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Ecosystems

, Volume 19, Issue 2, pp 284–295 | Cite as

Gross Nitrogen Dynamics in the Mycorrhizosphere of an Organic Forest Soil

  • M. Holz
  • M. Aurangojeb
  • Å. Kasimir
  • P. Boeckx
  • Y. Kuzyakov
  • L. Klemedtsson
  • T. RüttingEmail author
Article

Abstract

The rhizosphere is a hot-spot for biogeochemical cycles, including production of greenhouse gases, as microbial activity is stimulated by rhizodeposits released by roots and mycorrhizae. The biogeochemical cycle of nitrogen (N) in soil is complex, consisting of many simultaneously occurring processes. In situ studies investigating the effects of roots and mycorrhizae on gross N turnover rates are scarce. We conducted a 15N tracer study under field conditions in a spruce forest on organic soil, which was subjected to exclusion of roots and roots plus ectomycorrhizae (ECM) for 6 years by trenching. The forest soil had, over the 6-year period, an average emission of nitrous oxide (N2O) of 5.9 ± 2.1 kg N2O ha−1 year−1. Exclusion of roots + ECM nearly tripled N2O emissions over all years, whereas root exclusion stimulated N2O emission only in the latest years and to a smaller extent. Gross mineralization–ammonium (NH4 +) immobilization turnover was enhanced by the presence of roots, probably due to high inputs of labile carbon, stimulating microbial activity. We found contrasting effects of roots and ECM on N2O emission and mineralization, as the former was decreased but the latter was stimulated by roots and ECM. The N2O emission was positively related to the ratio of gross NH4 + oxidation (that is, autotrophic nitrification) to NH4 + immobilization. Ammonium oxidation was only stimulated by the presence of ECM, but not by the presence of roots. Overall, we conclude that plants and their mycorrhizal symbionts actively control soil N cycling, thereby also affecting N2O emissions from forest soils. Consequently, adapted forest management with permanent tree cover avoiding clearcutting could be a means to reduce N2O emissions and potential N leaching; despite higher mineralization in the presence of roots and ECM, N2O emissions are decreased as the relative importance of NH4 + oxidation is decreased, mainly due to a stimulated microbial NH4 + immobilization in the mycorrhizosphere.

Keywords

histosol mineralization–immobilization turnover nitrification nitrous oxide emissions Norway spruce 15N tracer 

Notes

Acknowledgment

We would like to thank Sami Namasse and Camille Ziegler for assisting in the 15N work, Katja Van Nieuland for assisting in the laboratory work and David Allbrand for N2O flux measurements. This study was funded by the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) with additional support by the Swedish strategic research area “Biodiversity and Ecosystem services in a Changing Climate – BECC” (www.cec.lu.se/research/becc).

Supplementary material

10021_2015_9931_MOESM1_ESM.pdf (493 kb)
Supplementary material 1 (PDF 492 kb)

