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Plant and soil effects on denitrification potential in agricultural soils

  • François Malique
  • Piaopiao Ke
  • Jürgen Boettcher
  • Michael Dannenmann
  • Klaus Butterbach-BahlEmail author
Regular Article
  • 146 Downloads

Abstract

Background and aims

Microbial denitrification is the primary driver of nitrogen losses from the plant-soil system and the key process for the closure of the global N cycle. All major controls of denitrification might be directly or indirectly affected by plants. However, there is a lack of research of the direct effects of plants on soil denitrification and how this effect might be mediated by soil properties. This study assesses the effect of three common crop species and two agricultural soils on denitrification potentials.

Methods

We conducted a factorial experiment under controlled conditions to analyze the effects of (1) different plant species (barley, wheat or ryegrass), (2) two different soils (texture/ SOC) and (3) two different soil moisture levels on Denitrification Enzyme Activity (DEA) in bulk and rhizosphere soil.

Results

The SOC richer clay loam soil showed on average higher DEA (+81%) compared to the SOC poorer silty loam soil. All three plants were found to stimulate denitrification with significant differences between certain species: rye grass (+92% ± 14%) ≥ barley (+75% ± 26%) ≥ wheat (+50% ± 19%).

Conclusions

DEA in agricultural soils is interactively controlled by plant species and soil type with an overall stimulating effect of plants on the denitrification potential. Future research should focus on disentangling single mechanisms of plant control on actual denitrification rates and N gas product ratios.

Keywords

Denitrification potential DEA Plant stimulation Soil texture 

Notes

Acknowledgements

We gratefully acknowledge Daniel Maurer, Anja Schäfler-Schmid, Tatiana Rittl, Julia Pazmino Murillo, Robin Jahn and Madeleine Nicolas for help during laboratory work, preparation of the setup of the experiment, and/or suggestions on writing. Data of the soil properties were provided by DASIM (Denitrification in Agricultural Soils – Integrated control and Modelling) research unit. We thank the German Science Foundation for funding our work through the research unit DFG-FOR 2337: DASIM.

Supplementary material

11104_2019_4038_MOESM1_ESM.docx (149 kb)
ESM 1 (DOCX 148 KB)

