Journal of Soils and Sediments

, Volume 16, Issue 12, pp 2687–2697 | Cite as

Changes in the activity and abundance of the soil microbial community in response to the nitrification inhibitor 3,4-dimethylpyrazole phosphate (DMPP)

  • Alessandro Florio
  • Anita Maienza
  • Maria Teresa Dell’Abate
  • Silvia Rita Stazi
  • Anna Benedetti
Soils, Sec 2 • Global Change, Environ Risk Assess, Sustainable Land Use • Research Article

Abstract

Purpose

The application of organic and inorganic fertilizers to soil can result in increased gaseous emissions, such as NH3, N2O, CO2, and CH4, as well as nitrate leaching, contributing to climate warming and ground and surface water pollution, particularly in regions with hot climates, where high temperatures and high soil nitrification rates often occur. The use of nitrification inhibitors (NIs) has been shown to effectively decrease nitrogen (N) losses from the soil-plant system.

Materials and methods

Non-disruptive laboratory incubation experiments were conducted to assess the extent to which temperature (20 and 30 °C) and nutrient source (mineral and organic fertilizers) influence the rate of carbon (C)- and N-related microbial processes in soil in response to the NI 3,4-dimethylpyrazole phosphate (DMPP). Furthermore, short-term changes in the ability of microbes to degrade C substrates were evaluated in disruptive soil microcosms using microbial community-level physiological profiling and the abundance of the bacterial 16S rRNA gene as a measure of total bacterial population size.

Results and discussion

DMPP reduced net nitrification after 2 and 4 weeks of incubation at 30 and 20 °C by an average of 78.3 and 84.5 %, respectively, and with similar dynamics for mineral or organic fertilization. The addition of labile organic matter with cattle effluent led to a rapid increase in C mineralization that was significantly reduced by DMPP at both temperatures, whereas no changes could be detected after the addition of mineral fertilizer. The culturable heterotrophic microorganisms showed metabolic diversification in the oxidation of C sources, with organic fertilizer playing a major role in the substrate utilization patterns during the first week of incubation and the DMPP effects prevailing from day 14 until day 28. Furthermore, the copy number of the bacterial 16S rRNA gene was reduced by the application of DMPP and organic fertilizer after 28 days.

Conclusions

Our results show the marked efficiency of DMPP as an NI at elevated temperatures of incubation and when associated with both mineral and organic fertilization, providing support for its use as a tool to mitigate N losses in Mediterranean ecosystems. However, we also observed impaired C respiration rates and bacterial abundances, as well as shifts in community-level physiological profiles in soil, possibly indicating a short-term effect of DMPP and organic fertilizers on non-target C-related processes and microorganisms.

Keywords

3,4-Dimethylpyrazol phosphate (DMPP) Community-level physiological profiling (CLPP) Nitrification Nitrification inhibitor N cycle Soil microbial ecology 

