Advertisement

Effect of nitrogen fertilisation on nitrous oxide emission and the abundance of microbial nitrifiers and denitrifiers in the bulk and rhizosphere soil of Solanum lycopersicum and Phaseolus vulgaris

  • Antonio Castellano-HinojosaEmail author
  • Jesús González-López
  • Eulogio J. Bedmar
Regular Article
  • 35 Downloads

Abstract

Aims

To determine the effect of three N-fertilisers on N2O emission and abundance of nitrification and denitrification genes in bulk and rhizosphere soil of tomato and common bean, two vegetable crops representative of main horticultural crops in South Spain.

Methods

Four consecutive harvests of tomato and common bean fertilised with urea, ammonium or nitrate were carried out. The total abundance of bacteria, archaea, nitrifiers and denitrifiers was estimated by quantitative PCR. Soil physicochemical properties and N2O emission were also determined.

Results

Regardless of the plant species, the highest N2O emission was produced by the soil treated with urea, followed by ammonium and nitrate. Bacteria were more abundant than archaea in the bulk and rhizosphere soil. The abundance of the ammonia-oxidising archaea was greater than the ammonia-oxidising bacteria in the rhizosphere, but lower in the bulk soil. N-fertilisation increased the gene copy number of denitrifiers, which were more abundant in the bulk soil.

Conclusions

N-fertilisation decreases N2O production due to increased abundance of the nosZ gene. The abundance of nitrification and denitrification genes in bulk and rhizosphere soils is dependent on the type of fertiliser. For both plant species, the ratio of the genes involved in production and reduction of N2O by bulk and rhizosphere was similar.

Keywords

Nitrogen fertiliser Nitrification genes Denitrification genes qPCR Cultivated soil 

Notes

Acknowledgements

Comments from anonymous reviewers helped improved this manuscript.

Funding information

This study was supported by the ERDF-cofinanced grant PEAGR2012-1968 from Consejería de Economía, Innovación y Ciencia (Junta de Andalucía, Spain) and the MINECO-CSIC Agreement RECUPERA 2020. ACH is the recipient of a grant of MECD (FPU 2014/01633).

Supplementary material

11104_2019_4188_MOESM1_ESM.docx (62 kb)
ESM 1 (DOCX 62 kb)