References

  1. Alldred M, Baines SB (2016) Effects of wetland plants on denitrification rates: a meta­ analysis. Ecol Appl 26:676–685CrossRefGoogle Scholar
  2. Bardon C, Piola F, Bellvert F, Haichar FZ, Comte G, Meiffren G, Pommier T, Puijalon S, Tsafack N, Poly F (2014) Evidence for biological denitrification inhibition (BDI) by plant secondary metabolites. New Phytol 204:620–630.  https://doi.org/10.1111/nph.12944 CrossRefGoogle Scholar
  3. Bardon C, Piola F, Haichar Z et al (2015) Identification of B-type procyanidins in Fallopia spp . Involved in biological denitrification inhibition. Environ Microbiol 18:644–655.  https://doi.org/10.1111/1462-2920.13062 CrossRefGoogle Scholar
  4. Bardon C, Poly F, Piola F et al (2016) Mechanism of biological denitrification inhibition: procyanidins induce an allosteric transition of the membrane-bound nitrate reductase through membrane alteration. FEMS Microbiol Ecol 92:1–11CrossRefGoogle Scholar
  5. Blagodatskaya EV, Blagodatsky SA, Anderson TH, Kuzyakov Y (2009) Contrasting effects of glucose, living roots and maize straw on microbial growth kinetics and substrate availability in soil. Eur J Soil Sci 60:186–197.  https://doi.org/10.1111/j.1365-2389.2008.01103.x CrossRefGoogle Scholar
  6. Blagodatskaya E, Littschwager J, Lauerer M, Kuzyakov Y (2010) Growth rates of rhizosphere microorganisms depend on competitive abilities of plants and N supply. Plant Biosyst 144:408–413.  https://doi.org/10.1080/11263501003718596 CrossRefGoogle Scholar
  7. Bonaglia S, Nascimento FJA, Bartoli M, Klawonn I, Brüchert V (2014) Meiofauna increases bacterial denitrification in marine sediments. Nat Commun 5:5133.  https://doi.org/10.1038/ncomms6133 CrossRefGoogle Scholar
  8. Boyer EW, Alexander RB, Parton WJ, Li C, Butterbach-Bahl K, Donner SD, Skaggs RW, Grosso SJD (2006) Modeling denitrification in terrestrial and aquatic ecosystems at regional scales. Ecol Appl 16:2123–2142. https://doi.org/10.1890/1051-0761(2006)016[2123:MDITAA]2.0.CO;2Google Scholar
  9. Burford JR, Bremner JM (1975) Relationships between the denitrification capacities of soils and total, water-soluble and readily decomposable soil organic matter. Soil Biol Biochem 7:389–394.  https://doi.org/10.1016/0038-0717(75)90055-3 CrossRefGoogle Scholar
  10. Butterbach-Bahl K, Baggs EM, Dannenmann M et al (2013) Nitrous oxide emissions from soils : how well do we understand the processes and their controls ? Nitrous oxide emissions from soils : how well do we understand the processes and their controls ? Author for correspondence. Philos Trans R Soc Lond Ser B Biol Sci 368:20130122.  https://doi.org/10.1098/rstb.2013.0165 CrossRefGoogle Scholar
  11. Cantarel AAM, Pommier T, Desclos-Theveniau M, Diquélou S, Dumont M, Grassein F, Kastl EM, Grigulis K, Laîné P, Lavorel S, Lemauviel-Lavenant S, Personeni E, Schloter M, Poly F (2015) Using plant traits to explain plant–microbe relationships involved in nitrogen acquisition. Ecology 96:788–799.  https://doi.org/10.1890/13-2107.1 CrossRefGoogle Scholar
  12. Cavigelli MA, Robertson GP, Ecology S, May N (2000) The functional significance of denitrifier community composition in a terrestrial ecosystem. Ecology 81:1402–1414CrossRefGoogle Scholar
  13. D’Haene K, Moreels E, De Neve S et al (2003) Soil properties influencing the denitrification potential of Flemish agricultural soils. Biol Fertil Soils 38:358–366.  https://doi.org/10.1007/s00374-003-0662-x CrossRefGoogle Scholar
  14. Davidson EA, Schimel JP (1995) Microbial processes of production and consumption of nitric oxide, nitrous oxide and methane. In: Matson PA, Harriss RD (eds) Biogenic trace gases: measuring emissions from soil and water. Springer, New York, pp 327–357Google Scholar
  15. Davidson EA, Seitzinger SP (2006) The enigma of progess in denitrification research. Ecol Appl 16:2057–2063. https://doi.org/10.1890/1051-0761(2006)016[2057:TEOPID]2.0.CO;2Google Scholar
