Seasonal variation in the temperature sensitivity of proteolytic enzyme activity in temperate forest soils

[1] Increasing soil temperature has the potential to alter the activity of the extracellular enzymes that mobilize nitrogen (N) from soil organic matter (SOM) and ultimately the availability of N for primary production. Proteolytic enzymes depolymerize N from proteinaceous components of SOM into amino acids, and their activity is a principal driver of the within-system cycle of soil N. The objectives of this study were to investigate whether the soils of temperate forest tree species differ in the temperature sensitivity of proteolytic enzyme activity over the growing season and the role of substrate limitation in regulating temperature sensitivity. Across species and sampling dates, proteolytic enzyme activity had relatively low sensitivity to temperature with a mean activation energy (Ea) of 33.5 kJ mol−1. Ea declined in white ash, American beech, and eastern hemlock soils across the growing season as soils warmed. By contrast, Eain sugar maple soil increased across the growing season. We used these data to develop a species-specific empirical model of proteolytic enzyme activity for the 2009 calendar year and studied the interactive effects of soil temperature (ambient or +5°C) and substrate limitation (ambient or elevated protein) on enzyme activity. Declines in substrate limitation had a larger single-factor effect on proteolytic enzyme activity than temperature, particularly in the spring. There was, however, a large synergistic effect of increasing temperature and substrate supply on proteolytic enzyme activity. Our results suggest limited increases in N availability with climate warming unless there is a parallel increase in the availability of protein substrates.

[1]  E. Davidson,et al.  The Dual Arrhenius and Michaelis–Menten kinetics model for decomposition of soil organic matter at hourly to seasonal time scales , 2012 .

[2]  A. J. Dolman,et al.  Spatial and temporal dynamics in eddy covariance observations of methane fluxes at a tundra site in Northeastern Siberia , 2011 .

[3]  S. Allison,et al.  Substrate concentration and enzyme allocation can affect rates of microbial decomposition. , 2011, Ecology.

[4]  E. Brzostek,et al.  Substrate supply, fine roots, and temperature control proteolytic enzyme activity in temperate forest soils. , 2011, Ecology.

[5]  N. Fierer,et al.  Widespread coupling between the rate and temperature sensitivity of organic matter decay , 2010 .

[6]  C. Drury,et al.  Temperature dependence of soil nitrogen mineralization rate: Comparison of mathematical models, reference temperatures and origin of the soils , 2010 .

[7]  S. Hobbie,et al.  The effects of substrate composition, quantity, and diversity on microbial activity , 2010, Plant and Soil.

[8]  Mark A. Bradford,et al.  Soil-carbon response to warming dependent on microbial physiology , 2010 .

[9]  M. Bradford,et al.  Thermal adaptation of heterotrophic soil respiration in laboratory microcosms , 2010 .

[10]  Benjamin P Colman,et al.  Amino acid abundance and proteolytic potential in North American soils , 2010, Oecologia.

[11]  Pierre Friedlingstein,et al.  Terrestrial nitrogen feedbacks may accelerate future climate change , 2010 .

[12]  J. Randerson,et al.  Carbon-nitrogen interactions regulate climate-carbon cycle feedbacks: results from an atmosphere-ocean general circulation model , 2009 .

[13]  J. Schimel,et al.  Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils , 2009 .

[14]  Vikki L. Rodgers,et al.  Intact amino acid uptake by northern hardwood and conifer trees , 2009, Oecologia.

[15]  S. Allison,et al.  Low levels of nitrogen addition stimulate decomposition by boreal forest fungi , 2009 .

[16]  D. Rothstein.  Soil amino-acid availability across a temperate-forest fertility gradient , 2009 .

[17]  W. Horwath,et al.  Regulation of extracellular protease activity in soil in response to different sources and concentrations of nitrogen and carbon. , 2008 .

[18]  E. Perfect,et al.  Protection of organic carbon in soil microaggregates via restructuring of aggregate porosity and filling of pores with accumulating organic matter , 2008 .

[19]  David L. Jones,et al.  Critical evaluation of methods for determining total protein in soil solution , 2008 .

[20]  A. Finzi,et al.  Differential effects of sugar maple, red oak, and hemlock tannins on carbon and nitrogen cycling in temperate forest soils , 2008, Oecologia.

[21]  E. Kandeler,et al.  Temperature sensitivity of microbial respiration, nitrogen mineralization, and potential soil enzyme activities in organic alpine soils , 2007 .

[22]  R. B. Jackson,et al.  Effects of elevated atmospheric carbon dioxide on amino acid and NH4+‐N cycling in a temperate pine ecosystem , 2007 .

[23]  R. Bradley,et al.  Soil enzyme inhibition by condensed litter tannins may drive ecosystem structure and processes: the case of Kalmia angustifolia. , 2007, The New phytologist.

[24]  U. Feller,et al.  Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. , 2007, Journal of experimental botany.

[25]  S. Wofsy,et al.  Factors controlling CO2 exchange on timescales from hourly to decadal at Harvard Forest , 2007 .

