, Volume 97, Issue 2–3, pp 183–194 | Cite as

Depleted 15N in hydrolysable-N of arctic soils and its implication for mycorrhizal fungi–plant interaction

  • Y. YanoEmail author
  • G. R. Shaver
  • A. E. Giblin
  • E. B. Rastetter


Uptake of nitrogen (N) via root-mycorrhizal associations accounts for a significant portion of total N supply to many vascular plants. Using stable isotope ratios (δ15N) and the mass balance among N pools of plants, fungal tissues, and soils, a number of efforts have been made in recent years to quantify the flux of N from mycorrhizal fungi to host plants. Current estimates of this flux for arctic tundra ecosystems rely on the untested assumption that the δ15N of labile organic N taken up by the fungi is approximately the same as the δ15N of bulk soil. We report here hydrolysable amino acids are more depleted in 15N relative to hydrolysable ammonium and amino sugars in arctic tundra soils near Toolik Lake, Alaska, USA. We demonstrate, using a case study, that recognizing the depletion in 15N for hydrolysable amino acids (δ15N = −5.6‰ on average) would alter recent estimates of N flux between mycorrhizal fungi and host plants in an arctic tundra ecosystem.


15Arctic tundra Decomposition Hydrolysable amino acids Mycorrhizal fungi Nitrogen transfer Plant–fungal interaction 





Hydrolysable amino acids


Hydrolysable amino sugars


Hydrolizable ammonium








Total dissolved N



We are grateful to Erik Hobbie and John Hobbie for their insightful comments on the manuscript; Marshall Otter for isotope analyses; Christie Haupert, Jim Laundre, and Carrie McCalley for their field and laboratory assistance. We acknowledge Northland College for the use of facility. This study was funded by NSF-DEB-0423385and NSF-DEB 0444592. Additional support was provided by Arctic Long Term Ecological Research program, funded by National Science Foundation, Division of Environmental Biology.


