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Responses of soil extracellular enzyme activities to experimental warming and CO2 enrichment at the alpine treeline

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Abstract

Background and aims

Climate warming and elevated CO2 can modify nutrient cycling mediated by enzymes in soils, especially in cold-limited ecosystems with a low availability of nutrients and a high temperature sensitivity of decomposition and mineralization.

Methods

We estimated responses of soil extracellular enzyme activities (EEAs) to 6 years of soil warming and 9 years of CO2 enrichment at an Alpine treeline site. EEAs were measured in the litter (L), fermentation (F) and humified (H) horizons under Larix decidua and Pinus uncinata trees.

Results

Soil warming indirectly affected EEAs through altered soil moisture, fine root biomass, and C:N ratio of the organic horizons. Warming increased β-glucosidase and β-xylosidase activities in the F horizon but led to reduced laccase activity in the L horizon, probably caused by drying of the litter horizon associated with the treatment. In the H horizon, previous CO2 enrichment altered the activity of leucine amino peptidase, N-acetylglucosaminidase, and phosphatase. No interactive effects between warming and CO2 enrichment were detected. Warming affected the temperature sensitivity of β-xylosidase but not of the other enzymes.

Conclusions

Altered EEAs after six years of soil warming indicate a sustained stimulation of carbon, nitrogen and nutrient cycling under climatic warming at the alpine treeline.

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References

  • Baldrian P, Vě M, Cajthaml T, Petránková M, Šnajdr J (2010) Small-scale distribution of extracellular enzymes, fungal, and bacterial biomass in Quercus petraea forest topsoil. Biol Fertil Soils 46:717–726

    Article  CAS  Google Scholar 

  • Barbeito I, Dawes M, Rixen C, Senn J, Bebi P (2012) Factors driving mortality and growth at treeline: a 30-year experiment of 92000 conifers. Ecology 93:389–401

    Article  PubMed  Google Scholar 

  • Bardgett RD, Freeman C, Ostle NJ (2008) Microbial contributions to climate change through carbon cycle feedbacks. ISME J 2:805–814

    Article  CAS  PubMed  Google Scholar 

  • Blackwood CB, Waldrop MP, Zak DR, Sinsabaugh RL (2007) Molecular analysis of fungal communities and laccase genes in decomposing litter reveals differences among forest types but no impact of nitrogen deposition. Environ Microbiol 9:1306–1316

    Article  CAS  PubMed  Google Scholar 

  • Bowman W, Seastedt T, Program L-TER (2001) Structure and function of an alpine ecosystem: Niwot ridge, Colorado. Oxford University Press, USA

    Google Scholar 

  • Bradford MA, Watts BW, Davies CA (2010) Thermal adaptation of heterotrophic soil respiration in laboratory microcosms. Glob Chang Biol 16:1576–1588

    Article  Google Scholar 

  • Brzostek E, Finzi A (2011) Substrate supply, fine roots, and temperature control proteolytic enzyme activity in temperate forest soils. Bull Ecol Soc Am 92:892–902

    Google Scholar 

  • Coker JA, Sheridan PP, Loveland-Curtze J, Gutshall KR, Auman AJ, Brenchley JE (2003) Biochemical characterization of a ß-galactosidase with a low temperature optimum obtained from an Antarctic arthrobacter isolate. J Bacteriol 185:5473–5482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Cornelissen JH, Van Bodegom PM, Aerts R, Callaghan TV, Van Logtestijn RS, Alatalo J, Stuart Chapin F, Gerdol R, Gudmundsson J, Gwynn-Jones D, Hartley AE, Hik DS, Hofgaard A, Jónsdóttir IS, Karlsson S, Klein JA, Laundre J, Magnusson B, Michelsen A, Molau U, Onipchenko VG, Quested HM, Sandvik SM, Schmidt IK, Shaver GR, Solheim B, Soudzilovskaia NA, Stenström A, Tolvanen A, Totland Ø, Wada N, Welker JM, Zhao X, Team M (2007) Global negative vegetation feedback to climate warming responses of leaf litter decomposition rates in cold biomes. Ecol Lett 10:619–627

    Article  PubMed  Google Scholar 

  • Criquet S, Ferre E, Farnet A, Petit Null JL (2004) Annual dynamics of phosphatase activities in an evergreen oak litter: influence of biotic and abiotic factors. Soil Biol Biochem 36:1111–1118

