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Biogeochemistry

, Volume 101, Issue 1–3, pp 123–132 | Cite as

Effect of pH and dissolved organic matter on the abundance of nirK and nirS denitrifiers in spruce forest soil

  • Jiří Bárta
  • Tereza Melichová
  • Daniel Vaněk
  • Tomáš Picek
  • Hana Šantrůčková
Article

Abstract

Acid N depositions in the Bohemian Forest during the second half of the last century caused enormous soil acidification which led to the leaching of essential nutrients including nitrates. We investigated the effect of dissolved organic matter (DOM) and pH on the abundance of 16S RDNA, nirK and nirS gene copies in four spruce forest sites. Soil samples for molecular based quantification (qPCR) were taken from the organic litter and humus layers. The amounts of dissolved organic carbon (DOC) and dissolved nitrogen (DN) were much lower in highly acidified soils. We found a strong correlation between nirK denitrifiers and the amount of available P (r = 0.83, p < 0.001), which suggested a higher nutrient sensitivity of this group of denitrifying bacteria. Additionally, we found that correlations between the amount of nirK denitrifiers and DOC and pH are exponentional showing two important threshold values, being 4.8 mol kg−1 and 5, respectively. The amount of nirK denitrifiers rapidly decreased below these values. The amount of nirK and nirS denitrifiers was higher in the organic litter horizon than the organic humus horizon at all sampling sites.

Keywords

Dissolved organic matter Available phosphorus nirK and nirS denitrifiers Acid forest soil N depositions qPCR 

Notes

Acknowledgements

This study was supported by the Czech Science Foundation, project 526/08/0751 and 206/07/1200 and the project MSM 6007665801. We acknowledge the laboratory and field assistance provided by our colleagues and students. We also thank the authorities of NP Šumava and The Jizera Mountains for permission to study the spruce forest ecosystems. We thank our American colleague Dr. Keith Edwards for language correction.

