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Uptake of pulse injected nitrogen by soil microbes and mycorrhizal and non-mycorrhizal plants in a species-diverse subarctic heath ecosystem

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Abstract

15N labeled ammonium, glycine or glutamic acid was injected into subarctic heath soil in situ, with the purpose of investigating how the nitrogen added in these pulses was subsequently utilized and cycled in the ecosystem. We analyzed the acquisition of 15N label in mycorrhizal and non-mycorrhizal plants and in soil microorganisms, in order to reveal probable differences in acquisition patterns between the two functional plant types and between plants and soil microorganisms. Three weeks after the label addition, with the 15N-forms added with same amount of nitrogen per square meter, we analyzed the 15N-enrichment in total soil, in soil K2SO4 (0.5 M) extracts and in the microbial biomass after vacuum-incubation of soil in chloroform and subsequent K2SO4 extraction. Furthermore the 15N-enrichment was analyzed in current years leaves of the dominant plant species sampled three, five and 21 days after label addition. The soil microorganisms had very high 15N recovery from all the N sources compared to plants. Microorganisms incorporated most 15N from the glutamic acid source, intermediate amounts of 15N from the glycine source and least 15N from the NH4 + source. In contrast to microorganisms, all ten investigated plant species generally acquired more 15N label from the NH4 + source than from the amino acid sources. Non-mycorrhizal plant species showed higher concentration of 15N label than mycorrhizal plant species 3 days after labeling, while 21 days after labeling their acquisition of 15N label from amino acid injection was lower than, and the acquisition of 15N label from NH4 injection was similar to that of the mycorrhizal species. We conclude that the soil microorganisms were more efficient than plants in acquiring pulses of nutrients which, under natural conditions, occur after e.g. freeze–thaw and dry–rewet events, although of smaller size. It also appears that the mycorrhizal plants in the short term may be less efficient than non-mycorrhizal plants in nitrogen acquisition, but in a longer term show larger nitrogen acquisition than non-mycorrhizal plants. However, the differences in 15N uptake patterns may also be due to differences in leaf longevity and woodiness between plant functional groups.

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References

  • Abuarghub SM, Read DJ (1988a) The biology of mycorrhiza in the Ericaceae XI. The distribution of nitrogen in soil of a typical upland Callunetum with special reference to the ‘free’ amino acids. New Phytol 108:425–431

    Article  Google Scholar 

  • Abuarghub SM, Read DJ (1988b) The biology of mycorrhizae in the Ericaceae. XII Quantitative analysis of individual ‘free’ amino acids in relation to time and depth in the soil profile. New Phytol 108:433–441

    Article  CAS  Google Scholar 

  • Aerts R, de Caluwe H (1995) Interspecific and intraspecific differences in shoot and leaf lifespan of four Carex species which differ in maximum dry matter production. Oecologia 102:467–477

    Article  Google Scholar 

  • Andresen LC, Michelsen A (2005) Off-season uptake of nitrogen in temperate heath vegetation. Oecologia 144:585–597

    Article  PubMed  Google Scholar 

  • Bardgett RD, Streeter TC, Bol R (2003) Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands. Ecology 84:1277–1287

    Article  Google Scholar 

  • Bennett JN, Prescott CE (2004) Organic and inorganic nitrogen nutrition of western red cedar, western hemlock and salal in mineral N-limited cedar-hemlock forests. Oecologia 141:468–476

    Article  PubMed  Google Scholar 

  • Bremner JM, Keeney DR (1965) Steam distillation methods for determination of ammonium, nitrate and nitrite. Anal Chim Acta 32:485–495

    Article  CAS  Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:827–842

    Article  Google Scholar 

  • Chalot M, Javelle A, Blaudez D, Lambilliote R, Cooke R, Sentenac H et al (2002) An update on nutrient transport processes in ectomycorrhizas. Plant Soil 244:165–175

    Article  CAS  Google Scholar 

  • Cheng X, Bledsoe CS (2004) Competition for inorganic and organic N by blue oak (Quercus douglasii) seedlings, an annual grass, and soil microorganisms in a pot study. Soil Biol Biochem 36:135–144

    Article  CAS  Google Scholar 

  • Clemmesen KE, Michelsen A, Jonasson S, Shaver GR (2006) Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phytol 171:391–404

    Article  Google Scholar 

  • Clemmesen KE, Sorensen PL, Michelsen A, Jonasson S, Ström L (2008) Site-dependent N uptake from N-form mixtures by arctic plants, soil microbes and ectomycorrhizal fungi. Oecologia 155:771–783

    Article  Google Scholar 

  • Falkengren-Grerup U, Månsson KF, Olsson MO (2000) Uptake capacity of amino acids by ten grasses and forbs in relation to soil acidity and nitrogen availability. Environ Exp Bot 44:207–219

    Article  PubMed  CAS  Google Scholar 

  • Finzi AC, Berthrong ST (2005) The uptake of amino acids by microbes and trees in three cold-temperate forests. Ecology 86:3345–3533