References

  1. Ambus P. 2005. Relationship between gross nitrogen cycling and nitrous oxide emission in grass-clover pasture. Nutr Cycl Agroecosyst 72:189–99.CrossRefGoogle Scholar
  2. Badr O, Probert S. 1993. Environmental impacts of atmospheric nitrous oxide. Appl Energy 44:197–231.CrossRefGoogle Scholar
  3. Björk RG, Ernfors M, Sikstrom U, Nilsson MB, Andersson MX, Rütting T, Klemedtsson L. 2010. Contrasting effects of wood ash application on microbial community structure, biomass and processes in drained forested peatlands. FEMS Microbiol Ecol 73:550–62.PubMedGoogle Scholar
  4. Booth MS, Stark JM, Rastetter E. 2005. Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol Monogr 75:139–57.CrossRefGoogle Scholar
  5. Burger M, Jackson LE. 2004. Plant and microbial nitrogen use and turnover: rapid conversion of nitrate to ammonium in soil with roots. Plant Soil 266:289–301.CrossRefGoogle Scholar
  6. Canary J, Harrison R, Compton J, Chappell H. 2000. Additional carbon sequestration following repeated urea fertilization of second-growth Douglas-fir stands in western Washington. For Ecol Manag 138:225–32.CrossRefGoogle Scholar
  7. Chapman SK, Langley JA, Hart SC, Koch GW. 2006. Plants actively control nitrogen cycling: uncorking the microbial bottleneck. New Phytol 169:27–34.CrossRefPubMedGoogle Scholar
  8. Davidson EA, Hart SC, Shanks CA, Firestone MK. 1991. Measuring gross nitrogen mineralization, immobilization, and nitrification by 15N isotopic pool dilution in intact soil cores. J Soil Sci 42:335–49.CrossRefGoogle Scholar
  9. Dijkstra F, Bader NE, Johnson DW, Cheng W. 2009. Does accelerated soil organic matter decomposition in the presence of plants increase plant N availability? Soil Biol Biochem 41:1080–7.CrossRefGoogle Scholar
  10. Ehrenfeld JG, Parsons WFJ, Han X, Parmelee RW, Zhu W. 1997. Live and dead roots in forest soil horizons: contrasting effects on nitrogen dynamics. Ecology 78:348–62.Google Scholar
  11. Ernfors M, Rütting T, Klemedtsson L. 2011. Increased nitrous oxide emissions from a drained organic forest soil after exclusion of ectomycorrhizal mycelia. Plant Soil 343:161–70.CrossRefGoogle Scholar
  12. Fisher FM, Gosz JR. 1986. Effects of trenching on soil processes and properties in a New Mexico mixed-conifer forest. Biol Fertil Soils 2:35–42.CrossRefGoogle Scholar
  13. Frank DA, Groffman PM. 2009. Plant rhizospheric N processes: what we don’t know and why we should care. Ecology 90:1512–19.CrossRefPubMedGoogle Scholar
  14. Gavrichkova O, Kuzyakov Y. 2010. Respiration costs associated with nitrate reduction as estimated by 14CO2 pulse labeling of corn at various growth stages. Plant Soil 329:433–45.CrossRefGoogle Scholar
  15. Gessler A, Schneider S, Von Sengbusch D, Weber P, Hanemann U, Huber C, Rothe A, Kreutzer K, Rennberg H. 1998. Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytol 138:275–85.CrossRefGoogle Scholar
  16. 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 32:120–8.CrossRefGoogle Scholar
  17. Hamilton EW, Frank DA. 2001. Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:2397–402.CrossRefGoogle Scholar
  18. Hart SC, Nason GE, Myrold DD, Perry DA. 1994. Dynamics of gross nitrogen transformations in an old-growth forest: the carbon connection. Ecology 75:880–91.CrossRefGoogle Scholar
  19. Hart SC, Binkley D, Perry DA. 1997. Influence of red alder on soil nitrogen transformations in two conifer forests of contrasting productivity. Soil Biol Biochem 29:1111–23.CrossRefGoogle Scholar
  20. Herman DJ, Johnson KK, Jaeger CH, Schwartz E, Firestone MK. 2006. Root influence on nitrogen mineralization and nitrification in rhizosphere soil. Soil Sci Soc Am J 70:1504–11.CrossRefGoogle Scholar
  21. Hodge A, Campbell CD, Fitter AH. 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–9.CrossRefPubMedGoogle Scholar
  22. Holub SM, Lajtha K, Spears JDH, Tóth JA, Crow SE, Caldwell BA, Papp M, Nagy PT. 2005. Organic matter manipulations have little effect on gross and net nitrogen transformations in two temperate forest mineral soils in the USA and central Europe. For Ecol Manag 214:320–30.CrossRefGoogle Scholar
  23. Jackson LE, Burger M, Cavagnaro TR. 2008. Roots, nitrogen transformations and ecosystem services. Annu Rev Plant Biol 59:341–63.CrossRefPubMedGoogle Scholar
  24. Kaiser C, Fuchslueger L, Koranda M, Gorfer M, Stange CF, Kitzler B, Rasche F, Strauss J, Sessitsch A, Zeichmeister-Boltenstern S, Richter A. 2011. Plants control the seasonal dynamics of microbial N cycling in a beech forest soil by belowground C allocation. Ecology 92:1036–51.CrossRefPubMedGoogle Scholar