References

  1. Bárta J, Applová M, Vaněk D, Krištůfková M, Šantrůčková H (2010) Effect of available P and phenolics on mineral N release in acidified spruce forest: connection with lignin-degrading enzymes and bacterial and fungal communities. Biogeochemistry 97:71–87CrossRefGoogle Scholar
  2. Cabrita MT, Brotas V (2000) Seasonal variation in denitrification and dissolved nitrogen fluxes in intertidal sediments of the Tagus estuary, Portugal. Mar Ecol 202:51–65CrossRefGoogle Scholar
  3. Cappo KA, Blume LJ, Raab GA, Bartz JK, Engels JL (1987) Analytical methods manual for the direct/delayed response project soil survey. US EPA, Las Vegas (sections 8–11)Google Scholar
  4. Chéneby D, Philippot L, Hartmann A, Hénault F, Germon JC (2000) 16S rRNA analysis for characterization of denitrifying bacteria isolated from three agricultural soils. FEMS Microbiol Ecol 34:121–128Google Scholar
  5. Clément JC, Pinay G, Marmonier P (2002) Seasonal dynamics of denitrification along topohydrosequences in three different riparian wetlands. J Environ Qual 31:1025–1037CrossRefGoogle Scholar
  6. Dauer JM, Chorover J, Chadwick OA, Oleksyn J, Tjoelker MG, Hobbie SE, Reich PB, Eissen-stat DM (2007) Controls over leaf and litter calcium concentrations among temperate trees. Biogeochemistry 86:175–187CrossRefGoogle Scholar
  7. David MB, Vance GF, Rissing JM, Stevenson FJ (1989) Organic carbon fractions in extracts of O and B horizons from a New England spodsols: effect of acid treatment. J Environ Qual 18:212–217CrossRefGoogle Scholar
  8. Fogel GB, Collins CR, Li J, Brunk CF (1999) Prokaryotic genome size and SSU rDNA copy number: estimation of microbial relative abundance from a mixed population. Microb Ecol 38:93–113CrossRefGoogle Scholar
  9. Galloway JN, Cowling EB (2002) Reactive nitrogen and the world: 200 years of change. Ambio 31:64–71Google Scholar
  10. Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby BJ (2003) The nitrogen cascade. Bioscience 53:341–356CrossRefGoogle Scholar
  11. Greenland DJ (1971) Adsorption of humic and fulvic acids by soils. Soil Sci 111:34–43CrossRefGoogle Scholar
  12. Henry S, Baudion E, López-Guitérez 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 59:327–335CrossRefGoogle Scholar
  13. 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 72:5181–5189CrossRefGoogle Scholar
  14. Heylen K, Gevers D, Vanparys B, Wittebolle L, Geets J, Boon N, De Vos P (2006) The incidence of nirS and nirK and their genetic heterogeneity in cultivated denitrifiers. Environ Microbiol 8:2012–2021CrossRefGoogle Scholar
  15. Kaňa J, Kopáček J (2006) Impact of soil sorption characteristics and bedrock composition on phosphorus concentrations in two Bohemian Forest Lakes. Water Air Soil Pollut 173:243–259CrossRefGoogle Scholar
  16. Kandeler E, Deighlmayr K, Tscherko D, Bru D, Philippot L (2006) Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Appl Environ Microbiol 72:5957–5962CrossRefGoogle Scholar
  17. Koopmans GF, Chardon WJ, de Willigen P, van Riemsdijk WH (2004) Phosphorus desorption dynamics in soil and the link to a dynamic concept of bioavailability. J Environ Qual 33:1393–1402CrossRefGoogle Scholar
  18. Kopáček J, Kaňa J, Šantrůčková H, Porcal P, Hejzlar J, Picek T, Veselý J (2002a) Physical, chemical, and biochemical characteristics of soils in watersheds of the Bohemian Forest Lakes: I. Plešné Lake. Silva Gabreta 8:43–62Google Scholar
  19. Kopáček J, Kaňa J, Šantrůčková H, Porcal P, Hejzlar J, Picek T, Šimek M, Veselý J (2002b) Physical, chemical, and biochemical characteristics of soils in watersheds of the Bohemian Forest Lakes: II.Čertovo and Černé Lakes. Silva Gabreta 8:63–93Google Scholar
  20. Livsey S, Barklund P (1992) Lophodermium piceae and Rhizosphaera kalkhoffii in fallen needles of Norway spruce (Picea abies). Eur J For Pathol 22:204–216CrossRefGoogle Scholar
  21. López-Gutiérrez J, Henry S, Hallet S, Martin-Laurent F, Catroux G, Philippot L (2004) Quantification of a novel group of nitrate-reducing bacteria in the environment by real-time PCR. J Microbiol Methods 57:399–407CrossRefGoogle Scholar
  22. Magill AH, Aber JD, Hendricks JJ, Bowden RD, Melillo JM, Steudler PA (1997) Biogeochemical response of forest ecosystems to simulated chronic nitrogen deposition. Ecol Appl 7:402–415CrossRefGoogle Scholar
  23. Nadelhoffer KJ, Emmett BA, Gundersen P, Kjonaas OJ, Koopmans CJ, Schleppi P, Tietema A (1999) Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398:145–148CrossRefGoogle Scholar
  24. Northup RR, Dahlgren RA, McColl JG (1998) Polyphenols as regulators of plant-litter-soil interactions in northern Californias pygmy forest: a positive feedback? Biogeochemistry 42:189–220CrossRefGoogle Scholar