    Article  Google Scholar 

  • Fry B (2006) Stable isotope ecology. Springer, New York

    Google Scholar 

  • Grogan P, Jonasson S (2003) Controls on annual nitrogen cycling in the understory of a subarctic birch forest. Ecology 84:202–218

    Article  Google Scholar 

  • Hofmockel KS, Schlesinger WH, Jackson RB (2007) Effects of elevated atmospheric carbon dioxide on amino acid and NH4 +–N cycling in a temperate pine ecosystem. Glob Change Biol 13:1950–1959

    Article  Google Scholar 

  • Illeris L, Jonasson S (1999) Soil and plant CO2 emission in response to variations in soil moisture and temperature and to amendment with nitrogen, phosphorus, and carbon in Northern Scandinavia. Arct Antarct Alp Res 31:264–271

    Article  Google Scholar 

  • Jaeger CH, Monson RK, Fisk MC, Schmidt SK (1999) Seasonal partitioning of nitrogen by plants and soil microorganisms in an alpine ecosystem. Ecology 80:1883–1891

    Article  Google Scholar 

  • Joergensen RG, Mueller T (1996) The fumigation–extraction method to estimate soil microbial biomass: calibration of the ken value. Soil Biol Biochem 28:33–37

    Article  CAS  Google Scholar 

  • Jonasson S, Michelsen A, Schmidt IK, Nielsen EV, Callaghan TV (1996) Microbial biomass C, N and P in two arctic soils and responses to addition of NPK fertilizer and sugar: implications for plant nutrient uptake. Oecologia 106:507–515

    Article  Google Scholar 

  • Jones DL, Kielland K (2002) Soil amino acid turnover dominates the nitrogen flux in permafrost-dominated teiga forest soils. Soil Biol Biochem 34:209–219

    Article  CAS  Google Scholar 

  • Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A (2005a) Dissolved organic nitrogen uptake by plants – an important N uptake pathway? Soil Biol Biochem 37:413–423

    Article  CAS  Google Scholar 

  • Jones DL, Shannon D, Junvee-Fortune T, Farrar JF (2005b) Plant capture of free amino acids is maximized under high soil amino acid concentrations. Soil Biol Biochem 37:179–181

    Article  CAS  Google Scholar 

  • Jonsson A, Ström L, Åberg J (2007) Composition and variations in the occurrence of dissolved free simple organic compounds of an unproductive lake ecosystem in northern Sweden. Biogeochemistry 82:153–163

    Article  CAS  Google Scholar 

  • Karlsson PS (1992) Leaf longevity in evergreen shrubs: variation within and among European species. Oecologia 91:346–349

    Article  Google Scholar 

  • Kielland K (1994) Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75:2373–2383

    Article  Google Scholar 

  • Kielland K (1995) Landscape patterns of free amino acids in arctic tundra soils. Biogeochemistry 31:85–98

    Article  CAS  Google Scholar 

  • Kielland K, McFarland J, Olson K (2006) Amino acid uptake in deciduous and coniferous taiga ecosystems. Plant Soil 288:297–307

    Article  CAS  Google Scholar 

  • Kielland K, McFarland JW, Ruess RW, Olson K (2007) Rapid cycling of organic nitrogen in taiga forest ecosystems. Ecosystems 10:360–368

    Article  CAS  Google Scholar 

  • Konestabo HS, Michelsen A, Holmstrup M (2007) Responses of springtail and mite populations to prolonged periods of soil freeze–thaw cycles in a sub-arctic ecosystem. Appl Soil Ecol 36:136–146

    Article  Google Scholar 

  • Larsen KS, Jonasson S, Michelsen A (2002) Repeated freeze–thaw cycles and their effects on biological processes in two arctic ecosystem types. Appl Soil Ecol 21:187–195

    Article  Google Scholar 

  • Lipson DA, Raab TK, Schmidt SK, Monson RK (1999) Variation in competitive abilities of plants and microbes for specific amino acids. Biol Fertil Soils 29:257–261

    Article  CAS  Google Scholar 

  • McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B et al (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71

    Article  PubMed  CAS  Google Scholar 

  • Michelsen A, Schmidt IK, Jonasson S, Quarmby C, Sleep D (1996) Leaf 15N abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non- and arbuscular mycorrhizal species access different sources of soil nitrogen. Oecologia 105:53–63

    Article  Google Scholar 

  • Michelsen A, Quarmby C, Sleep D, Jonasson S (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 115:406–418

    Article  Google Scholar 

  • Michelsen A, Graglia E, Schmidt IK, Jonasson S, Sleep D, Quarmby C (1999) Differential responses of grass and a dwarf shrub to long-term changes in soil microbial biomass C, N and P following factorial addition of NPK fertilizer, fungicide and labile carbon to a heath. New Phytol 143:523–538

    Article  Google Scholar 

  • Miller AE, Bowman WD (2003) Alpine plants show species-level differences in the uptake of organic and inorganic nitrogen. Plant Soil 250:283–292

