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Field-Scale Pattern of Denitrifying Microorganisms and N2O Emission Rates Indicate a High Potential for Complete Denitrification in an Agriculturally Used Organic Soil

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Abstract

More than 50% of all anthropogenic N2O emissions come from the soil. Drained Histosols that are used for agricultural purposes are particularly potent sources of denitrification due to higher stocks of organic matter and fertiliser application. However, conditions that favour denitrification can vary considerably across a field and change significantly throughout the year. Spatial and temporal denitrifier dynamics were assessed in a drained, intensely managed Histosol by focusing on the genetic nitrite and N2O reduction potential derived from the abundance of nirK, nirS and nosZ genes. These data were correlated with soil properties at two different points in time in 2013. N2O emissions were measured every 2 weeks over three vegetation periods (2012–2014). Very low N2O emission rates were measured throughout the entire period of investigation in accordance with the geostatistical data that revealed an abundance of microbes carrying the N2O reductase gene nosZ. This, along with neutral soil pH values, is indicative of high microbial denitrification potential. While the distribution of the microbial communities was strongly influenced by total organic carbon and nitrogen pools in March, the spatial distribution pattern was not related to the distribution of soil properties in October, when higher nutrient availability was observed. Different nitrite reducer groups prevailed in spring and autumn. While nirS, followed by nosZ and nirK, was most abundant in March, the latter was the dominant nitrite reductase in October.

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References

  1. Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell K, Johnson CA (2001) Climate change 2001: the scientific basis. Contribution of working group I to the third assessment report of the intergovernmental panel on Climate change. Cambridge University Press, United Kingdom and New York

    Google Scholar 

  2. Eggleston HS, Miwa K, Ngara T, Tanabe K (2006) 2006 IPCC guidelines for national greenhouse gas inventories, prepared by the National Greenhouse Gas Inventories Programme, IGES, Japan

  3. 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 3:403–407

    Article  Google Scholar 

  4. Enwall K, Throbäck IN, Stenberg M, Söderström M, Hallin S (2010) Soil resources influence spatial patterns of denitrifying communities at scales compatible with land management. Appl Environ Microbiol 76:2243–2250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Philippot L, Čuhel J, Saby NPA, Chèneby D, Chroňáková A, Bru D, Arrouays D, Martin-Laurent F, Šimek M (2009) Mapping field-scale spatial patterns of size and activity of the denitrifier community. Environ Microbiol 11:1518–1526

    Article  PubMed  Google Scholar 

  6. Jones CM, Stres B, Rosenquist M, Hallin S (2008) Phylogenetic analysis of nitrite, nitric oxide, and nitrous oxide respiratory enzymes reveal a complex evolutionary history for denitrification. Mol Biol Evol 25:1955–1966

    Article  CAS  PubMed  Google Scholar 

  7. Flessa H, Dörsch P, Beese F (1995) Seasonal variation of N2O and CH4 fluxes in differently managed arable soils in southern Germany. J Geophys Res-Atmos 100:23115–23124

    Article  CAS  Google Scholar 

  8. Töwe S, Wallisch S, Bannert A, Fischer D, Hai B, Haesler F, Kleineidam K, Schloter M (2011) Improved protocol for the simultaneous extraction and column-based separation of DNA and RNA from different soils. J Microbiol Methods 84:406–412

    Article  PubMed  Google Scholar 

  9. Töwe S, Albert A, Kleineidam K, Brankatschk R, Dümig A, Welzl G, Munch JC, Zeyer J, Schloter M (2010) Abundance of microbes involved in nitrogen transformation in the rhizosphere of Leucanthemopsis alpina (L.) Heywood grown in soils from different sites of the Damma glacier forefield. Microb Ecol 60:762–770