  25. Pawłowski L (1997) Acidification: its impact on the environment and mitigation strategies. Ecol Eng 8:271–288CrossRefGoogle Scholar
  26. Pote DH, Daniel TC, Sharpley AN, Moore PA, Edwards DR, Nichols DJ (1996) Relating extractable soil phosphorus to phosphorus losses in runoff. Soil Sci Am J 60:855–859CrossRefGoogle Scholar
  27. Quails RG, Raines BL (1992) Biodegradability of dissolved organic matter in forest throughfall, soil solution, and stream water. Soil Sci Soc Am J 56:578–586CrossRefGoogle Scholar
  28. Rösch C, Mergel A, Bothe H (2002) Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Appl Environ Microbiol 68:3818–3829CrossRefGoogle Scholar
  29. Saleh-Lakha S, Shannon KE, Henderson SL, Goyer C, Trevors JT, Zebarth BJ, Buton DL (2009) Effect of pH and temperature on denitrification gene expression and activity in Pseudomonas mandelii. Appl Environ Microbiol 75:3903–3911CrossRefGoogle Scholar
  30. Šantrůčková H, Vrba J, Picek T, Kopáček J (2004) Soil biochemical activity and phosphorus transformations and losses from acidified forest soils. Soil Biol Biochem 36:1569–1576CrossRefGoogle Scholar
  31. Šantrůčková H, Krištůfková M, Vaněk D (2006) Decomposition rate and nutrient release from plant litter of Norway spruce forest in the Bohemian Forest. Biologia (Bratisl) 61:S499–S508CrossRefGoogle Scholar
  32. Šantrůčková H, Šantrůček J, Setlik J, Svoboda M, Kopacek J (2007) Carbon isotopes in tree rings of Norway spruce exposed to atmospheric pollution. Environ Sci Technol 41:5778–5782CrossRefGoogle Scholar
  33. Schindler DW, Bayley SE, Curtis PJ, Parker BR, Stainton MP, Kelly CA (1992) Natural and man-caused factors affecting the abundance and cycling of dissolved organic substances in Precambrian shield lakes. Hydrobiology 229:1–21Google Scholar
  34. Schwertmann U (1964) Differenzierung der eisenoxiden des bodens duerch extraction mit amoniumoxalaat lösung. Z Pflanzenerähr Düng Bodenkd 105:194–202CrossRefGoogle Scholar
  35. Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24CrossRefGoogle Scholar
  36. Sinsabaugh RL, Gallo ME, Lauber C, Waldrop MP, Zak DR (2005) Extracellular enzyme activities and soil organic matter dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry 75:201–215CrossRefGoogle Scholar
  37. Snajdr J, Valaskova V, Merhautova V, Herinkova J, Cajthaml T, Baldrian P (2008) Spatial variability of enzyme activities and microbial biomass in the upper layers of Quercus petraea forest soil. Soil Biol Biochem 40:2068–2075CrossRefGoogle Scholar
  38. Svoboda M, Matějka K, Kopáček J (2006) Biomass and element pools of understory vegetation in the catchments of Čertovo Lake and Plešné Lake in the Bohemian Forest. Biologia (Bratisl) 61:S509–S521CrossRefGoogle Scholar
  39. Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder A (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 179–244Google Scholar
  40. Tomlinson GH (2003) Acid deposition, nutrient leaching and forest growth. Biogeochemistry 65:51–81CrossRefGoogle Scholar
  41. van der Zee SEATM, Fokkink LGJ, van Riemsdijk WH (1987) A new technique for assessment of reversibly adsorbed phosphate. Soil Sci Am J 51:599–604CrossRefGoogle Scholar
  42. van Kessel C, Pennock DJ, Farrell RE (1993) Seasonal variations in denitrification and nitrous oxide evolution at the landscape scale. Soil Sci Soc Am J 57:988–995CrossRefGoogle Scholar
  43. Veselý J (1994) Investigation of the nature of the Šumava lakes: a review. J Natl Mus Nat Hist Ser 163:103–120Google Scholar
  44. Waldrop MP, Zak DR (2006) Response of oxidative enzyme activities to nitrogen deposition affects soil concentrations of dissolved organic carbon. Ecosystems 9:921–933CrossRefGoogle Scholar
  45. Wertz S, Dandie CE, Goyer C, Trevors JT, Pattern CL (2009) Diversity of nirK denitrifying genes and transcripts in an agricultural soil. Appl Environ Microbiol 75:7365–7377CrossRefGoogle Scholar
  46. Winder RS, Levy-Booth DJ (2009) Quantification of nitrogen cycling functional gene abundance in soil of variably-retained stands of Douglas-fir (Pseudotsuga menziesii ssp. menziesii (Mirb.) Franco). Working papers of the Finnish Forest Research Institute 128:225Google Scholar
  47. Yaganza ES, Rioux D, Simard M, Arul Jl, Tweddell RJ (2004) Ultrastructural alterations of Erwinia carotovora subsp. atroseptica caused by treatment with aluminum chloride and sodium metabisulfite. Appl Environ Microbiol 70:6800–6808CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Jiří Bárta
    • 1
  • Tereza Melichová
    • 1
  • Daniel Vaněk
    • 1
  • Tomáš Picek
    • 1
  • Hana Šantrůčková
    • 1
  1. 1.Department of Ecosystem Biology, Faculty of ScienceUniversity of South BohemiaCeske BudejoviceCzech Republic

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