  16. Domeignoz-Horta LA, Philippot L, Peyrard C, Bru D, Breuil MC, Bizouard F, Justes E, Mary B, Léonard J, Spor A (2018) Peaks of in situ N2O emissions are influenced by N2O-producing and reducing microbial communities across arable soils. Glob Chang Biol 24:360–370.  https://doi.org/10.1111/gcb.13853 CrossRefGoogle Scholar
  17. Firestone MK, Davidson EA (1989) Summary for policymakers. In: Intergovernmental panel on climate change (ed) Climate change 2013 - the physical science basis. Cambridge University Press, Cambridge, pp 1–30Google Scholar
  18. Gaillard R, Duval BD, Osterholz WR, Kucharik CJ (2016) Simulated effects of soil texture on nitrous oxide emission factors from corn and soybean agroecosystems in Wisconsin. J Environ Qual 45:1540.  https://doi.org/10.2134/jeq2016.03.0112 CrossRefGoogle Scholar
  19. Gödde M, Conrad R (2000) Influence of soil properties on the turnover of nitric oxide and nitrous oxide by nitrification and denitrification at constant temperature and moisture. Biol Fertil Soils 32:120–128.  https://doi.org/10.1007/s003740000247 CrossRefGoogle Scholar
  20. Groffman PM, Holland EA, Myrold DD et al (1999) Denitrification. In: Robertson GP, Coleman DC, Bledsoe CS, Sollins P (eds) Standard soil methods for long-term ecological research. Oxford University Press, New York, pp 277–288Google Scholar
  21. Groffman PM, Altabet MA, Bohlke JK et al (2006) Methods for measuring denitrification: diverse approaches to a difficult problem. Ecol Appl 16:2091–2122. https://doi.org/10.1890/1051-0761(2006)016[2091:MFMDDA]2.0.CO;2Google Scholar
  22. Guo L, Lin H (2018) Addressing two bottlenecks to advance the understanding of preferential flow in soils. In: Advances in Agronomy, pp 61–117Google Scholar
  23. Guyonnet JP, Vautrin F, Meiffren G, Labois C, Cantarel AAM, Michalet S, Comte G, Haichar FZ (2017) The effects of plant nutritional strategy on soil microbial denitrification activity through rhizosphere primary metabolites. Ecology 93:1–11.  https://doi.org/10.1093/femsec/fix022 Google Scholar
  24. Haichar FEZ, Marol C, Berge O et al (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230.  https://doi.org/10.1038/ismej.2008.80 CrossRefGoogle Scholar
  25. Henry S, Texier S, Hallet S, Bru D, Dambreville C, Chèneby D, Bizouard F, Germon JC, Philippot L (2008) Disentangling the rhizosphere effect on nitrate reducers and denitrifiers: insight into the role of root exudates. Environ Microbiol 10:3082–3092.  https://doi.org/10.1111/j.1462-2920.2008.01599.x CrossRefGoogle Scholar
  26. Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152.  https://doi.org/10.1007/s11104-008-9885-9 CrossRefGoogle Scholar
  27. Holland EA, Robertson GP, Greenberg J et al (1999) Soil CO2, N2O and CH4 exchange. In: Robertson GP, Bledsoe CS, Coleman DC, Sollins P (eds) Standard soil methods for long-term ecological research. Oxford University Press, New York, pp 185–201Google Scholar
  28. Husson O (2013) Redox potential (eh) and pH as drivers of soil/plant/microorganism systems: a transdisciplinary overview pointing to integrative opportunities for agronomy. Plant Soil 362:389–417.  https://doi.org/10.1007/s11104-012-1429-7 CrossRefGoogle Scholar
  29. Jäger HJ, Schmidt SW, Kammann C et al (2003) The University of Gießen Free-Air Carbon Dioxide Enrichment study: description of the experimental site and of a new enrichment system. J Appl Bot Bot 77:117–127Google Scholar
  30. Jamali H, Quayle W, Scheer C, Rowlings D, Baldock J (2016) Effect of soil texture and wheat plants on N2O fluxes: a lysimeter study. Agric For Meteorol 223:17–29.  https://doi.org/10.1016/j.agrformet.2016.03.022 CrossRefGoogle Scholar