  1. Abuzinadah RA, Read DJ (1986a) The role of proteins in the nitrogen nutrition of ectomycorrhizal plants—I. Utilization of peptides and proteins by ectomycorrhizal fungi. New Phytol 103:481–493CrossRefGoogle Scholar
  2. Abuzinadah RA, Read DJ (1986b) The role of proteins in the nitrogen nutrition of ectomycorrhizal plants—III. Protein utilization by Betula, Picea and Pinus in mycorrhizal association with Hebeloma crustuliniforme. New Phytol 103:507–514CrossRefGoogle Scholar
  3. Bol R, Ostle NJ, Petzke KJ, Chenu CC, Balesdent J (2008) Amino acid 15N in long-term bare fallow soils: influence of annual N fertilizer and manure applications. Euro J Soil Sci 59:617–629CrossRefGoogle Scholar
  4. Cabrera ML, Beare MH (1993) Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci Soc Am J 57:1007–1012Google Scholar
  5. Chalot M, Blaudez D, Brun A (2006) Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. Trends Plant Sci 11:263–266CrossRefGoogle Scholar
  6. Chapin FS III, Fetcher N, Kielland K et al (1988) Productivity and nutrient cycling of Alaskan tundra: enhancement by flowing soil water. Ecology 69:693–702CrossRefGoogle Scholar
  7. Chapin FS III, Shaver GR, Giblin AE et al (1995) Response of arctic tundra to experimental and observed changes in climate. Ecology 76:694–711CrossRefGoogle Scholar
  8. Clemmensen KE, Michelsen A (2006) Integrated long-term responses of an arctic-alpine willow and associated ectomycorrhizal fungi to an altered environment. Can J Bot 84:831–843CrossRefGoogle Scholar
  9. Clemmensen KE, Michelsen A, Jonasson S et al (2006) Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phytol 171:391–404CrossRefGoogle Scholar
  10. Clemmensen KE, Sorensen PL, Michelsen A et al (2008) Site-dependent N uptake from N-form mixtures by arctic plants, soil microbes and ectomycorrhizal fungi. Oecologia 155:771–783CrossRefGoogle Scholar
  11. Dijkstra P, Ishizu A, Doucett R et al (2006) 13C and 15N natural abundance of the soil microbial biomass. Soil Biol Biochem 38:3257–3266CrossRefGoogle Scholar
  12. Emmerton KS, Callaghan TV, Jones HE et al (2001a) Assimilation and isotopic fractionation of nitrogen by mycorrhizal and nonmycorrhizal subarctic plants. New Phytol 151:513–524CrossRefGoogle Scholar
  13. Emmerton KS, Callaghan TV, Jones HE et al (2001b) Assimilation and isotopic fractionation of nitrogen by mycorrhizal fungi. New Phytol 151:503–511CrossRefGoogle Scholar
  14. Fogel ML, Tuross N (1999) Transformation of plant biochemicals to geological macromolecules during early diagenesis. Oecologia 120:336–346CrossRefGoogle Scholar
  15. Friedel JK, Scheller E (2002) Composition of hydrolysable amino acids in soil organic matter and soil microbial biomass. Soil Biol Biochem 34:315–325CrossRefGoogle Scholar
  16. Giblin AE, Laundre JA, Nadelhoffer KJ et al (1994) Measuring nutrient availability in arctic soils using ion exchange resins: a field test. Soil Sci Soc Am J 58:1154–1162Google Scholar
  17. Hinzman LD, Kane DL, Benson CS (1996) Energy balance and hydrological processes in an arctic watershed. In: Reynolds JF, Tenhunen JD et al (eds) Landscape function and disturbance in arctic tundra, Ecological Studies 120. Springer, BerlinGoogle Scholar
  18. Hobbie JE, Hobbie EA (2006) 15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in arctic tundra. Ecology 87:816–822CrossRefGoogle Scholar
  19. Hobbie EA, Wallander H (2005) Integrating ectomycorrhizal fungi into quantitative frameworks of forest carbon and nitrogen cycling. In: Gadd G (ed) Fungi in biogeochemical cycles. Cambridge University Press, New YorkGoogle Scholar
  20. Hobbie EA, Macko SA, Shugart HH (1999) Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia 118:353–360CrossRefGoogle Scholar
  21. Hobbie EA, Macko SA, Williams M (2000) Correlations between foliar δ15N and nitrogen concentrations may indicate plant-mycorrhizal interactions. Oecologia 122:273–283CrossRefGoogle Scholar
  22. Holmes RM, McClelland JW, Sigman DM et al (1998) Measuring 15N-NH4 + in marine, estuarine and fresh waters: an adaptation of the ammonia diffusion method for samples with low ammonium concentrations. Mar Chem 60:235–243CrossRefGoogle Scholar
  23. Keeney DR, Nelson DW (1982) Nitrogen in organic forms. In: Page AL et al (eds) Methods of soil analysis, Part 2. Agronomy No. 9. Am Soc Ag, MadisonGoogle Scholar
  24. Kerley SJ, Read DJ (1995) The biology of mycorrhiza in the ericaceae. XVIII. Chitin degradation by Hymenoscyphus ericae and transfer of chitin-nitrogen to the host plant. New Phytol 131:369–375CrossRefGoogle Scholar
  25. Kerley SJ, Read DJ (1997) The biology of mycorrhiza in the ericaceae. XIX. Fungal mycelium as a nitrogen source for the ericoid mycorrhizal fungus Hymenoscyphus ericae and its host plants. New Phytol 136:691–701CrossRefGoogle Scholar
  26. Kielland K, McFarland J, Olson K (2006) Amino acid uptake in deciduous and coniferous taiga ecosystems. Plant Soil 288:297–307CrossRefGoogle Scholar
  27. Knicker H (2004) Stabilization of N-compounds in soil and organic-matter-rich sediments—what is the difference? Mar Chem 92:167–195CrossRefGoogle Scholar