References

  1. 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 56:420–6CrossRefGoogle Scholar
  2. Arancon NQ, Edwards CA, Bierman P (2006) Influences of vermicomposts on field strawberries: part 2. Effects on soil microbiological and chemical properties. Bioresour Technol 97:831–40CrossRefGoogle Scholar
  3. Badalucco L, Gelsomino A, Dell'Orco S, Grego S, Nannipieri P (1992) Biochemical characterization of soil organic compounds extracted by 0.5 m K2SO4 before and after chloroform fumigation. Soil Biol Biochem 24:569–78CrossRefGoogle Scholar
  4. Barth G, von Tucher S, Schmidhalter U (2001) Influence of soil parameters on the effect of 3,4-dimethylpyrazole-phosphate as a nitrification inhibitor. Biol Fert Soils 34:98–102CrossRefGoogle Scholar
  5. Barth G, von Tucher S, Schmidhalter U (2008) Effectiveness of 3,4-dimethylpyrazole phosphate as nitrification inhibitor in soil as influenced by inhibitor concentration, application form, and soil matric potential. Pedosphere 18:378–85CrossRefGoogle Scholar
  6. Benedetti A, Alianiello F, Dell’Abate MT (1994) A modified Stanford and Smith method for the study of the mineralization of nitrogen from organic materials. In: Neeteson JJ, Hassink J (eds) Nitrogen mineralization in agricultural soils. AB-DLO Thema’s, Haren, pp 127–32Google Scholar
  7. Bond-Lamberty B, Thomson A (2010) Temperature-associated increases in the global soil respiration record. Nature 464:579–82CrossRefGoogle Scholar
  8. Buyer JS, Roberts DP, Russek-Cohen E (2002) Soil land plant effects on microbial community structure. Can J Microbiol 48:955–64CrossRefGoogle Scholar
  9. Chen D, Helen CS, Islam A, Edis R (2010) Influence of nitrification inhibitors on nitrification and nitrous oxide (N2O) emission from a clay loam soil fertilized with urea. Soil Biol Biochem 42:660–4CrossRefGoogle Scholar
  10. Clark IM, Buchkina N, Jhurreea D, Goulding KWT, Hirsch PR (2012) Impacts of nitrogen application rates on the activity and diversity of denitrifying bacteria in the Broadbalk Wheat Experiment. Phil Trans R Soc B 367:1235–44CrossRefGoogle Scholar
  11. Davidson E, Belk E, Boone RD (1998) Soil water content and temperature as independent or confounded factors controlling soil respiration in a temperate mixed hardwood forest. Glob Change Biol 4:217–27CrossRefGoogle Scholar
  12. De Antoni MM, Scheer C, Grace P, Rowlings D, Bell M, McGree J (2014) Influence of different nitrogen rates and DMPP nitrification inhibitor on annual N2O emissions from a subtropical wheat–maize cropping system. Agric Ecosys Environ 186:33–43CrossRefGoogle Scholar
  13. Dell’Abate MT, Benedetti A, Trinchera A, Galluzzo D (2003) Nitrogen and carbon mineralisation of leather meal in soil as affected by particle size of fertiliser and microbiological activity of soil. Biol Fertil Soils 37:124–9Google Scholar
  14. 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 11:1032–9CrossRefGoogle Scholar
  15. Dittert K, Bol R, King B, Chadwick D, Hatch D (2001) Use of a novel nitrification inhibitor to reduce nitrous oxide emission from 15N-labelled dairy slurry injected into soil. Rapid Commun Mass Spectrom 15:1291–6CrossRefGoogle Scholar
  16. Du Plessis KR, Botha A, Joubert L, Bester R, Conradie WJ, Wolfaardt GM (2005) Response of the microbial community to copper oxychloride in acidic sandy loam soil. J Appl Microbiol 98:901–909Google Scholar
  17. Florio A, Clark IM, Hirsch PH, 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 70:795–807CrossRefGoogle Scholar
  18. Florio A, Felici B, Migliore M, Dell’Abate MT, Benedetti A (2015) Nitrogen losses, uptake and abundance of ammonia oxidizers in soil under mineral and organo-mineral fertilization regimes. J Sci Food Agric. doi:10.1002/jsfa.7364 Google Scholar