    Article  CAS  Google Scholar 

  • Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173

    Article  CAS  PubMed  Google Scholar 

  • Davidson EA, Belk E, Boone RD (1998) Soil water content and temperature as independent or confounded factors controlling soil respiration in a temperate mixed hardwood forest. Glob Chang Biol 4:217–227

    Article  Google Scholar 

  • Dawes MA, Hagedorn F, Handa IT, Streit K, Ekblad A, Rixen C, Körner C, Hättenschwiler S (2013) An alpine treeline in a carbon dioxide-rich world: synthesis of a nine-year free-air carbon dioxide enrichment study. Oecologia 171:623–637

    Article  PubMed  Google Scholar 

  • Dawes MA, Zweifel R, Dawes N, Rixen C, Hagedorn F (2014) CO2 enrichment alters diurnal stem radius fluctuations of 36-yr-old Larix decidua growing at the alpine tree line. New Phytol 202:1237–1248

    Article  CAS  PubMed  Google Scholar 

  • Dawes MA, Philipson CD, Fonti P, Bebi P, Hättenschwiler S, Hagedorn F, Rixen C (2015) Soil warming and CO2 enrichment induce biomass shifts in alpine tree line vegetation. Glob Chang Biol 21:2005–2021

    Article  PubMed  Google Scholar 

  • Dawes MA, Schleppi P, Hättenschwiler S, Rixen C, Hagedorn F (2016) Soil warming opens the nitrogen cycle at the alpine treeline. Glob Chang Biol 23:421–434

    Article  PubMed  Google Scholar 

  • Ebersberger D, Niklaus PA, Kandeler E (2003) Long term CO2 enrichment stimulates N-mineralisation and enzyme activities in calcareous grassland. Soil Biol Biochem 35:965–972

    Article  CAS  Google Scholar 

  • Fenner N, Freeman C, Reynolds B (2005) Observations of a seasonally shifting thermal optimum in peatland carbon-cycling processes; implications for the global carbon cycle and soil enzyme methodologies. Soil Biol Biochem 37:1814–1821

    Article  CAS  Google Scholar 

  • German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397

    Article  CAS  Google Scholar 

  • Gramss G, Voigt K-D, Kirsche B (1999) Oxidoreductase enzymes liberated by plant roots and their effects on soil humic material. Chemosphere 38:1481–1494

    Article  CAS  Google Scholar 

  • Hagedorn F, Machwitz M (2007) Controls on dissolved organic matter leaching from forest litter grown under elevated atmospheric. Soil Biol Biochem 39:1759–1769

    Article  CAS  Google Scholar 

  • Hagedorn F, van Hees PAW, Handa IT, Hättenschwiler S (2008) Elevated atmospheric CO2 fuels leaching of old dissolved organic matter at the alpine treeline. Glob Biogeochem Cycles 22:GB2004

    Article  Google Scholar 

  • Hagedorn F, Martin M, Rixen C, Rusch S, Bebi P, Zürcher A, Siegwolf R, Wipf S, Escape C, Roy J, Hättenschwiler S (2010) Short-term responses of ecosystem carbon fluxes to experimental soil warming at the Swiss alpine treeline. Biogeochemistry 97:7–19

    Article  CAS  Google Scholar 

  • Hagedorn F, Hiltbrunner D, Streit K, Ekblad A, Lindahl B, Miltner A, Frey B, Handa IT, Hättenschwiler S (2013) Nine years of CO2 enrichment at the alpine treeline stimulates soil respiration but does not alter soil microbial communities. Soil Biol Biochem 57:390–400

    Article  CAS  Google Scholar 

  • Hamilton WE, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:2397–2402

    Article  Google Scholar 

  • Harsch MA, Hulme PE, McGlone MS, Duncan RP (2009) Are treelines advancing? A global meta-analysis of treeline response to climate warming. Ecol Lett 12:1040–1049

    Article  PubMed  Google Scholar 

  • Hättenschwiler S, Handa IT, Egli L, Asshoff R, Ammann W, Körner C (2002) Atmospheric CO2 enrichment of alpine treeline conifers. New Phytol 156:363–375

    Article  Google Scholar 

  • Henry HA (2012) Soil extracellular enzyme dynamics in a changing climate. Soil Biol Biochem 47:53–59

