Abstract
The nature of linkages between soil C and N cycling is important in the context of terrestrial ecosystem responses to global environmental change. Extracellular enzymes produced by soil microorganisms drive organic matter decomposition, and are considered sensitive indicators of soil responses to environmental variation. We investigated the response of eight hydrolytic soil enzymes (four peptidases and four glycosidases) to experimental warming in a long-term climate manipulation experiment in a sub-arctic peat bog, to determine to what extent the response of these two functional groups are similar. We found no significant effect of experimental spring and summer warming and/or winter snow addition on either the potential activity or the temperature sensitivity (of Vmax) of any of the enzymes. However, strong and contrasting seasonal patterns in both variables were observed. All of the peptidases, as well as alpha-glucosidase, had lower potential activity at the end of summer (August) compared to the beginning (June). Conversely, beta-glucosidase had significantly higher potential activity in August. Peptidases had consistently higher temperature sensitivities in June compared to August, while all four glycosidases showed the opposite pattern. Our results suggest that warming effects on soil enzymes are small compared to seasonal differences, which are most likely mediated by the seasonality of substrate supply and microbial nutrient demand. Furthermore the contrasting seasonal patterns for glycosidases and peptidases suggest that enzyme-based models of soil processes need to allow for potential divergence between the production and activity of these two enzyme functional groups.
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References
ACIA (2004) Impacts of a Warming Arctic: Arctic Climate Impact Assessment. Cambridge University Press, Cambridge
Aerts R (1997) Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79:439–449
Aerts R, Cornelissen JHC, van Logtestijn RSP, Callaghan TV (2007) Climate change has only a minor impact on nutrient resorption parameters in a high-latitude peatland. Oecologia 151:132–139
Aerts R, Callaghan TV, Dorrepaal E, van Logtestijn RSP, Cornelissen JHC (2012) Seasonal climate manipulations have only minor effects on litter decomposition rates and N dynamics but strong effects on litter P dynamics of sub-arctic bog species. Oecologia 170:809–819
Allison SD (2012) A trait-based approach for modelling microbial litter decomposition. Ecol Lett 15:1058–1070
Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA 105:11512–11519
Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944
Allison SD, Gartner TB, Holland K, Weintraub M, Sinsabaugh RL (2007) Soil enzymes: linking proteomics and ecological process. In: Lipson DA, Mills AL, Stetzenbach LD (eds) Manual of Environmental Microbiology, 3rd edn. ASM Press, Herndon, pp 704–711
Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340
Allison SD, Weintraub M, Gartner TB, Waldrop MP (2011) Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. In: Shukla G, Varma A (eds) Soil enzymology. Springer-Verlag, Berlin
Bell TH, Henry HAL (2011) Fine scale variability in soil extracellular enzyme activity is insensitive to rain events and temperature in a mesic system. Pedobiologia 54:141–146
Bell TH, Klironomos JN, Henry HAL (2010) Seasonal responses of extracellular enzyme activity and microbial biomass to warming and nitrogen addition. Soil Sci Soc Am J 74:820–828
Bonnett SAF, Ostle N, Freeman C (2006) Seasonal variations in decomposition processes in a valley-bottom riparian peatland. Sci Total Environ 370:561–573
Caldwell BA (2005) Enzyme activities as a component of soil biodiversity: a review. Pedobiologia 49:637–644
Chapman SJ, Thurlow M (1998) Peat respiration at low temperatures. Soil Biol Biochem 30:1013–1021
Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113
DeForest JL (2009) The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and l-DOPA. Soil Biol Biochem 41:1180–1186
Dorrepaal E, Aerts R, Cornelissen JHC, Callaghan TV, van Logtestijn RSP (2004) Summer warming and increased winter snow cover affect Sphagnum fuscum growth, structure and production in a sub-arctic bog. Global Change Biol 10:93–104
Dorrepaal E, Toet S, van Logtestijn RSP, Swart E, van de Weg MJ, Callaghan TV, Aerts R (2009) Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 460:U616–U679
Falge E, Baldocchi D, Tenhunen J, Aubinet M, Bakwin P, Berbigier P, Bernhofer C, Burba G, Clement R, Davis KJ, Elbers JA, Goldstein AH, Grelle A, Granier A, Guomundsson J, Hollinger D, Kowalski AS, Katul G, Law BE, Malhi Y, Meyers T, Monson RK, Munger JW, Oechel W, Paw KT, Pilegaard K, Rannik U, Rebmann C, Suyker A, Valentini R, Wilson K, Wofsy S (2002) Seasonality of ecosystem respiration and gross primary production as derived from FLUXNET measurements. Agric For Meteorol 113:53–74
Finzi AC, Austin AT, Cleland EE, Frey SD, Houlton BZ, Wallenstein MD (2011) Responses and feedbacks of coupled biogeochemical cycles to climate change: examples from terrestrial ecosystems. Front Ecol Environ 9:61–67
Freeman C, Ostle N, Kang H (2001) An enzymic ‘latch’ on a global carbon store—a shortage of oxygen locks up carbon in peatlands by restraining a single enzyme. Nature 409:149
German DP, Chacon SS, Allison SD (2011) Substrate concentration and enzyme allocation can affect rates of microbial decomposition. Ecology 92:1471–1480
Henry HAL (2012) Soil extracellular enzyme dynamics in a changing climate. Soil Biol Biochem 47:53–59
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