  19. Garland JL (1996a) Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization. Soil Biol Biochem 28:213–21CrossRefGoogle Scholar
  20. Garland JL (1996b) Patterns of potential C source utilization by rhizosphere communities. Soil Biol Biochem 28:223–30CrossRefGoogle Scholar
  21. Garland JL (1997) Analysis and interpretation of community-level physiological profiles in microbial ecology. FEMS Microbiol Ecol 24:289–300CrossRefGoogle Scholar
  22. Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57:2351–9Google Scholar
  23. Gonzalez M, Gomez E, Comese R, Quesada M, Conti M (2010) Influence of organic amendments on soil quality potential indicators in an urban horticultural system. Bioresour Technol 101:8897–901CrossRefGoogle Scholar
  24. Guo D, Di HJ, Cameron KC, Li B (2014) Effect of application rate of a nitrification inhibitor, dicyandiamide (DCD), on nitrification rate, and ammonia-oxidizing bacteria and archaea growth in a grazed pasture soil:An incubation study. J Soils Sediments 14:897–903CrossRefGoogle Scholar
  25. Hatch D, Trindade H, Cardenas L, Carneiro J, Hawkins J, Scholefield D, Chadwick D (2005) Laboratory study of the effects of two nitrification inhibitors on greenhouse gas emissions from slurry-treated arable soil: impact of diurnal temperature cycle. Biol Fertil Soils 41:225–32CrossRefGoogle Scholar
  26. Hayyis-Hellal J, Vallaeys T, Garnier-Zarli E, Bousserrhine N (2009) Effects of mercury on soil microbial communities in tropical soils of French Guyana. Appl Soil Ecol 41:59–68CrossRefGoogle Scholar
  27. Huang Y, Li Y, Yao H (2013) Nitrate enhances N2O emission more than ammonium in a highly acidic soil. J Soils Sediments 14:146–54CrossRefGoogle Scholar
  28. Insam H, Goberna M (2004) Use of Biolog for the Community Level Physiological Profiling (CLPP) of environmental samples. Mol Microb Ecol Man Second Ed 4(01):853–60Google Scholar
  29. Irigoyen I, Muro J, Azpilikueta M, Aparicio-Tejo P, Lamsfus C (2003) Ammonium oxidation kinetics in the presence of nitrification inhibitors DCD and DMPP at various temperatures. Aust J Soil Res 41:1177–83CrossRefGoogle Scholar
  30. Ishikawa T, Subbarao GV, Ito O, Okada K (2003) Suppression of nitrification and nitrous oxide emission by the tropical grass Brachiaria humidicola. Plant Soil 255:413–9CrossRefGoogle Scholar
  31. Jarvis SC, Stockdale EA, Shepherd MA, Powlson DS (1996) Nitrogen mineralization in temperate agricultural soils: processes and measurement. Adv Agron 57:187–235CrossRefGoogle Scholar
  32. Justice JK, Smith RL (1962) Nitrification of ammonium sulfate in a calcareous soil as influenced by combinations of moisture, temperature, and levels of added nitrogen. Soil Sci Soc Am Proc 26:246–50CrossRefGoogle Scholar
  33. Kamshake LJ, Hannah SA, Comen JM (1967) Automated analysis for nitrate by hydrazine reduction. Water Resour 1:205–16Google Scholar
  34. Kleineidam K, Košmrlj K, Kublik S, Palmer I, Pfab H, Ruser R (2011) Influence of the nitrification inhibitor 3,4-dimethylpyrazole phosphate (DMPP) on ammonia-oxidizing bacteria and archaea in rhizosphere and bulk soil. Chemosphere 84:182–6CrossRefGoogle Scholar
  35. Kroeze C, Mosier A, Bouwman L (1999) Closing the global N2O budget: a retrospective analysis 1500–1994. Glob Biogeochem Cycl 13:1–8CrossRefGoogle Scholar
  36. Li H, Liang X, Chen Y, Lian Y, Tian G, Ni W (2008) Effect of nitrification inhibitor DMPP on nitrogen leaching, nitrifying organisms, and enzyme activities in a rice-oilseed rape cropping system. J Environ Sci 20:149–55CrossRefGoogle Scholar