  31. Keiluweit M, Gee K, Denney A, Fendorf S (2018) Anoxic microsites in upland soils dominantly controlled by clay content. Soil Biol Biochem 118:42–50.  https://doi.org/10.1016/j.soilbio.2017.12.002 CrossRefGoogle Scholar
  32. Kesik M, Blagodatsky S, Papen H, Butterbach-Bahl K (2006) Effect of pH, temperature and substrate on N2O, NO and CO2 production by Alcaligenes faecalis p. J Appl Microbiol 101:655–667.  https://doi.org/10.1111/j.1365-2672.2006.02927.x CrossRefGoogle Scholar
  33. Kimbrough DE, Kouame Y, Moheban P, Springthorpe S (2006) The effect of electrolysis and oxidation-reduction potential on microbial survival, growth and disinfection. Int J Environ Pollut 27:211–221.  https://doi.org/10.1504/IJEP.2006.010464 CrossRefGoogle Scholar
  34. Klemedtsson L, Simkins S, Svensson BH, Johnsson H, Rosswall T (1991) Soil denitrification in three cropping systems characterized by differences in nitrogen and carbon supply. Plant Soil 138:273–286.  https://doi.org/10.1007/BF00012254 CrossRefGoogle Scholar
  35. Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669.  https://doi.org/10.1111/nph.12235 CrossRefGoogle Scholar
  36. Maag M, Vinther FP (1996) Nitrous oxide emission by nitrification and denitrification in different soil types and at different soil moisture contents and temperatures. Appl Soil Ecol 4:5–14CrossRefGoogle Scholar
  37. McGill BM, Sutton-Grier AE, Wright JP (2010) Plant trait diversity buffers variability in denitrification potential over changes in season and soil conditions. PLoS One 5:e11618.  https://doi.org/10.1371/journal.pone.0011618 CrossRefGoogle Scholar
  38. Payne EGI, Fletcher TD, Cook PLM, Deletic A, Hatt BE (2014) Processes and drivers of nitrogen removal in stormwater biofiltration. Crit Rev Environ Sci Technol 44:796–846.  https://doi.org/10.1080/10643389.2012.741310 CrossRefGoogle Scholar
  39. Philippot L, Hallin S, Schloter M (2007) Ecology of denitrifying prokaryotes in agricultural soil. In: Advances in agronomy, pp 249–305Google Scholar
  40. Phogat VK, Tomar VS, Dahiya R (2015) Soil physical properties. In: Rattan RK, Katyal JC, Dwivedi BS et al (eds) Soil science: an introduction. Indian Society of Soil Sciences, pp 135–171Google Scholar
  41. Putz M, Schleusner P, Rütting T, Hallin S (2018) Relative abundance of denitrifying and DNRA bacteria and their activity determine nitrogen retention or loss in agricultural soil. Soil Biol Biochem 123:97–104.  https://doi.org/10.1016/j.soilbio.2018.05.006 CrossRefGoogle Scholar
  42. Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science (80- ) 326:123–125.  https://doi.org/10.1126/science.1176985 CrossRefGoogle Scholar
  43. Rigby H, Clarke BO, Pritchard DL, Meehan B, Beshah F, Smith SR, Porter NA (2016) A critical review of nitrogen mineralization in biosolids-amended soil, the associated fertilizer value for crop production and potential for emissions to the environment. Sci Total Environ 541:1310–1338.  https://doi.org/10.1016/j.scitotenv.2015.08.089 CrossRefGoogle Scholar
  44. Schaufler G, Kitzler B, Schindlbacher A, Skiba U, Sutton MA, Zechmeister-Boltenstern S (2010) Greenhouse gas emissions from European soils under different land use: effects of soil moisture and temperature. Eur J Soil Sci 61:683–696CrossRefGoogle Scholar
  45. Schindlbacher A, Zechmeister-boltenstern S, Butterbach-bahl K (2004) Effects of soil moisture and temperature on NO, NO2, and N2O emissions from European forest soils. J Geophys Res 109:1–12.  https://doi.org/10.1029/2004JD004590 CrossRefGoogle Scholar
  46. Seitzinger S, Harrison J, Bohlke J et al (2006) Denitrification across landscaes and waterscapes: a synthesis. Ecol Appl 16:2064–2090. https://doi.org/10.1890/1051-0761(2006)016[2064:DALAWA]2.0.CO;2Google Scholar
  47. Simek M, Cooper JE (2002) The influence of soil pH on denitrification: progress towards the understanding of this interaction over the last 50 years. Eur J Soil Sci 53:345–354.  https://doi.org/10.1046/j.1365-2389.2002.00461.x CrossRefGoogle Scholar