    Article  CAS  Google Scholar 

  • Henry HAL, Juarez JD, Field CB, Vitousek PM (2005) Interactive effects of elevated CO2, N deposition and climate change on extracellular enzyme activity and soil density fractionation in a California annual grassland. Glob Chang Biol 11:1808–1815

    Article  Google Scholar 

  • Hoppe H (1983) Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Mar Ecol Prog Ser 11:299–308

    Article  CAS  Google Scholar 

  • Huang P, Senesi N, Buffle J (1998) Structure and surface reactions of soil particles. John Wiley & Sons Ltd, Chichester

    Google Scholar 

  • Hungate BA, Lund CP, Pearson HL, Chapin FS (1997) Elevated CO2 and nutrient addition after soil N cycling and N trace gas fluxes with early season wet-up in a California annual grassland. Biogeochemistry 37:89–109

    Article  CAS  Google Scholar 

  • Huston AL, Krieger-Brockett BB, Deming JW (2000) Remarkably low temperature optima for extracellular enzyme activity from Arctic bacteria and sea ice. Environ Microbiol 2:383–388

    Article  CAS  PubMed  Google Scholar 

  • Kammer A, Hagedorn F, Shevchenko I, Leifeld J, Guggenberger G, Goryacheva T, Rigling A, Moiseev P (2009) Treeline shifts in the Ural mountains affect soil organic matter dynamics. Glob Chang Biol 15:1570–1583

    Article  Google Scholar 

  • Keeler BL, Hobbie SE, Kellogg LE (2009) Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites: implications for litter and soil organic matter decomposition. Ecosystems 12:1–15

    Article  CAS  Google Scholar 

  • Kelley AM, Fay PA, Polley HW, Gill RA, Jackson RB (2011) Atmospheric CO2 and soil extracellular enzyme activity: a meta-analysis and CO2 gradient experiment. Ecosphere 2:1–20

    Article  Google Scholar 

  • Koch O, Tscherko D, Kandeler E (2007) Temperature sensitivity of microbial respiration, nitrogen mineralization, and potential soil enzyme activities in organic alpine soils. Global Biogeochem Cy 21:GB4017

    Article  Google Scholar 

  • Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194

    Article  PubMed  Google Scholar 

  • Pinheiro J, Bates D (2000) Mixed-effects models in S and S-PLUS. Springer, New York

    Book  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D (2016) Nlme: linear and nonlinear mixed effects models. R package version 3:1–128

    Google Scholar 

  • Pritsch K, Courty P, Churin J-L, Cloutier-Hurteau B, Ali M, Damon C, Duchemin M, Egli S, Ernst J, Fraissinet-Tachet L, Kuhar F, Legname E, Marmeisse R, Müller A, Nikolova P, Peter M, Plassard C, Richard F, Schloter M, Selosse M-A, Franc A, Garbaye J (2011) Optimized assay and storage conditions for enzyme activity profiling of ectomycorrhizae. Mycorrhiza 21:589–600

    Article  CAS  PubMed  Google Scholar 

  • Rosseel Y (2012) Lavaan: an R package for structural equation modeling. J Stat Softw 48:1–36

    Article  Google Scholar 

  • Sardans J, Peñuelas J (2005) Drought decreases soil enzyme activity in a Mediterranean Quercus ilex L. forest. Soil Biol Biochem 37:455–461

    Article  CAS  Google Scholar 

  • Schindlbacher A, Wunderlich S, Borken W, Kitzler B, Zechmeister-Boltenstern S, Jandl R (2012) Soil respiration under climate change: prolonged summer drought offsets soil warming effects. Glob Chang Biol 18:2270–2279

    Article  PubMed Central  Google Scholar 

  • Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798

    Article  CAS  PubMed  Google Scholar 

  • Smith W, Germino M, Johnson D, Reinhardt K (2009) The altitude of alpine treeline: a bellwether of climate change effects. Bot Rev 75:163–190

    Article  Google Scholar 

  • Šnajdr J, Dobiášová P, Větrovský T, Valášková V, Alawi A, Boddy L, Baldrian P (2011) Saprotrophic basidiomycete mycelia and their interspecific interactions affect the spatial distribution of extracellular enzymes in soil. FEMS Microbiol Ecol 78:80–90

