Temperature sensitivity of extracellular enzymes differs with peat depth but not with season in an ombrotrophic bog
Abstract
Peatlands contain a large portion of Earth's terrestrial soil organic matter in part due to a reduction in decomposition rates. Organic matter decomposition is initially mediated by extracellular enzyme activity, which is in turn controlled by temperature, moisture, and substrate availability; and all are subject to seasonal variation. As depth increases in peatlands, temperature variability and labile carbon inputs decrease. We hypothesized that the more stable recalcitrant subsurface would contain a smaller less diverse enzyme pool, that is better adapted to a narrow temperature range. Thus temperature dependence would be diminished at depth compared to superficial peat. Potential enzyme activity rates were determined across seasons and with depth in peat samples collected from the Marcell Experimental Forest in northern Minnesota, USA. The temperature dependence, assessed by activation energy, was quantified for three hydrolytic enzymes involved in nutrient cycling at up to 15 temperature points ranging from 2 °C to 65 °C. Potential enzyme activity decreased with peat depth as expected and corresponded with changes in peat composition and microbial biomass from the acrotelm to the catotelm. In an environmentally relevant temperature range (2–23 °C), activation energy decreased with depth for β-glucosidase as predicted and leucine amino peptidase activation energy wasmore »
- Authors:
-
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Roanoke College, Salem, VA (United States)
- Georgia Inst. of Technology, Atlanta, GA (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1462891
- Alternate Identifier(s):
- OSTI ID: 1548003
- Grant/Contract Number:
- AC05-00OR22725; SC0012088
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Soil Biology and Biochemistry
- Additional Journal Information:
- Journal Volume: 125; Journal Issue: C; Journal ID: ISSN 0038-0717
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Peat depth; Extracellular enzyme activity; Decomposition; Nutrient cycling; Seasonality; Activation energy
Citation Formats
Steinweg, Jessica Megan, Kostka, Joel E., Hanson, Paul J., and Schadt, Christopher Warren. Temperature sensitivity of extracellular enzymes differs with peat depth but not with season in an ombrotrophic bog. United States: N. p., 2018.
Web. doi:10.1016/j.soilbio.2018.07.001.
Steinweg, Jessica Megan, Kostka, Joel E., Hanson, Paul J., & Schadt, Christopher Warren. Temperature sensitivity of extracellular enzymes differs with peat depth but not with season in an ombrotrophic bog. United States. https://doi.org/10.1016/j.soilbio.2018.07.001
Steinweg, Jessica Megan, Kostka, Joel E., Hanson, Paul J., and Schadt, Christopher Warren. Thu .
"Temperature sensitivity of extracellular enzymes differs with peat depth but not with season in an ombrotrophic bog". United States. https://doi.org/10.1016/j.soilbio.2018.07.001. https://www.osti.gov/servlets/purl/1462891.
@article{osti_1462891,
title = {Temperature sensitivity of extracellular enzymes differs with peat depth but not with season in an ombrotrophic bog},
author = {Steinweg, Jessica Megan and Kostka, Joel E. and Hanson, Paul J. and Schadt, Christopher Warren},
abstractNote = {Peatlands contain a large portion of Earth's terrestrial soil organic matter in part due to a reduction in decomposition rates. Organic matter decomposition is initially mediated by extracellular enzyme activity, which is in turn controlled by temperature, moisture, and substrate availability; and all are subject to seasonal variation. As depth increases in peatlands, temperature variability and labile carbon inputs decrease. We hypothesized that the more stable recalcitrant subsurface would contain a smaller less diverse enzyme pool, that is better adapted to a narrow temperature range. Thus temperature dependence would be diminished at depth compared to superficial peat. Potential enzyme activity rates were determined across seasons and with depth in peat