    Article  CAS  Google Scholar 

  • Näsholm T, Ekblad A, Nordin A, Giesler R, Högberg M, Högberg P (1998) Boreal forest plants take up organic nitrogen. Nature 392:914–916

    Article  Google Scholar 

  • Nordin A, Schmidt IK, Shaver GR (2004) Nitrogen uptake by arctic soil microbes and plants in relation to soil nitrogen supply. Ecology 85:955–962

    Article  Google Scholar 

  • Paul EA, Clark FE (1996) Soil microbiology and biochemistry. Academic, New York

    Google Scholar 

  • Robinson CH, Michelsen A, Lee JA, Whitehead SJ, Callaghan TV, Press MC et al (1997) Elevated atmospheric CO2 affects decomposition of Festuca vivipara (L.) Sm. litter and roots in experiments simulating environmental change in two contrasting arctic ecosystems. Glob Change Biol 3:37–49

    Article  Google Scholar 

  • Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J, GCTE-NEWS (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562

    Article  Google Scholar 

  • SAS Institute Inc (2003) The SAS system for windows. SAS Institute Inc., Cary, NC, USA

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602

    Article  Google Scholar 

  • Schimel JP, Chapin IFS (1996) Tundra plant uptake of amino acid and NH4 + nitrogen in situ: plants compete well for amino acid N. Ecology 77:2142–2147

    Article  Google Scholar 

  • Schmidt IK, Jonasson S, Michelsen A (1999) Mineralization and microbial immobilization of N and P in arctic soils in relation to season, temperature and nutrient amendment. Appl Soil Ecol 11:147–160

    Article  Google Scholar 

  • Schmidt IK, Ruess L, Bååth E, Michelsen A, Ekelund F, Jonasson S (2000) Long-term manipulation of the microbes and microfauna of two subarctic heaths by addition of fungicide, bactericide, carbon and fertilizer. Soil Biol Biochem 32:707–720

    Article  CAS  Google Scholar 

  • Sharma S, Szele Z, Schilling R, Munch JC, Schloter M (2006) Influence of freeze–thaw stress on the structure and function of microbial communities and denitrifying populations in soil. Appl Environ Microbiol 72:2148–2154

    Article  PubMed  CAS  Google Scholar 

  • Sorensen PL, Clemmesen KE, Michelsen A, Jonasson S, Ström L (2008) Plant and microbial uptake and allocation of organic and inorganic nitrogen related to plant growth forms and soil conditions at two subarctic tundra sites in Sweden. Arct Antarct Alp Res 40:171–180

    Article  Google Scholar 

  • Ström L, Christensen TR (2007) Below ground carbon turnover and greenhouse gas exchanges in a sub-arctic wetland. Soil Biol Biochem 39:1689–1698

    Article  Google Scholar 

  • Svennerstam H, Ganeteg U, Bellini C, Näsholm T (2007) Comprehensive screening of arabidopsis mutants suggests the lysine histidine transporter 1 to be involved in plant uptake of amino acids. Plant Physiol 143:1853–1860

    Article  PubMed  CAS  Google Scholar 

  • Vinolas LC, Healey JR, Jones DL (2001) Kinetics of soil microbial uptake of free amino acids. Biol Fertil Soils 33:67–74

    Article  CAS  Google Scholar 

  • Weintraub MN, Schimel JP (2005) The seasonal dynamics of amino acids and other nutrients in Alaskan Arctic soils. Biogeochemistry 73:259–280

    Article  Google Scholar 

  • Williams LE, Miller AJ (2001) Transporters responsible for the uptake and partitioning of nitrogenous solutes. Annu Rev Plant Physiol Plant Mol Biol 52:659–688

    Article  PubMed  CAS  Google Scholar 

  • Xu X, Ouyang H, Kuzyakov Y, Richter A, Wanek W (2006) Significance of organic nitrogen acquisition for dominant plant species in an alpine meadow on the Tibet plateau, China. Plant Soil 285:221–231

    Article  CAS  Google Scholar 

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Acknowledgements

The Danish Research Council for Nature and Universe is acknowledged for the funding of the field work. The Isotope Ratio Mass Spectrometer at the University of Copenhagen. Darren Sleep and Chris Quarmby at the Stable Isotope Facility, CEH Merlewood, Grange-Over-Sands, UK are thanked for collaboration with analysis of 15N. The Villum Kann Rasmussen Foundation and the University of Copenhagen are thanked for supporting LCA. Finally, we would like to thank anonymous referees for constructive comments on earlier versions of the manuscript.

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Correspondence to Louise C. Andresen.

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Andresen, L.C., Jonasson, S., Ström, L. et al. Uptake of pulse injected nitrogen by soil microbes and mycorrhizal and non-mycorrhizal plants in a species-diverse subarctic heath ecosystem. Plant Soil 313, 283–295 (2008). https://doi.org/10.1007/s11104-008-9700-7

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