    Article  PubMed  Google Scholar 

  • Sterkenburg E, Bahr A, Brandström Durling M, Clemmensen KE, Lindahl BD (2015) Changes in fungal communities along a boreal forest soil fertility gradient. New Phytol 207:1145–1158

    Article  PubMed  Google Scholar 

  • Streit K, Hagedorn F, Hiltbrunner D, Portmann M, Saurer M, Buchmann N, Wild B, Richter A, Wipf S, Siegwolf RTW (2014) Soil warming alters microbial substrate use in alpine soils. Glob Chang Biol 20:1327–1338

    Article  PubMed  Google Scholar 

  • Talbot J, Yelle D, Nowick J, Treseder K (2012) Litter decay rates are determined by lignin chemistry. Biogeochemistry 108:279–295

    Article  CAS  Google Scholar 

  • Wallenstein D (2011) Controls on the temperature sensitivity of soil enzymes: a key driver of in situ enzyme activity rates enzymes: a key driver of in situ enzyme activity rates. In: Shukla G, Varma A (eds) Soil enzymology. Springer, Berlin, pp 245–258

    Google Scholar 

  • Wallenstein MD, McMahon SK, Schimel JP (2009) Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Glob Chang Biol 15:1631–1639

    Article  Google Scholar 

  • Yang Z, Wullschleger SD, Liang L, Graham DE, Gu B (2016) Effects of warming on the degradation and production of low-molecular-weight labile organic carbon in an Arctic tundra soil. Soil Biol Biochem 95:202–211

    Article  CAS  Google Scholar 

  • Zantua M, Bremner J (1975) Comparison of methods of assaying urease activity in soils. Soil Biol Biochem 7:291–295

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to many colleagues at the SLF and WSL for contributing to the Stillberg CO2 enrichment and soil warming experiment. In particular, we thank Stephan Hättenschwiler and I. Tanya Handa for planning and initiating this climate change study. We thank Barbara Meier and Rosmarie Eppenberger at the WSL for their assistance in lab measurements. We also thank Adam Butler at the BioSS (UK) for helping with statistical analysis. Major funding sources for this 12-year study included the following: the Swiss National Science Foundation from 2001 to 2005 (grant 31-061428.00 to Stephan Hättenschwiler) and from 2007 to 2010 (grant 315200-116861 to CR); the Velux Foundation from 2007 to 2012 (grant 371 to FH); and the WSL from 2012 to 2016 (grant to CR and MD). This work is part of RCS’s Master’s thesis, which was funded by CAPES, Brazil; the Large-scale Biosphere-Atmosphere Programme of MCTI, Brazil is acknowledged for additional support.

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Authors and Affiliations

  1. Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), Zürcherstrasse 111, -8903, Birmensdorf, CH, Switzerland

    Rômulo C. Souza, Emily F. Solly, Melissa A. Dawes, Frank Hagedorn, Simon Egli & Martina Peter

  2. WSL Institute for Snow and Avalanche Research – SLF, Flüelastrasse 11, -7260, Davos Dorf, CH, Switzerland

    Rômulo C. Souza, Melissa A. Dawes, Frank Graf & Christian Rixen

  3. Instituto Nacional de Pesquisas da Amazônia (INPA), Av. André Araújo 2.936, Petrópolis, CEP, Manaus, AM, 69067-375, Brazil

    Rômulo C. Souza & Charles R. Clement

  4. Universidade Estadual de Campinas (UNICAMP), Rua Monteiro Lobato 255, Cidade Universitária “Zeferino Vaz” Barão Geraldo, CEP, Campinas, SP, 13083-970, Brazil

    Laszlo Nagy

Authors
  1. Rômulo C. Souza
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  2. Emily F. Solly
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  3. Melissa A. Dawes
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  4. Frank Graf
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  5. Frank Hagedorn
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  6. Simon Egli
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  7. Charles R. Clement
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  8. Laszlo Nagy
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  9. Christian Rixen
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  10. Martina Peter
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Correspondence to Rômulo C. Souza or Martina Peter.

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Souza, R.C., Solly, E.F., Dawes, M.A. et al. Responses of soil extracellular enzyme activities to experimental warming and CO2 enrichment at the alpine treeline. Plant Soil 416, 527–537 (2017). https://doi.org/10.1007/s11104-017-3235-8

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