samples collected from the Marcell Experimental Forest in northern Minnesota, USA. The temperature dependence, assessed by activation energy, was quantified for three hydrolytic enzymes involved in nutrient cycling at up to 15 temperature points ranging from 2 °C to 65 °C. Potential enzyme activity decreased with peat depth as expected and corresponded with changes in peat composition and microbial biomass from the acrotelm to the catotelm. In an environmentally relevant temperature range (2–23 °C), activation energy decreased with depth for β-glucosidase as predicted and leucine amino peptidase activation energy was the lowest of all enzymes. Stable temperatures at depth appear to result in a microbial community containing enzymes that have lower sensitivity to temperature increases. Surprisingly, there was no significant seasonal effect on enzyme temperature dependence observed in our study. Based on these results, and without shifts in microbial community composition, warming of peat could result in increased carbon and phosphorus cycling at the surface but little change at depth. As a result, differences in enzyme temperature sensitivity suggest nitrogen cycling could remain constant with warming, potentially resulting in proteolytic nitrogen cycling being decoupled from carbon and phosphorus cycling.},
doi = {10.1016/j.soilbio.2018.07.001},
journal = {Soil Biology and Biochemistry},
number = C,
volume = 125,
place = {United States},
year = {Thu Jul 26 00:00:00 EDT 2018},
month = {Thu Jul 26 00:00:00 EDT 2018}
}
Web of Science
Figures / Tables:
Works referenced in this record:
Responses of extracellular enzymes to simple and complex nutrient inputs
journal, May 2005
- Allison, Steven D.; Vitousek, Peter M.
- Soil Biology and Biochemistry, Vol. 37, Issue 5
Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes
journal, October 2006
- Allison, Steven D.
- Biogeochemistry, Vol. 81, Issue 3
Microbial communities in natural and disturbed peatlands: A review
journal, February 2013
- Andersen, R.; Chapman, S. J.; Artz, R. R. E.
- Soil Biology and Biochemistry, Vol. 57
High-throughput Fluorometric Measurement of Potential Soil Extracellular Enzyme Activities
journal, January 2013
- Bell, Colin W.; Fricks, Barbara E.; Rocca, Jennifer D.
- Journal of Visualized Experiments, Issue 81
Seasonal variation in the temperature sensitivity of proteolytic enzyme activity in temperate forest soils: TEMPERATURE SENSITIVITY OF PROTEOLYSIS
journal, February 2012
- Brzostek, Edward R.; Finzi, Adrien C.
- Journal of Geophysical Research: Biogeosciences, Vol. 117, Issue G1
Temperature response of denitrification and anaerobic ammonium oxidation rates and microbial community structure in Arctic fjord sediments: Temperature and N cycling in Arctic sediments
journal, September 2014
- Canion, Andy; Overholt, Will A.; Kostka, Joel E.
- Environmental Microbiology, Vol. 16, Issue 10
Response of plant community structure and primary productivity to experimental drought and flooding in an Alaskan fen
journal, February 2015
- Churchill, Amber C.; Turetsky, Merritt R.; McGuire, A. David
- Canadian Journal of Forest Research, Vol. 45, Issue 2
Carbon Accumulation in Peatland
journal, March 1998
- Clymo, R. S.; Turunen, J.; Tolonen, K.
- Oikos, Vol. 81, Issue 2
Temperature and soil organic matter decomposition rates - synthesis of current knowledge and a way forward
journal, August 2011
- Conant, Richard T.; Ryan, Michael G.; Ågren, Göran I.
- Global Change Biology, Vol. 17, Issue 11
Annual variations of phenoloxidase activities in an evergreen oak litter: influence of certain biotic and abiotic factors
journal, October 2000
- Criquet, S.; Farnet, A. M.; Tagger, S.
- Soil Biology and Biochemistry, Vol. 32, Issue 11-12
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
journal, June 2009
- DeForest, Jared L.
- Soil Biology and Biochemistry, Vol. 41, Issue 6
Effects of short-term drying and irrigation on CO2 and CH4 production and emission from mesocosms of a northern bog and an alpine fen
journal, February 2010
- Deppe, Marianna; Knorr, Klaus-H.; McKnight, Diane M.