  28. Kramer MG, Sollins P, Sletten RS et al (2003) N isotope fractionation and measures of organic matter alteration during decomposition. Ecology 84:2021–2025CrossRefGoogle Scholar
  29. Lipson DA, Monson RK (1998) Plant–microbe competition for soil amino acids in the alpine tundra: effects of freeze–thaw and dry–rewet events. Oecologia 113:406–414CrossRefGoogle Scholar
  30. Macko SA, Estep MLF (1984) Microbial alteration of stable nitrogen and carbon isotopic composition of organic matter. Org Geochem 6:787–790CrossRefGoogle Scholar
  31. Macko SA, Fogel Estep KL, Engel MH et al (1986) Kinetic fractionation of stable nitrogen isotopes during amino acid transamination. Geochim Cosmochim Acta 50:2143–2146CrossRefGoogle Scholar
  32. McKane RB, Johnson LC, Shaver GR et al (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71CrossRefGoogle Scholar
  33. Michelsen A, Quarmby C, Sleep S et al (1998) Vascular plant 15N natural abundance in heath and forest tundra ecosystems is closely correlated with presence and type of mycorrhizal fungi in roots. Oecologia 115:406–418CrossRefGoogle Scholar
  34. Mulvaney RL, Khan SA (2001) Diffusion methods to determine different forms of nitrogen in soil hydrolysates. Soil Sci Soc Am J 65:1284–1292CrossRefGoogle Scholar
  35. Nadelhoffer K, Shaver G, Fry B et al (1996) 15N natural abundances and N use by tundra plants. Oecologia 107:386–394CrossRefGoogle Scholar
  36. Ostle NJ, Bol R, Petzke KJ et al (1999) Compound specific δ15Ν% values: amino acids in grassland and arable soils. Soil Biol Biochem 31:1751–1755CrossRefGoogle Scholar
  37. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–492CrossRefGoogle Scholar
  38. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602CrossRefGoogle Scholar
  39. Schimel JP, Chapin FS III (1996) Tundra plant uptake of amino acid and NH4 + nitrogen in situ: plants compete well for amino acid N. Ecology 77:2142–2147CrossRefGoogle Scholar
  40. Selle A, Willmann M, Grunze N, Geßler A, Weiß M, Nehls U (2005) The high-affinity poplar ammonium importer PttAMT1.2 and its role in ectomycorrhizal symbiosis. New Phytol 168:697–706CrossRefGoogle Scholar
  41. Shaver GR, Nadelhoffer KJ, Giblin AE (1991) Biogeochemical diversity and element transport in a heterogeneous landscape, the North Slope of Alaska. In: Turner MG, Gardner RH (eds) Quantitative methods in landscape ecology. Springer, New YorkGoogle Scholar
  42. Shaver GR, Candell J, Chapin FS III et al (2000) Global warming and terrestrial ecosystmes: a conceptual framework for analysis. BioSci 50:871–882CrossRefGoogle Scholar
  43. Shaver GR, Bret-Harte SM, Jones MH et al (2001) Species composition interacts with fertilizer to control long-term change in tundra productivity. Ecology 82:3163–3181Google Scholar
  44. Sigman DM, Altabet MA, Michener R et al (1997) Natural abundance-level measurement of the nitrogen isotopic composition of oceanic nitrate: an adaptation of the ammonia diffusion method. Mar Chem 57:227–242CrossRefGoogle Scholar
  45. Smith S, Read D (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, San DiegoGoogle Scholar
  46. Taylor AFS, Högbom L, Högberg M et al (1997) Natural 15N abundance in fruit bodies of ectomycorrhizal fungi from boreal forests. New Phytol 136:713–720CrossRefGoogle Scholar
  47. Taylor AFS, Gebauer G, Read DJ (2004) Uptake of nitrogen and carbon from double-labelled (15N and 13C) glycine by mycorrhizal pine seedlings. New Phytol 164:383–388CrossRefGoogle Scholar
  48. Urcelay C, Bret-Harte MS, Daz S et al (2003) Mycorrhizal colonization mediated by species interactions in arctic tundra. Oecologia 137:399–404CrossRefGoogle Scholar
  49. Walker DA, Walker MD (1996) Terrain and vegetation of the Imnavait Creek watershed. In: Reynolds JF, Tenhunen JD (eds) Landscape function and disturbance in arctic tundra, Ecological Studies 120. Springer, BerlinGoogle Scholar
  50. Werner RA, Schmidt HL (2002) The in vivo nitrogen isotope discrimination among organic plant compounds. Phytochem 61:465–484CrossRefGoogle Scholar
  51. Zang X, van Heemst JDH, Dria KJ et al (2000) Encapsulation of protein in humic acid from a histosol as an explanation for the occurrence of organic nitrogen in soil and sediment. Org Geochem 31:679–695CrossRefGoogle Scholar
  52. Zhang X, Amelung W, Yuan Y et al (1999) Land-use effects on amino sugars in particle size fractions of an Argiudoll. Appl Soil Ecol 11:271–275CrossRefGoogle Scholar
  53. Zeller B, Brechet C, Maurice JP et al (2007) 13C and 15N isotopic fractionation in trees, soils and fungi in a natural forest stand and a Norway spruce plantation. Annal For Sci 64:419–429CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Y. Yano
    • 1
    • 2
    Email author
  • G. R. Shaver
    • 1
  • A. E. Giblin
    • 1
  • E. B. Rastetter
    • 1
  1. 1.The Ecosystems Center, Marine Biological LaboratoryWoods HoleUSA
  2. 2.Human and Health Services, Municipality of AnchorageAnchorageUSA

Personalised recommendations