  25. Koranda M, Schnecker J, Kaiser C, Fuchslueger L, Kitzler B, Stange CF, Sessitsch A, Zechmeister-Boltenstern S, Richter A. 2011. Microbial processes and community composition in the rhizosphere of European beech—the influence of plant C exudates. Soil Biol Biochem 43:551–8.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kuzyakov Y. 2010. Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–71.CrossRefGoogle Scholar
  27. Kuzyakov Y, Xu X. 2013. Competition between roots and microorganisms for N: mechanisms and ecological relevance. New Phytol 198:656–69.CrossRefPubMedGoogle Scholar
  28. Landi L, Valori F, Ascher J, Renella G, Falchini L, Nannipieri P. 2006. Root exudate effects on the bacterial communities, CO2 evolution, nitrogen transformations and ATP content of rhizosphere and bulk soils. Soil Biol Biochem 38:509–16.CrossRefGoogle Scholar
  29. Laughlin RJ, Stevens RJ, Zhuo S. 1997. Determining nitrogen-15 in ammonium by producing nitrous oxide. Soil Sci Soc Am J 61:462–5.CrossRefGoogle Scholar
  30. LeBauer DS, Treseder KK. 2008. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–9.CrossRefPubMedGoogle Scholar
  31. Lorenz K, Preston CM, Raspe S, Morrison IK, Feger KH. 2000. Litter decomposition and humus characteristics in Canadian and German spruce ecosystems: information from tannin analysis and 13C CPMAS NMR. Soil Biol Biochem 32:779–92.CrossRefGoogle Scholar
  32. Mary B, Recous S, Darwis D, Robin D. 1996. Interactions between decomposition of plant residues and nitrogen cycling in soil. Plant Soil 181:71–82.CrossRefGoogle Scholar
  33. Matson PA, Vitousek PM. 1987. Cross-system comparisons of soil nitrogen transformations and nitrous oxide flux in tropical forest ecosystems. Global Biogeochem Cycles 1:163–70.CrossRefGoogle Scholar
  34. Meyer A, Tarvainen L, Nousratpour A, Björk RG, Ernfors M, Grelle A, Kasimir Klemedtsson Å, Lindroth A, Räntfors M, Rütting T, Wallin G, Weslien P, Klemedtsson L. 2013. A fertile peatland forest does not constitute a major greenhouse gas sink. Biogeosciences 10:7739–58.CrossRefGoogle Scholar
  35. Müller C, Stevens RJ, Laughlin RJ. 2004. A 15N tracing model to analyse N transformations in old grassland soil. Soil Biol Biochem 36:619–32.CrossRefGoogle Scholar
  36. Müller C, Rütting T, Kattge J, Laughlin RJ, Stevens RJ. 2007. Estimation of parameters in complex 15N tracing models by Monte Carlo sampling. Soil Biol Biochem 39:715–26.CrossRefGoogle Scholar
  37. Münchmeyer U. 2001. Zur N-Umsetzung in degradierten Niedermoorböden Nordostdeutschlands unter besonderer Berücksichtigung der N-Mineralisierung und des Austrages gasförmiger N-Verbindungen. Beiträge aus der Hallenser Pflanzenernährungsforschung, vol. 5. Stuttgart: BG Teubner, pp 1–125.Google Scholar
  38. Myrold DD, Tiedje JM. 1986. Simultaneous estimation of several nitrogen cycle rates using 15N: theory and application. Soil Biol Biochem 18:559–68.CrossRefGoogle Scholar
  39. Nason GE, Myrold DD. 1991. 15N in soil research: appropriate application of rate estimation procedures. Agric Ecosyst Environ 34:427–41.CrossRefGoogle Scholar
  40. Norton JM, Firestone MK. 1996. N dynamics in the rhizosphere of Pinus ponderosa seedlings. Soil Biol Biochem 28:351–62.CrossRefGoogle Scholar
  41. Paavolainen L, Kitunen V, Smolander A. 1998. Inhibition of nitrification in forest soil by monoterpenes. Plant Soil 205:147–54.CrossRefGoogle Scholar
  42. Pausch J, Zhu B, Kuzyakov Y, Cheng W. 2013. Plant inter-specific effects on rhizosphere priming of soil organic matter decomposition. Soil Biol Biochem 57:91–9.CrossRefGoogle Scholar
  43. Payton ME, Miller AE, Raun WR. 2000. Testing statistical hypotheses using standard error bars and confidence intervals. Commun Soil Sci Plant Anal 31:547–51.CrossRefGoogle Scholar
  44. Philippot L, Hallin S, Börjesson G, Baggs EM. 2008. Biochemical cycling in the rhizosphere having an impact on global change. Plant Soil 321:61–81.CrossRefGoogle Scholar
  45. Phillips RP, Fahey TJ. 2006. Tree species and mycorrhizal associations influence the magnitude of rhizosphere effects. Can J For Res 5:1302–13.Google Scholar
  46. Qian JH, Doran JW, Walters DT. 1997. Maize plant contributions to root zone available carbon and microbial transformations of nitrogen. Soil Biol Biochem 29:1451–62.CrossRefGoogle Scholar
  47. Ravishankara AR, Daniel JS, Portmann RW. 2009. Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–5.CrossRefPubMedGoogle Scholar