References

  1. Ågren GI, Wetterstedt JÅ, Billberger MFK (2012) Nutrient limitation on terrestrial plant growth - modeling the interaction between nitrogen and phosphorus. New Phytol 194:953–960.  https://doi.org/10.1111/j.1469-8137.2012.04116.x CrossRefGoogle Scholar
  2. Arnaldos M, Kunkel SA, Stark BC, Pagilla KR (2013) Enhanced heme protein expression by ammonia-oxidizing communities acclimated to low dissolved oxygen conditions. Appl Microbiol Biotechnol 97:10211–10221.  https://doi.org/10.1007/s00253-013-4755-7 CrossRefGoogle Scholar
  3. Bárta J, Melichová T, Vaněk D, Picek T, Šantrůčková H (2010) Effect of pH and dissolved organic matter on the abundance of nirK and nirS denitrifiers in spruce forest soil. Biogeochemistry 101:123–132.  https://doi.org/10.1007/s10533-010-9430-9
  4. Bueno E, Mesa S, Bedmar EJ, Richardson DJ, Delgado MJ (2012) Bacterial adaptation of respiration from oxic to microoxic and anoxic conditions: redox control. Antioxid Redox Signal 16:819–852.  https://doi.org/10.1089/ars.2011.4051
  5. 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? Phil Trans R Soc A 368:91–97.  https://doi.org/10.1098/rstb.2013.0122 Google Scholar
  6. 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 CrossRefGoogle Scholar
  7. Correa-Galeote D, Tortosa G, Bedmar EJ (2014) Quantification of functional microbial nitrogen cycle genes in environmental samples. In: Marco DE (ed) Metagenomics of the microbial nitrogen cycle: theory, methods and applications. Caister Academic Press, Norwich, pp 65–85Google Scholar
  8. Coskun D, Britto DT, Shi W, Kronzucker HJ (2017) How plant root exudates shape the nitrogen cycle. Trends Plant Sci 8:661–673.  https://doi.org/10.1016/j.tplants.2017.05.004 CrossRefGoogle Scholar
  9. Danielson RE, Sutherland PL (1986) Porosity. In: Klute A (ed) Methods of soil analysis part 1. Physical and mineralogical methods, agronomy monograph no. 9. Soil Science Society of America, Madison, pp 443–461Google Scholar
  10. De Vries FT, Bardgett RD (2016) Plant community controls on short term ecosystem nitrogen retention. New Phytol 210:861–874.  https://doi.org/10.1111/nph.13832 CrossRefGoogle Scholar
  11. De Vries FT, Jørgensen HB, Hedlund K, Bardgett RD (2015) Disentangling plant and soil microbial controls on carbon and nitrogen loss in grassland mesocosms. J Ecol 103:629–640.  https://doi.org/10.1111/1365-2745.12383 CrossRefGoogle Scholar
  12. Edgerton MD (2009) Increasing crop productivity to meet global needs for feed, food and fuel. Plant Physiol 149:7–13.  https://doi.org/10.1104/pp.108.130195 CrossRefGoogle Scholar
  13. Enwall K, Nyberg K, Bertilsson S, Cederlund H, Stenström J, Hallin S (2007) Long-term impact of fertilization on activity and composition of bacterial communities and metabolic guilds in agricultural soil. Soil Biol Biochem 39:106–115.  https://doi.org/10.1016/j.soilbio.2006.06.015 CrossRefGoogle Scholar
  14. Erisman JW, Galloway JN, Dice NB, Sutton MA, Bleeker A, Grizzetti B et al (2015) Nitrogen: too much of a vital resource. Science Brief. WWF Netherlands, ZeistGoogle Scholar
  15. FAO (2017) Soil organic carbon: the hidden potential. Food and Agriculture Organization of the United Nations, Rome. http://www.fao.org/3/a-i6937e.pdf. Accessed 15 May 2019Google Scholar
  16. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892.  https://doi.org/10.1126/science.1136674 CrossRefGoogle Scholar
  17. Giles ME, Morley NJ, Baggs EM, Daniell TJ (2012) Soil nitrate reducing processes – drivers, mechanisms for spatial variation and significance for nitrous oxide production. Front Microbiol 3:407.  https://doi.org/10.3389/fmicb.2012.00407 CrossRefGoogle Scholar
  18. Glaser K, Hackl E, Inselsbacher E, Strauss J, Wanek W, Zechmeister-Boltenstern S, Sessitsch A (2010) Dynamics of ammonia oxidizing communities in barley-planted bulk soil and rhizosphere following nitrate and ammonium fertilizer amendment. FEMS Microbiol Ecol 74:575–591.  https://doi.org/10.1111/j.1574-6941.2010.00970.x CrossRefGoogle Scholar