  48. Singh B, Ryden JC, Whitehead DC (1989) Denitrification potential and actual rates of denitrification in soils under long-term grassland and arable cropping. Soil Biol Biochem 21:897–901CrossRefGoogle Scholar
  49. Smith MS, Tiedje JM (1979) The effect of roots on soil Denitrification1. Soil Sci Soc Am J 43:951.  https://doi.org/10.2136/sssaj1979.03615995004300050027x CrossRefGoogle Scholar
  50. Stanford G, Epstein E (1974) Nitrogen mineralization-water relations in soils. Soil Sci Soc Am J 38:103–107.  https://doi.org/10.2136/sssaj1974.03615995003800010032x CrossRefGoogle Scholar
  51. Sutton-Grier AE, Wright JP, McGill BM, Richardson C (2011) Environmental conditions influence the plant functional diversity effect on potential denitrification. PLoS One 6:1–10.  https://doi.org/10.1371/journal.pone.0016584 CrossRefGoogle Scholar
  52. Sutton-Grier AE, Wright JP, Richardson CJ (2013) Different plant traits affect two pathways of riparian nitrogen removal in a restored freshwater wetland. Plant Soil 365:41–57.  https://doi.org/10.1007/s11104-011-1113-3 CrossRefGoogle Scholar
  53. Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Environmental microbiology of anaerobes. John Wiley & Sons, Inc., pp 179–244Google Scholar
  54. van der Salm C, Dolfing J, Heinen M, Velthof GL (2007) Estimation of nitrogen losses via denitrification from a heavy clay soil under grass. Agric Ecosyst Environ 119:311–319.  https://doi.org/10.1016/j.agee.2006.07.018 CrossRefGoogle Scholar
  55. Viotti P, Collivignarelli MC, Martorelli E, Raboni M (2016) Oxygen control and improved denitrification efficiency by dosing ferrous ions in the anoxic reactor. Desalin Water Treat 57:18240–18247.  https://doi.org/10.1080/19443994.2015.1089200 CrossRefGoogle Scholar
  56. Wallenstein MD, Myrold DD, Firestone M, Voytek M (2006) Environmental controls on denitrifying communities and denitrification rates: insights from molecular methods. Ecol Appl 16:2143–2152CrossRefGoogle Scholar
  57. World Programme for the Census of Agriculture (2010) Classification of crops. Appendix 3Google Scholar
  58. Yamashita T, Flessa H, John B, Helfrich M, Ludwig B (2006) Organic matter in density fractions of water-stable aggregates in silty soils: effect of land use. Soil Biol Biochem 38:3222–3234.  https://doi.org/10.1016/j.soilbio.2006.04.013 CrossRefGoogle Scholar
  59. Yanai RD, Majdi H, Park BB (2003) Measured and modelled differences in nutrient concentrations between rhizosphere and bulk soil in a Norway spruce stand. Plant Soil 257:133–142.  https://doi.org/10.1023/A:1026257508033 CrossRefGoogle Scholar
  60. Zak DR, Pregitzer KS, King JS, Holmes WE (2000) Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis. New Phytol 147:201–222CrossRefGoogle Scholar
  61. Zhang Y, Duan B, Xian JR, Korpelainen H, Li C (2011) Links between plant diversity, carbon stocks and environmental factors along a successional gradient in a subalpine coniferous forest in Southwest China. For Ecol Manag 262:361–369.  https://doi.org/10.1016/j.foreco.2011.03.042 CrossRefGoogle Scholar
  62. Zhang S, Liu F, Xiao R, Li Y, He Y, Wu J (2016) Effects of vegetation on ammonium removal and nitrous oxide emissions from pilot-scale drainage ditches. Aquat Bot 130:37–44.  https://doi.org/10.1016/j.aquabot.2016.01.003 CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Institute for Meteorology and Climate Research, Atmospheric Environmental Research (IMK-IFU)Karlsruhe Institute of Technology (KIT)Garmisch-PartenkirchenGermany
  2. 2.State Key Laboratory of Environmental Simulation and Pollution Control, School of EnvironmentTsinghua UniversityBeijingChina
  3. 3.Institute of Soil ScienceLeibniz University HannoverHannoverGermany

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