    Article  PubMed  Google Scholar 

  10. Team RC (2008) A language and environment for statistical computing. R foundation for statistical computing

  11. Pebesma EJ (2004) Multivariable geostatistics in S: the gstat package. Comput Geosci 30:683–691

    Article  Google Scholar 

  12. Steffens M, Koelbl A, Giese M, Hoffmann C, Totsche KU, Breuer L, Koegel-Knabner I (2009) Spatial variability of topsoils and vegetation in a grazed steppe ecosystem in Inner Mongolia (PR China). J Plant Nutr Soil Sci 172:78–90

    Article  CAS  Google Scholar 

  13. Stempfhuber B, Richter-Heitmann T, Regan KM, Kölbl A, Wüst PK, Marhan S, Sikorski J, Overmann J, Friedrich MW, Kandeler E, Schloter M (2015) Spatial interaction of archaeal ammonia-oxidizers and nitrite-oxidizing bacteria in an unfertilized grassland soil. Front Microbiol 6:1567

    PubMed  Google Scholar 

  14. Leppelt T, Dechow R, Gebbert S, Freibauer A, Lohila A, Augustin J, Drösler M, Fiedler S, Glatzel S, Höper H, Järveoja J, Lærke PE, Maljanen M, Mander Ü, Mäkiranta P, Minkkinen K, Ojanen P, Regina K, Strömgren M (2014) Nitrous oxide emission budgets and land-use-driven hotspots for organic soils in Europe. Biogeosciences 11:6595–6612

    Article  Google Scholar 

  15. García-Lledó A, Vilar-Sanz A, Trias R, Hallin S, Bañeras L (2011) Genetic potential for N2O emissions from the sediment of a free water surface constructed wetland. Water Res 45:5621–5632

    Article  PubMed  Google Scholar 

  16. Jungkunst HF, Fiedler S, Stahr K (2004) N2O emissions of a mature Norway spruce (Picea abies) stand in the Black Forest (southwest Germany) as differentiated by the soil pattern. J Geophys Res-Atmos 109:1–11

    Article  Google Scholar 

  17. Keil D, Meyer A, Berner D, Poll C, Schützenmeister A, Piepho H-P, Vlasenko A, Philippot L, Schloter M, Kandeler E, Marhan S (2011) Influence of land-use intensity on the spatial distribution of N-cycling microorganisms in grassland soils. FEMS Microbiol Ecol 77:95–106

    Article  CAS  PubMed  Google Scholar 

  18. Ligi T, Truu M, Truu J, Nõlvak H, Kaasik A, Mitsch WJ, Mander Ü (2014) Effects of soil chemical characteristics and water regime on denitrification genes (nirS, nirK, and nosZ) abundances in a created riverine wetland complex. Ecol Eng 72:47–55

    Article  Google Scholar 

  19. Chen Y, Wen Y, Zhou Q, Vymazal J (2014) Effects of plant biomass on denitrifying genes in subsurface-flow constructed wetlands. Bioresour Technol 157:341–345

    Article  CAS  PubMed  Google Scholar 

  20. Regan KM, Nunan N, Boeddinghaus RS, Baumgartner V, Berner D, Boch S, Oelmann Y, Overmann J, Prati D, Schloter M, Schmitt B, Sorkau E, Steffens M, Kandeler E, Marhan S (2014) Seasonal controls on grassland microbial biogeography: are they governed by plants, abiotic properties or both? Soil Biol Biochem 71:21–30

    Article  CAS  Google Scholar 

  21. Meyer A, Focks A, Radl V, Welzl G, Schöning I, Schloter M (2014) Influence of land use intensity on the diversity of ammonia oxidizing bacteria and archaea in soils from grassland ecosystems. Microb Ecol 67:161–166

    Article  CAS  PubMed  Google Scholar 

  22. Rasche F, Knapp D, Kaiser C, Koranda M, Kitzler B, Zechmeister-Boltenstern S, Richter A, Sessitsch A (2011) Seasonality and resource availability control bacterial and archaeal communities in soils of a temperate beech forest. ISME J 5:389–402