  37. Lin XG, Yin R, Zhang HY, Huang JF, Chen RR, Cao ZH (2004) Changes of soil microbiological properties caused by land use changing from rice-wheat rotation to vegetable cultivation. Environ Geochem Health 26:119–28CrossRefGoogle Scholar
  38. Linzmeier W, Gutser R, Schmidhalter U (2001) Nitrous oxide emission from soil and from a nitrogen-15-labelled fertilizer with the new nitrification inhibitor 3,4-dimethylpyrazole phosphate (DMPP). Biol Fertil Soils 34:103–8CrossRefGoogle Scholar
  39. 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 15:1113–8CrossRefGoogle Scholar
  40. Lloyd J, Taylor JA (1994) On the temperature dependence of soil respiration. Funct Ecol 8:315–23CrossRefGoogle Scholar
  41. Lupwayi NZ, Harker KN, Dosdall LM, Turkington TK, Blackshaw RE, O’Donovan JT, Carcamo HA, Otani JK, Clayton GW (2009) Changes in functional structure of soil bacterial communities due to fungicide and insecticide applications in canola. Agr Ecosyst Environ 130:109–14CrossRefGoogle Scholar
  42. Macadam XMB, del Prado A, Merino P, Estavillo JM, Pinto M, Gonzales-Murua C (2003) Dicyandiamide and 3,4-dimethyl pyrazole phosphate decrease N2O emissions from grassland but dicyandiamide produces deleterious effects on clover. J Plant Physiol 160:1517–23CrossRefGoogle Scholar
  43. Mahmood T, Ali R, Latif Z, Ishaque W (2011) Dicyandiamide increases the fertilizer N loss from an alkaline calcareous soil treated with 15 N-labelled urea under warm climate and under different crops. Biol Fertil Soils 47:619–31CrossRefGoogle Scholar
  44. Maienza A, Bååth E, Stazi SR, Benedetti A, Grego S, Dell’Abate MT (2014) Microbial dynamics after adding bovine manure effluent together with a nitrification inhibitor (3,4 DMPP) in a microcosm experiment. Biol Fertil Soils 50:869–77CrossRefGoogle Scholar
  45. Marinari S, Masciandaro G, Ceccanti B, Grego S (2000) Influence of organic and mineral fertilisers on soil biological and physical properties. Bioresour Technol 72:9–17CrossRefGoogle Scholar
  46. McCarty GW (1999) Modes of action of nitrification inhibitors. Biol Fertil Soils 29:1–9CrossRefGoogle Scholar
  47. Menéndez S, Merino P, Pinto M, Gonzales-Murua C, Estavillo JM (2006) 3,4-Dimethylpyrazol Phosphate effect on nitrous oxide, nitric oxide, ammonia, and carbon dioxide emissions from grasslands. J Env Qual 35:973–81CrossRefGoogle Scholar
  48. Menéndez S, Barrena I, Setien I, Gonzales-Murua C, Estavillo JM (2012) Efficiency of nitrification inhibitor DMPP to reduce nitrous oxide emissions under different temperature and moisture conditions. Soil Biol Biochem 53:82–9CrossRefGoogle Scholar
  49. Merino P, Menéndez S, Pinto M, Gonzàlez-Murua C, Estavillo JM (2005) 3,4-Dimethylpyrazole phosphate reduces nitrous oxide emissions from grassland after slurry application. Soil Use Manage 21:53–7CrossRefGoogle Scholar
  50. Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700Google Scholar
  51. Myers RJK (1975) Temperature effects on ammonification and nitrification in a tropical soil. Soil Biol Biochem 7:83–6CrossRefGoogle Scholar
  52. Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148:257–66CrossRefGoogle Scholar
  53. 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 42:1425–36CrossRefGoogle Scholar
  54. Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM (2003) Assumption–free analysis of quantitative real-time polymerse chain reaction (PCR) data. Neurosci Lett 339:62–6CrossRefGoogle Scholar
  55. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker Q, van den Hoff MJB, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37:1–12CrossRefGoogle Scholar