- Biogeochemistry, Vol. 100, Issue 1-3
Effects of Short-Term Drying and Irrigation on Electron Flow in Mesocosms of a Northern Bog and an Alpine Fen
journal, November 2009
- Deppe, Marianna; McKnight, Diane M.; Blodau, Christian
- Environmental Science & Technology, Vol. 44, Issue 1
Soil organic matter turnover is governed by accessibility not recalcitrance
journal, March 2012
- Dungait, Jennifer A. J.; Hopkins, David W.; Gregory, Andrew S.
- Global Change Biology, Vol. 18, Issue 6
Methodologies for Extracellular Enzyme Assays from Wetland Soils
journal, August 2013
- Dunn, Christian; Jones, Timothy G.; Girard, Astrid
- Wetlands, Vol. 34, Issue 1
Hydrological effects on the diversity of phenolic degrading bacteria in a peatland: implications for carbon cycling
journal, July 2005
- Fenner, Nathalie; Freeman, Christopher; Reynolds, Brian
- Soil Biology and Biochemistry, Vol. 37, Issue 7
Observations of a seasonally shifting thermal optimum in peatland carbon-cycling processes; implications for the global carbon cycle and soil enzyme methodologies
journal, October 2005
- Fenner, N.; Freeman, C.; Reynolds, B.
- Soil Biology and Biochemistry, Vol. 37, Issue 10
The use of fluorogenic substrates for measuring enzyme activity in peatlands
journal, August 1995
- Freeman, C.; Liska, G.; Ostle, N. J.
- Plant and Soil, Vol. 175, Issue 1
Microbial activity and enzymic decomposition processes following peatland water table drawdown
journal, March 1996
- Freeman, C.; Liska, G.; Ostle, N. J.
- Plant and Soil, Vol. 180, Issue 1
An enzymic 'latch' on a global carbon store
journal, January 2001
- Freeman, Chris; Ostle, Nick; Kang, Hojeong
- Nature, Vol. 409, Issue 6817
Depth related diversity of methanogen Archaea in Finnish oligotrophic fen
journal, December 2002
- Galand, Pierre E.; Saarnio, Sanna; Fritze, Hannu
- FEMS Microbiology Ecology, Vol. 42, Issue 3
Temporal and Spatial Variation in Peatland Carbon Cycling and Implications for Interpreting Responses of an Ecosystem-Scale Warming Experiment
journal, January 2017
- Griffiths, Natalie A.; Hanson, Paul J.; Ricciuto, Daniel M.
- Soil Science Society of America Journal, Vol. 81, Issue 6
Attaining whole-ecosystem warming using air and deep-soil heating methods with an elevated CO 2 atmosphere
journal, January 2017
- Hanson, Paul J.; Riggs, Jeffery S.; Nettles, W. Robert
- Biogeosciences, Vol. 14, Issue 4
Fine-root growth in a forested bog is seasonally dynamic, but shallowly distributed in nutrient-poor peat
journal, March 2017
- Iversen, Colleen M.; Childs, Joanne; Norby, Richard J.
- Plant and Soil, Vol. 424, Issue 1-2, p. 123-143
Experimental climate effect on seasonal variability of polyphenol/phenoloxidase interplay along a narrow fen-bog ecological gradient in Sphagnum fallax: PHENOL/PHENOLOXIDASE INTERPLAY IN PEATLAND
journal, May 2011
- Jassey, Vincent E. J.; Chiapusio, GeneviÈVe; Gilbert, Daniel
- Global Change Biology, Vol. 17, Issue 9
Phenoloxidase and peroxidase activities in Sphagnum-dominated peatland in a warming climate
journal, March 2012
- Jassey, Vincent E. J.; Chiapusio, Geneviève; Gilbert, Daniel
- Soil Biology and Biochemistry, Vol. 46
Temperature sensitivity of microbial respiration, nitrogen mineralization, and potential soil enzyme activities in organic alpine soils: TEMPERATURE SENSITIVITY IN ALPINE SOILS
journal, December 2007
- Koch, Oliver; Tscherko, Dagmar; Kandeler, Ellen
- Global Biogeochemical Cycles, Vol. 21, Issue 4
Enzyme activities related to litter decomposition in forests of different age and altitude in North East India
journal, March 1992
- Kshattriya, S.; Sharma, G. D.; Mishra, R. R.
