186CrossRefGoogle Scholar
  20. Kou YP, Wei K, Chen GX, Wang ZY, Xu H (2015) Effects of 3,4-dimethylpyrazole phosphate and dicyandiamide on nitrous oxide emission in a greenhouse vegetable soil. Plant Soil Environ 61:29–35Google Scholar
  21. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809CrossRefGoogle Scholar
  22. Li J, Luo J, Shi Y, Li Y, Ma Y, Ledgard S, Wang L, Houlbrooke D, Bo L, Lindsey S (2016) Dung and farm dairy effluent affect urine patch nitrous oxide emissions from a pasture. Anim Prod Sci 56:337–342CrossRefGoogle Scholar
  23. Liu Y, Yang Y, Qin HL, Zhu YJ, Wei WX (2014) Differential responses of nitrifier and denitrifier to dicyandiamide in short- and long-term intensive vegetable cultivation soils. J Integr Agric 13:1090–1098CrossRefGoogle Scholar
  24. Luo J, Ledgard S, Wise B, Lindsey S (2016) Effect of dicyandiamide (DCD) on nitrous oxide emissions from cow urine deposited on a pasture soil, as influenced by DCD application method and rate. Anim Prod Sci 56:350–354CrossRefGoogle Scholar
  25. Mahmood S, Prosser JI (2006) The influence of synthetic sheep urine on ammonia oxidizing bacterial communities in grassland soil. FEMS Microbiol Ecol 56:444–454CrossRefGoogle Scholar
  26. Mertens J, Broos K, Wakelin SA, Kowalchuk GA, Springael D, Smolders E (2009) Bacteria, not archaea, restore nitrification in a zinc-contaminated soil. Isme J 3:916–923CrossRefGoogle Scholar
  27. Myhre G, Shindell D, Bréon F-M, Collins W, Fuglestvedt J, Huang J, Koch D, Lamarque J-F, Lee D, Mendoza B, Nakajima T, Robock A, Stephens G, Takemura T, Zhang H (2013) Anthropogenic and natural radiative forcing. In: Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change, pp 659–740Google Scholar
  28. O’Callaghan M, Gerard EM, Carter PE, Lardner R, Sarathchandra U, Burch G, Ghani A, Bell N (2010) Effect of the nitrification inhibitor dicyandiamide (DCD) on microbial communities in a pasture soil amended with bovine urine. Soil Biol Biochem 42:1425–1436CrossRefGoogle Scholar
  29. Prosser JI, Nicol GW (2008) Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 10(11):2931–2941CrossRefGoogle Scholar
  30. Qin S, Ding K, Cough T, Hu C, Luo J (2017) Temporal in situ dynamics of N2O reductase activity as affected by nitrogen fertilization and implications for the N2O/(N2O+N2) product ratio and N2O mitigation. Biol Fertil Soils 53:723–727CrossRefGoogle Scholar
  31. 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 popula-tions. Appl Environ Microbiol 63:4704–4712Google Scholar
  32. Schauss K, Focks A, Leininger S, Kotzerke A, Heuer H, Thiele-Bruhn S, Sharma S, Wilke BM, Matthies M, Smalla K, Munch JC, Amelung W, Kaupenjohann M, Schloter M, Schleper C (2009) Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environ Microbiol 11:446–456CrossRefGoogle Scholar
  33. Shen WS, Lin XG, Shi WM, Min J, Gao N, Zhang HY, Yin R, He XH (2010) Higher rates of nitrogen fertilization decrease soil enzyme activities, microbial functional diversity and nitrification capacity in a Chinese polytunnel greenhouse vegetable land. Plant Soil 337:137–150CrossRefGoogle Scholar
  34. Shen W, Ni Y, Gao N, Bian B, Zheng S, Lin X, Chu H (2016) Bacterial community composition is shaped by soil secondary salinization and acidification brought on by high nitrogen fertilization rates. Appl Soil Ecol 108:76–83CrossRefGoogle Scholar
  35. Stites W, Kraft GJ (2001) Nitrate and chloride loading to groundwater from an irrigated north-central US sand-plain vegetable field. J Environ Qual 30:1176–1184CrossRefGoogle Scholar
  36. 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 49:401–417Google Scholar
  37. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7:1985–1995CrossRefGoogle Scholar
  38. Valentine DL (2007) Adaptations to energy stress dictate the ecology and evolution of the archaea. Nat Rev Microbiol 5:316–323CrossRefGoogle Scholar
  39. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu DY, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74CrossRefGoogle Scholar
  40. Weiske A, Benckiser G, Herber 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 34:109–117CrossRefGoogle Scholar
  41. Wu Y, Lu L, Wang B, Lin X, Zhu J, Cai Z, Yan X, Jia Z (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 75:1431–1439CrossRefGoogle Scholar
  42. Xia W, Zhang C, Zeng X, Feng Y, Weng J, Lin X, Zhu J, Xiong Z, Xu J, Cai Z, Jia Z (2011) Autotrophic growth of nitrifying community in an agricultural soil. Isme J 5:1226–1236CrossRefGoogle Scholar
  43. Yao H, Gao Y, Nicol GW, Campbell CD, Prosser JI, Zhang L, Han W, Singh BK (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microbiol 77:4618–4625CrossRefGoogle Scholar
  44. 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 6:1032–1045CrossRefGoogle Scholar
  45. Zheng X, Han S, Huang Y, Wang Y, Wang M (2004) Re-quantifying the emission factors based on field measurements and estimating the direct N2O emission from Chinese croplands. Glob Biogeochem Cycles 18.  https://doi.org/10.1029/2003GB002167 CrossRefGoogle Scholar
  46. Zhu JH, Li XL, Christie P, Li JL (2005) Environmental implications of low nitrogen use efficiency in excessively fertilized hot pepper (Capsicum frutescens L.) cropping systems. Agric Ecosyst Environ 111:70–80CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Jie Li
    • 1
  • Yuanliang Shi
    • 1
  • Jiafa Luo
    • 2
  • Yan Li
    • 3
  • Lingli Wang
    • 1
  • Stuart Lindsey
    • 2
  1. 1.Institute of Applied EcologyChinese Academy of SciencesShenyangChina
  2. 2.Ruakura Research CentreAgResearch LimitedHamiltonNew Zealand
  3. 3.Shandong Academy of Agricultural SciencesJinanChina

Personalised recommendations