  19. Gojon A (2017) Nitrogen nutrition in plants: rapid progress and new challenges. J Exp Bot 68:2457–2462.  https://doi.org/10.1093/jxb/erx171 CrossRefGoogle Scholar
  20. González-Martínez A, Rodríguez-Sánchez A, García-Ruiz MJ, Muñoz-Palazón B, Cortes-Lorenzo C, Osorio F et al (2016) Performance and bacterial community dynamics of a CANON bioreactor acclimated from high to low operational temperatures. Chem Eng J 287:557–567.  https://doi.org/10.1016/j.cej.2015.11.081 CrossRefGoogle Scholar
  21. Guyonnet JP, Vautrin F, Meiffren G, Labois C, Cantarel AA, Michalet S et al (2017) The effects of plant nutritional strategy on soil microbial denitrification activity through rhizosphere primary metabolites. FEMS Microbiol Ecol 93:fix022.  https://doi.org/10.1093/femsec/fix022 CrossRefGoogle Scholar
  22. Hai B, Diallo NH, Sall S, Haesler F, Schauss K, Bonzi M, Assigbetse K, Chotte JL, Munch JC, Schloter M (2009) Quantification of key genes steering the microbial nitrogen cycle in the rhizosphere of sorghum cultivars in tropical agroecosystems. Appl Environ Microbiol 75:4993–5000.  https://doi.org/10.1128/AEM.02917-08 CrossRefGoogle Scholar
  23. Hamonts K, Clough TJ, Stewart A, Clinton PW, Richardson AE, Wakelin SA, O’Callaghan M, Condron LM (2013) Effect of nitrogen and waterlogging on denitrifier gene abundance, community structure and activity in the rhizosphere of wheat. FEMS Microbiol Ecol 83:568–584.  https://doi.org/10.1111/1574-6941.12015 CrossRefGoogle Scholar
  24. Harty MA, Forrestal PJ, Watson CJ, McGeough KL, Carolan R, Elliot C et al (2016) Reducing nitrous oxide emissions by changing N fertiliser use from calcium ammonium nitrate (CAN) to urea based formulations. Sci Total Environ 563-564:576–586.  https://doi.org/10.1016/j.scitotenv.2016.04.120 CrossRefGoogle Scholar
  25. Hu HW, Chen DL, He JZ (2015) Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiol Rev 39:729–749.  https://doi.org/10.1093/femsre/fuv021 CrossRefGoogle Scholar
  26. Hussain Q, Liu Y, Jin Z, Zhang A, Pan G, Li L, Crowley D, Zhang X, Song X, Cui L (2011) Temporal dynamics of ammonia oxidizer (amoA) and denitrifier (nirK) communities in the rhizosphere of a rice ecosystem from Tai Lake region, China. Appl Soil Ecol 48:210–218.  https://doi.org/10.1016/j.apsoil.2011.03.004 CrossRefGoogle Scholar
  27. IPCC (2013) Summary for policymakers, Climate change 2013: the physical science basis, Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds.), Cambridge University Press, CambridgeGoogle Scholar
  28. Ke XB, Angel R, Lu YH, Conrad R (2013) Niche differentiation of ammonia oxidizers and nitrite oxidizers in rice paddy soil. Environ Microbiol 15:2275–2292.  https://doi.org/10.1111/1462-2920.12098 CrossRefGoogle Scholar
  29. Liu R, Hayden HL, Suter H, Hu H, Lam SK, He J, Mele PM, Chen D (2017) The effect of temperature and moisture on the source of N2O and contributions from ammonia oxidizers in an agricultural soil. Biol Fertil Soils 53:141–152.  https://doi.org/10.1007/s00374-016-1167-8 CrossRefGoogle Scholar
  30. Lu C, Tian H (2017) Global nitrogen and phosphorus fertilizer use for agriculture production in the past half century: shifted hot spots and nutrient imbalance. Earth Syst Sci Data 9:181–192.  https://doi.org/10.5194/essd-9-181-2017 CrossRefGoogle Scholar
  31. Martínez-Romero E (2003) Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant Soil 252:11–23.  https://doi.org/10.1023/A:1024199013926 CrossRefGoogle Scholar
  32. Meier IC, Finzi AC, Phillips RP (2017) Root exudates increase N availability by stimulating microbial turnover of fast-cycling N pools. Soil Biol Biochem 106:119–128.  https://doi.org/10.1016/j.soilbio.2016.12.004 CrossRefGoogle Scholar
  33. Mommer L, Hinsinger P, Prigent-Combaret C, Visser EJW (2016) Advances in the rhizosphere: stretching the interface of life. Plant Soil 407:1–8.  https://doi.org/10.1007/s11104-016-3040-9 CrossRefGoogle Scholar