  48. Ross DJ, Scott NA, Tate KR, Rodda NJ, Townsend JA. 2001. Root effects on soil carbon and nitrogen cycling in a Pinus radiata D. Don plantation on a coastal sand. Aust J Soil Res 39:1027–39.CrossRefGoogle Scholar
  49. Rütting T, Müller C. 2007. 15N tracing models with a Monte Carlo optimization procedure provide new insights on gross N transformations in soils. Soil Biol Biochem 39:2351–61.CrossRefGoogle Scholar
  50. Rütting T, Huygens D, Müller C, van Cleemput O, Godoy R, Boeckx P. 2008. Functional role of DNRA and nitrite reduction in a pristine south Chilean Nothofagus forest. Biogeochemistry 90:243–58.CrossRefGoogle Scholar
  51. Rütting T, Clough TJ, Müller C, Lieffering M, Newton PCD. 2010. Ten years of elevated atmospheric CO2 alters soil N transformations in a sheep-grazed pasture. Glob Change Biol 16:2530–42.CrossRefGoogle Scholar
  52. Rütting T, Huygens D, Staelens J, Müller C, Boeckx P. 2011. Advances in 15N-tracing experiments: new labelling and data analysis approaches. Biochem Soc Trans 39:279–83.CrossRefPubMedGoogle Scholar
  53. Schimel JP, Bennett J. 2004. Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602.CrossRefGoogle Scholar
  54. Silver WL, Herman DJ, Firestone MK. 2001. Dissimilatory nitrate reduction to ammonium in upland tropical forest soils. Ecology 82:2410–16.CrossRefGoogle Scholar
  55. Staelens J, Rütting T, Huygens D, Schrijver A, Müller C, Verheyen K, Boeckx P. 2012. In situ gross nitrogen transformations differ between temperate deciduous and coniferous forest soils. Biogeochemistry 108:259–77.CrossRefGoogle Scholar
  56. Stevens RJ, Laughlin RJ. 1994. Determining nitrogen-nitrite or nitrate by producing nitrous oxide. Soil Sci Soc Am J 58:1108–16.CrossRefGoogle Scholar
  57. Stockdale EA, Hatch DJ, Murphy DV, Ledgard SF, Watson CJ. 2002. Original article verifying the nitrification to immobilisation ratio N/I. as a key determinant of potential nitrate loss in grassland and arable soils. Agronomie 22:831–8.CrossRefGoogle Scholar
  58. Sutton MA, Howard CM, Erisman JW, Billen G, Bleeker A, Grennfelt P, van Grinsven H, Grizzett B. 2011. The European nitrogen assessment: sources, effects, and policy perspectives. Edinburgh: Cambridge University Press.CrossRefGoogle Scholar
  59. Templer PH, Silver WL, Pett-Ridge J, DeAngelis KM, Firestone MK. 2008. Plant and microbial controls on nitrogen retention and loss in a humid tropical forest. Ecology 89:3030–40.CrossRefGoogle Scholar
  60. Tiedje JM. 1988. Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB, Ed. Biology of Anaerobic Microorganisms. New York: Wiley. p 179–244.Google Scholar
  61. Tietema A, Wessel WW. 1992. Gross nitrogen transformation in the organic layer of acid forest ecosystems subjected to increased atmospheric nitrogen input. Soil Biol Biochem 24:943–50.CrossRefGoogle Scholar
  62. Vitousek PM, Howarth RW. 1991. Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115.CrossRefGoogle Scholar
  63. Westbrook C, Devito K. 2004. Gross nitrogen transformations in soils from uncut and cut boreal upland and peatland coniferous forest stands. Biogeochemistry 68:33–50.CrossRefGoogle Scholar
  64. White CS. 1986. Volatile and water-soluble inhibitors of nitrogen mineralization and nitrification in a ponderosa pine ecosystem. Biol Fertil Soils 2:97–104.Google Scholar
  65. Willison TW, Baker JC, Murphy DV. 1998. Methane fluxes and nitrogen dynamics from a drained fenland peat. Biol Fertil Soils 27:279–83.CrossRefGoogle Scholar
  66. Wu T. 2011. Can ectomycorrhizal fungi circumvent the nitrogen mineralization for plant nutrition in temperate forest ecosystems? Soil Biol Biochem 43:1109–17.CrossRefGoogle Scholar
  67. Zeller B, Liu J, Buchmann N, Richter A. 2008. Tree girdling increases soil N mineralisation in two spruce stands. Soil Biol Biochem 40:1155–66.CrossRefGoogle Scholar
  68. Zhu T, Zhang J, Cai Z. 2011. The contribution of nitrogen transformation processes to total N2O emissions from soils used for intensive vegetable cultivation. Plant Soil 343:313–27.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • M. Holz
    • 1
  • M. Aurangojeb
    • 2
  • Å. Kasimir
    • 2
  • P. Boeckx
    • 3
  • Y. Kuzyakov
    • 1
  • L. Klemedtsson
    • 2
  • T. Rütting
    • 2
    Email author
  1. 1.Department of Soil Science of Temperate Ecosystems and Department of Agricultural Soil ScienceUniversity of GöttingenGöttingenGermany
  2. 2.Department of Earth SciencesUniversity of GothenburgGothenburgSweden
  3. 3.Isotope Bioscience Laboratory - ISOFYSGhent UniversityGhentBelgium

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