  56. Shen WS, Lin XG, Gao N, Shi WM, Min J, He XH (2011) Nitrogen fertilization changes abundance and community composition of ammonia-oxidizing bacteria. Soil Sci Soc Am J 75:2198–205CrossRefGoogle Scholar
  57. Sheng R, Meng DL, Wu MM, Di HJ, Qin HL, Wei WX (2013) Effect of agricultural land use change on community composition of bacteria and ammonia oxidizers. J Soils Sediments 13:1246–56CrossRefGoogle Scholar
  58. Smalla K, Wachtendorf U, Heuer H, Liu WT, Forney L (1998) Analysis of BIOLOG GN substrate utilization patterns by microbial communities. Appl Environ Microbiol 64:1220–5Google Scholar
  59. Stanford G, Smith SJ (1972) Nitrogen mineralization potentials of soils. Soil Sci Soc Am Proc 36:465–72CrossRefGoogle Scholar
  60. Stark JM (1996) Modeling the temperature response of nitrification. Biogeochemistry 35:433–45CrossRefGoogle Scholar
  61. Subbarao GV, Ito O, Sahrawat K, Berry WL, Nakahara K, Ishikawa T (2006) Scope and strategies for regulation of nitrification in agricultural systems-challenges and opportunities. Crit Rev Plant Sci 25:303–35CrossRefGoogle Scholar
  62. Tindaon F, Benckiser G, Ottow JCG (2012) Evaluation of ecological doses of the nitrification inhibitors 3,4-dimethylpyrazole phosphate (DMPP) and 4-chloromethylpyrazole (ClMP) in comparison to dicyandiamide (DCD) in their effects on dehydrogenase and dimethyl sulfoxide reductase activity in soils. Biol Fertil Soils 48:643–50CrossRefGoogle Scholar
  63. Töwe S, Kleineidam K, Schloter M (2010) Differences in amplification efficiency of standard curves in quantitative real-time PCR assays and consequences for gene quantification in environmental samples. J Microbiol Methods 82:338–41CrossRefGoogle Scholar
  64. Wall L, Gehrke CW, Neuner JE, Lathey RD, Rexnord PR (1975) Cereal protein nitrogen: evolution and comparison of four different methods. Assoc Off Anal Chem 58:811–7Google Scholar
  65. Weber KP, Grove JA, Gehder M, Anderson WA, Legge RL (2007) Data transformations in the analysis of community-level substrate utilization data from microplates. J Microbiol Methods 69:461–9CrossRefGoogle Scholar
  66. 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 34:109–17CrossRefGoogle Scholar
  67. World Reference Base for Soil Resources (2006) A framework for international classification, correlation and communications. World Soil Resources Reports 103Google Scholar
  68. Yang J, Li X, Xu L, Hu F, Li H, Liu M (2012) Influence of the nitrification inhibitor DMPP on the community composition of ammonia-oxidizing bacteria at microsites with increasing distance from the fertilizer zone. Biol Fertil Soils 49:23–30CrossRefGoogle Scholar
  69. Zerulla W, Barth T, Dressel J, Erhardt K, von Locquenghien KH, Pasda G (2001) 3,4-Dimethylpyrazole phosphate (DMPP)—a new nitrification inhibitor for agriculture and horticulture. Biol Fertil Soils 34:79–84CrossRefGoogle Scholar
  70. Zhao CS, Hu CX, Huang W, Sun XC, Tan QL, Di HJ (2010) A lysimeter study of nitrate leaching and optimum nitrogen application rates for intensively irrigated vegetable production systems in Central China. J Soils Sediments 10:9–17CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Consiglio per la ricerca in agricoltura e l’analisi dell’economia agraria, Centro di ricerca per lo studio delle relazioni tra pianta e suolo – Via della Navicella 2-4RomeItaly
  2. 2.Ecologie Microbienne, Université Lyon 1, Université de Lyon, CNRS UMR 5557, INRA UMR 1418Villeurbanne cedexFrance
  3. 3.National Research CouncilInstitute of Biometeorology (IBIMET-CNR)FlorenceItaly
  4. 4.Department of Science and Technology for Agricultural (DAFNE)Tuscia UniversityViterboItaly

Personalised recommendations