  34. Nie SA, Xu HJ, Li S, Li H, Su JQ (2014) Relationships between abundance of microbial functional genes and the status and fluxes of carbon and nitrogen in rice rhizosphere and bulk soils. Pedosphere 24:645–651.  https://doi.org/10.1016/S1002-0160(14)60050-3 CrossRefGoogle Scholar
  35. Pan H, Ying S, Liu H, Zeng L, Zhang Q, Liu Y, Xu J, Li Y, di H (2018) Microbial pathways for nitrous oxide emissions from sheep urine and dung in a typical steppe grassland. Biol Fertil Soils 54:717–730.  https://doi.org/10.1007/s00374-018-1297-2 CrossRefGoogle Scholar
  36. Philippot L, Hallin S, Borjesson G, Baggs EM (2009) Biochemical cycling in the rhizosphere having an impact on global change. Plant Soil 321:61–81.  https://doi.org/10.1007/s11104-008-9796-9 CrossRefGoogle Scholar
  37. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799.  https://doi.org/10.1038/nrmicro3109 CrossRefGoogle Scholar
  38. Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531.  https://doi.org/10.1016/j.tim.2012.08.001 CrossRefGoogle Scholar
  39. 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.117698 CrossRefGoogle Scholar
  40. Rengel Z, Marschner P (2005) Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytol 168:305–312.  https://doi.org/10.1111/j.1469-8137.2005.01558.x CrossRefGoogle Scholar
  41. Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339.  https://doi.org/10.1007/s11104-009-9895-2 CrossRefGoogle Scholar
  42. Sebilo M, Mayer B, Nicolardot B, Pinay G, Mariotti A (2013) Long-term fate of nitrate fertilizer in agricultural soils. Proc Natl Acad Sci U S A 110:18185–18189.  https://doi.org/10.1073/2Fpnas.1305372110 CrossRefGoogle Scholar
  43. Sigurdarson JJ, Svane S, Karring H (2018) The molecular processes of urea hydrolysis in relation to ammonia emissions from agriculture. Rev Environ Sci Biotechnol 17:241–258.  https://doi.org/10.1007/s11157-018-9466-1 CrossRefGoogle Scholar
  44. Subbarao GV, Yoshihashi T, Worthington M, Nakahara K, Ando Y, Sahrawat KL, Rao IM, Lata JC, Kishii M, Braun HJ (2015) Suppression of soil nitrification by plants. Plant Sci 233:155–164.  https://doi.org/10.1016/j.plantsci.2015.01.012 CrossRefGoogle Scholar
  45. Thion CE, Poirel JD, Cornulier T, De Vries FT, Bardgett RD, Prosser JI (2016) Plant nitrogen-use strategy as a driver of rhizosphere archaeal and bacterial ammonia oxidiser abundance. FEMS Microbiol Ecol 92:fiw091.  https://doi.org/10.1093/femsec/fiw091 CrossRefGoogle Scholar
  46. Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677.  https://doi.org/10.1038/nature01014 CrossRefGoogle Scholar
  47. Tortosa G, Hidalgo A, Salas A, Bedmar EJ, Mesa S, Delgado MJ (2015) Nitrate and flooding induce N2O emissions from soybean nodule. Symbiosis 67:1–3.  https://doi.org/10.1007/s13199-015-0341-3 CrossRefGoogle Scholar
  48. Trias R, Ruiz-Rueda O, Garcia-Lledó A, Vilar-Sanz A, López-Flores R, Quintana XD et al (2012) Emergent macrophytes act selectively on ammonia-oxidizing bacteria and archaea. Appl Environ Microbiol 78:6352–6356.  https://doi.org/10.1128/AEM.00919-12 CrossRefGoogle Scholar
  49. Wei B, Yu X, Zhang S, Gu L (2011) Comparison of the community structures of ammonia-oxidizing bacteria and archaea in rhizoplanes of floating aquatic macrophytes. Microbiol Res 166:468–474.  https://doi.org/10.1016/j.micres.2010.09.001 CrossRefGoogle Scholar
  50. Zhai Y, Hou M, Nie S (2018) Variance of microbial composition and structure and relation with soil properties in rhizospheric and non-rhizospheric soil of a flooded paddy. Paddy Water Environ 16:163–172.  https://doi.org/10.1007/s10333-017-0627-6 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Soil Microbiology and Symbiotic SystemsEstación Experimental del Zaidín, CSICGranadaSpain
  2. 2.Department of Microbiology, Faculty of PharmacyUniversity of GranadaGranadaSpain

Personalised recommendations