[26]  H. Wösten,et al.  Role of proteins in soil carbon and nitrogen storage: controls on persistence , 2007 .

[27]  P. Sollins,et al.  Organic C and N stabilization in a forest soil: Evidence from sequential density fractionation , 2006 .

[28]  Noah Fierer,et al.  Predicting the temperature dependence of microbial respiration in soil: A continental‐scale analysis , 2006 .

[29]  Ricardo Cavicchioli,et al.  Cold-adapted enzymes. , 2006, Annual review of biochemistry.

[30]  A. Finzi,et al.  Amino Acid Cycling in Three Cold-Temperate Forests of the Northeastern USA , 2006 .

[31]  E. Davidson,et al.  Temperature sensitivity of soil carbon decomposition and feedbacks to climate change , 2006, Nature.

[32]  A. Finzi,et al.  THE UPTAKE OF AMINO ACIDS BY MICROBES AND TREES IN THREE COLD‐TEMPERATE FORESTS , 2005 .

[33]  C. Freeman,et al.  Observations of a seasonally shifting thermal optimum in peatland carbon-cycling processes; implications for the global carbon cycle and soil enzyme methodologies , 2005 .

[34]  J. Schimel,et al.  Seasonal protein dynamics in Alaskan arctic tundra soils , 2005 .

[35]  J. Schimel,et al.  NITROGEN MINERALIZATION: CHALLENGES OF A CHANGING PARADIGM , 2004 .

[36]  K. Weathers,et al.  Nitrogen cycling in a northern hardwood forest: Do species matter? , 2004 .

[37]  W. Bowman,et al.  Litter effects of two co-occurring alpine species on plant growth, microbial activity and immobilization of nitrogen , 2004 .

[38]  R. Dahlgren,et al.  Tannins in nutrient dynamics of forest ecosystems - a review , 2003, Plant and Soil.

[39]  R. Dahlgren,et al.  Linking Chemical Reactivity and Protein Precipitation to Structural Characteristics of Foliar Tannins , 2003, Journal of Chemical Ecology.

[40]  Jerry M. Melillo,et al.  Soil Warming and Carbon-Cycle Feedbacks to the Climate System , 2002, Science.

[41]  David L. Jones,et al.  Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts , 2002 .

[42]  Joshua P. Schimel,et al.  Temperature controls of microbial respiration in arctic tundra soils above and below freezing , 2002 .

[43]  R. Monson,et al.  An empirical model of amino acid transformations in an alpine soil , 2001 .

[44]  R. Monson,et al.  LINKS BETWEEN MICROBIAL POPULATION DYNAMICS AND NITROGEN AVAILABILITY IN AN ALPINE ECOSYSTEM , 1999 .

[45]  K. Pregitzer,et al.  Soil temperature, matric potential, and the kinetics of microbial respiration and nitrogen mineralization , 1999 .

[46]  Charles D. Canham,et al.  CANOPY TREE–SOIL INTERACTIONS WITHIN TEMPERATE FORESTS: SPECIES EFFECTS ON SOIL CARBON AND NITROGEN , 1998 .

[47]  H. Schulten,et al.  The chemistry of soil organic nitrogen: a review , 1997, Biology and Fertility of Soils.

[48]  K. Hayano,et al.  Seasonal variation of soil protease activities and their relation to proteolytic bacteria and Bacillus spp in paddy field soil , 1995 .

[49]  M. Tabatabai,et al.  Cellulase activity of soils , 1994 .

[50]  David R. Foster,et al.  Land-Use History (1730-1990) and Vegetation Dynamics in Central New England, USA , 1992 .

[51]  Gordon B. Bonan,et al.  Soil temperature, nitrogen mineralization, and carbon source–sink relationships in boreal forests , 1992 .

[52]  David R. Foster,et al.  Disturbance history, community organization and vegetation dynamics of the old-growth pisgah forest, South-Western New Hampshire, U.S.A , 1988 .

[53]  G. Somero,et al.  Temperature Adaptation of Enzymes: Biological Optimization Through Structure-Function Compromises , 1978 .

[54]  Svante Arrhenius,et al.  Über die Reaktionsgeschwindigkeit bei der Inversion von Rohrzucker durch Säuren , 1889 .

[55]  M. Mack,et al.  Kinetic studies of proteolytic enzyme activity of arctic soils under varying toluene concentrations , 2011 .

[56]  J. Melillo,et al.  MIT Joint Program on the Science and Policy of Global Change Consequences of Considering Carbon / Nitrogen Interactions on the Feedbacks between Climate and the Terrestrial Carbon Cycle , 2007 .

[57]  D. Barraclough.  The direct or MIT route for nitrogen immobilization: A 15N mirror image study with leucine and glycine , 1997 .

[58]  L. Landi,et al.  Determination of extracellular neutral phosphomonoesterase activity in soil , 1996 .

[59]  W. Frankenberger,et al.  Use of plasmolytic agents and antiseptics in soil enzyme assays , 1986 .