    Article  CAS  PubMed  Google Scholar 

  23. Heylen K, Gevers D, Vanparys B, Wittebolle L, Geets J, Boon N, Vos PD (2006) The incidence of nirS and nirK and their genetic heterogeneity in cultivated denitrifiers. Environ Microbiol 8:2012–2021

    Article  CAS  PubMed  Google Scholar 

  24. Smith JM, Ogram A (2008) Genetic and functional variation in denitrifier populations along a short-term restoration chronosequence. Appl Environ Microbiol 74:5615–5620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Töwe S, Albert A, Kleineidam K, Brankatschk R, Dümig A, Welzl G, Munch J, Zeyer J, Schloter M (2010) Abundance of microbes involved in nitrogen transformation in the rhizosphere of Leucanthemopsis alpina (L.) Heywood grown in soils from different sites of the Damma glacier forefield. Microb Ecol 60:762–770

    Article  PubMed  Google Scholar 

  26. Sharma S, Aneja MK, Mayer J, Munch JC, Schloter M (2005) Diversity of transcripts of nitrite reductase genes (nirK and nirS) in rhizospheres of grain legumes. Appl Environ Microbiol 71:2001–2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Philippot L, Andert J, Jones CM, Bru D, Hallin S (2011) Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil. Glob Chang Biol 17:1497–1504

    Article  Google Scholar 

  28. Michotey V, Mejean V, Bonin P (2000) Comparison of Methods for Quantification of Cytochrome cd1-Denitrifying Bacteria in Environmental Marine Samples. Appl Environ Microbiol 66(4):1564–1571

  29. Throback IN, Enwall K, Jarvis A, Hallin S (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol Ecol 49:401–417

  30. 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 64:3769–3775

  31. Henry S, Baudoin E, López-Gutiérrez JC, Martin-Laurent F, Brauman A, Philippot L (2004) Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J Microbiol Methods 59(3):327–335

  32. Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative Detection of the nosZ Gene, Encoding Nitrous Oxide Reductase, and Comparison of the Abundances of 16S rRNA, narG, nirK, and nosZ Genes in Soils. Appl Environ Microbiol 72(8):5181–5189

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Acknowledgements

We would like to thank Elvira Schulz, Enja Braun, Sylvia Bondzio, Gudrun Hufnagel and Cornelia Galonska for the technical assistance in measuring soil chemical parameters and performing molecular analyses. The study (BWM 11001) was funded by the Baden-Württemberg Ministry of the Environment, Climate Protection and the Energy Sector.

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Authors and Affiliations

  1. Research Unit Comparative Microbiome Analysis, Helmholtz Zentrum München, Ingolstädter Landstr. 1, 85764, Neuherberg, Germany

    Stefanie Schulz & Michael Schloter

  2. Department of Ecology and Ecosystem Management, Technical University of Munich, Emil-Ramann-Straße 2, 85354, Freising, Germany

    Angelika Kölbl

  3. Institute for Geography, Soil Science, Johannes Gutenberg-University Mainz, Johann-Joachim-Becher-Weg 21, 55099, Mainz, Germany

    Martin Ebli & Sabine Fiedler

  4. Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, Ingolstädter Landstr. 1, 85764, Neuherberg, Germany

    Franz Buegger

Authors
  1. Stefanie Schulz
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  2. Angelika Kölbl
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  3. Martin Ebli
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  4. Franz Buegger
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  5. Michael Schloter
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  6. Sabine Fiedler
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Correspondence to Sabine Fiedler.

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Schulz, S., Kölbl, A., Ebli, M. et al. Field-Scale Pattern of Denitrifying Microorganisms and N2O Emission Rates Indicate a High Potential for Complete Denitrification in an Agriculturally Used Organic Soil. Microb Ecol 74, 765–770 (2017). https://doi.org/10.1007/s00248-017-0991-1

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