Janssens IA, Dieleman W, Luyssaert S, Subke JA, Reichstein M, Ceulemans R, Ciais P, Dolman AJ, Grace J, Matteucci G, Papale D, Piao SL, Schulze ED, Tang J, Law BE (2010) Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci 3:315–322
Keuper F, Dorrepaal E, Van Bodegom P, Aerts R, van Logtestijn RSP, Callaghan TV, Cornelissen JHC (2011) A race for space? How Sphagnum fuscum stabilizes vegetation composition during long-term climate manipulations. Global Change Biol 17:2162–2171
Knicker H (2011) Soil organic N—an under-rated player for C sequestration in soils? Soil Biol Biochem 43:1118–1129
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 Cycles. doi:10.1029/2007GB002983
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379
Limpens J, Berendse F, Blodau C, Canadell JG, Freeman C, Holden J, Roulet N, Rydin H, Schaepman-Strub G (2008) Peatlands and the carbon cycle: from local processes to global implications—a synthesis. Biogeosciences 5:1475–1491
Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174
Moorhead DL, Lashermes G, Sinsabaugh RL (2012) A theoretical model of C- and N-acquiring exoenzyme activities, which balances microbial demands during decomposition. Soil Biol Biochem 53:133–141
Nannipieri P, Kandeler E, Ruggiero P (2002) Enzyme activities and microbiological and biochemical processes in soil. In: Burns RG, Dick RP (eds) Enzymes in the environment: activity, ecology and applications. Marcel Dekker, New York, pp 1–33
Rosswall T, Granhall U (1980) Nitrogen cycling in a subarctic ombrotrophic mire. Ecol Bulletins 30:209–234
Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J (2001) Gcte-news, a meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562
Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563
Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394
Schmidt SK, Costello EK, Nemergut DR, Cleveland CC, Reed SC, Weintraub MN, Meyer AF, Martin AM (2007) Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. Ecology 88:1379–1385
Schmidt MW, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kogel-Knabner I, Lehmann J, Manning DA, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56
Sinsabaugh RL, Foreman CM (2003) Integrating dissolved organic matter metabolism and microbial diversity: an overview of conceptual models. In: Findlay SEG, Sinsabaugh RL (eds) Aquatic ecosystems: interactivity of dissolved organic matter. Academic Press, New York
Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264
Sinsabaugh RL, Hill BH, Shah JJF (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795
Skujinš J (1976) Extracellular enzymes in soil. Crit Rev Microbiol 4:383–421
Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton
Todd-Brown KEO, Hopkins FM, Kivlin SN, Talbot JM, Allison SD (2012) A framework for representing microbial decomposition in coupled climate models. Biogeochemistry 109:19–33
Trasar-Cepeda C, Gil-Sotres F, Leiros MC (2007) Thermodynamic parameters of enzymes in grassland soils from Galicia, NW Spain. Soil Biol Biochem 39:311–319
Vicca S, Luyssaert S, Penuelas J, Campioli M, Chapin FS, Ciais P, Heinemeyer A, Hogberg P, Kutsch WL, Law BE, Malhi Y, Papale D, Piao SL, Reichstein M, Schulze ED, Janssens IA (2012) Fertile forests produce biomass more efficiently. Ecol Lett 15:520–526
Vitt DH (2006) Functional characteristics and indicators of boreal peatlands. In: Wieder RK, Vitt DH (eds) Boreal peatland ecosystems. Ecological studies. Springer-Verlag, Berlin
Wallenstein M, McMahon SK, Schimel JP (2009) Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Global Change Biol 15:1631–1639
Wallenstein M, Allison SD, Ernakovich J, Steinweg JM, Sinsabaugh RL (2011) Controls on the temperature sensitivity of soil enzymes: a key driver of in situ enzyme activity rates. In: Shukla G, Varma A (eds) Soil Enzymology. Springer-Verlag, Berlin
Weedon JT, Aerts R, Kowalchuk GA, van Bodegom PM (2011) Enzymology under global change: organic nitrogen turnover in alpine and sub-arctic soils. Biochem Soc Trans 39:309–314
Weedon JT, Kowalchuk GA, Aerts R, van Hal JR, van Logtestijn RKSP, Taş N, Röling WF, van Bodegom PM (2012) Summer warming accelerates sub-arctic peatland nitrogen cycling without changing enzyme pools or microbial community structure. Global Change Biol 18:138–150
Weedon JT, Aerts R, Kowalchuk G, van Logtestijn RkSP, Andringa D, van Bodegom P (2013) Temperature sensitivity of peatland C and N cycling: does substrate supply play a role? Soil Biol Biochem 69:109–120
Weintraub MN, Schimel JP (2005) Seasonal protein dynamics in Alaskan arctic tundra soils. Soil Biol Biochem 37:1469–1475
Acknowledgments
This study was financially supported by the Netherlands Organisation for Scientific Research (NWO) by NWO-ALW grant 816.01.012 to RA and GAK. We gratefully acknowledge the efforts of J.H.C. Cornelissen, R.S.P. van Logtestijn and E. Dorrepaal in establishing and maintaining the OTC experiment, thank R.S.P. van Logtestijn for field assistance, and J. Kamstra and P. Cenijn for access to the fluorometer. We also are grateful to Abisko Naturvetenskapliga Station for hosting us during fieldwork. The County Administrative Board at Luleå gave permission to perform the field experiments in Abisko National Park. Comments from anonymous reviewers allowed us to improve upon an earlier version of this manuscript.
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Weedon, J.T., Aerts, R., Kowalchuk, G.A. et al. No effects of experimental warming but contrasting seasonal patterns for soil peptidase and glycosidase enzymes in a sub-arctic peat bog. Biogeochemistry 117, 55–66 (2014). https://doi.org/10.1007/s10533-013-9870-0
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DOI: https://doi.org/10.1007/s10533-013-9870-0