- Soil Biology and Biochemistry, Vol. 24, Issue 3
Changes in Soil Microbial Community Structure and Function in an Alpine Dry Meadow Following Spring Snow Melt
journal, May 2002
- Lipson, D. A.; Schadt, C. W.; Schmidt, S. K.
- Microbial Ecology, Vol. 43, Issue 3
Local Spatial Heterogeneity of Holocene Carbon Accumulation throughout the Peat Profile of an Ombrotrophic Northern Minnesota Bog
journal, May 2018
- McFarlane, Karis J.; Hanson, Paul J.; Iversen, Colleen M.
- Radiocarbon, Vol. 60, Issue 3
Temperature of upland and peatland soils in a north central Minnesota forest
journal, August 1998
- Nichols, Dale S.
- Canadian Journal of Soil Science, Vol. 78, Issue 3
Considerations in the storage of soil samples for enzyme activity analysis
journal, November 2012
- Peoples, Matthew S.; Koide, Roger T.
- Applied Soil Ecology, Vol. 62
Effect of clay minerals on the activity of polysaccharide cleaving soil enzymes
journal, January 1982
- Pflug, Werner
- Zeitschrift für Pflanzenernährung und Bodenkunde, Vol. 145, Issue 5
Temperature the dominant control on the enzyme-latch across a range of temperate peatland types
journal, June 2016
- Pinsonneault, Andrew J.; Moore, Tim R.; Roulet, Nigel T.
- Soil Biology and Biochemistry, Vol. 97
Understanding drivers of peatland extracellular enzyme activity in the PEATcosm experiment: mixed evidence for enzymic latch hypothesis
journal, December 2015
- Romanowicz, Karl J.; Kane, Evan S.; Potvin, Lynette R.
- Plant and Soil, Vol. 397, Issue 1-2
Seasonal Dynamics of Previously Unknown Fungal Lineages in Tundra Soils
journal, September 2003
- Schadt, C. W.
- Science, Vol. 301, Issue 5638
Microbial Stress-Response Physiology and its Implications for Ecosystem Function
journal, June 2007
- Schimel, Joshua; Balser, Teri C.; Wallenstein, Matthew
- Ecology, Vol. 88, Issue 6
Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment
journal, December 2009
- Sinsabaugh, Robert L.; Hill, Brian H.; Follstad Shah, Jennifer J.
- Nature, Vol. 462, Issue 7274
Resource allocation to extracellular enzyme production: A model for nitrogen and phosphorus control of litter decomposition
journal, October 1994
- Sinsabaugh, R. L.; Moorhead, D. L.
- Soil Biology and Biochemistry, Vol. 26, Issue 10
Microbial responses to multi-factor climate change: effects on soil enzymes
journal, January 2013
- Steinweg, J. Megan; Dukes, Jeffrey S.; Paul, Eldor A.
- Frontiers in Microbiology, Vol. 4
Activation Energy of Extracellular Enzymes in Soils from Different Biomes
journal, March 2013
- Steinweg, J. Megan; Jagadamma, Sindhu; Frerichs, Joshua
- PLoS ONE, Vol. 8, Issue 3
Modeling the effects of temperature and moisture on soil enzyme activity: Linking laboratory assays to continuous field data
journal, December 2012
- Steinweg, J. Megan; Dukes, Jeffrey S.; Wallenstein, Matthew D.
- Soil Biology and Biochemistry, Vol. 55
Snow removal alters soil microbial biomass and enzyme activity in a Tibetan alpine forest
journal, April 2014
- Tan, Bo; Wu, Fu-zhong; Yang, Wan-qin
- Applied Soil Ecology, Vol. 76
Thermodynamic parameters of enzymes in grassland soils from Galicia, NW Spain
journal, January 2007
- Trasar-Cepeda, C.; Gil-Sotres, F.; Leirós, M. C.
- Soil Biology and Biochemistry, Vol. 39, Issue 1
Trade-offs in resource allocation among moss species control decomposition in boreal peatlands
journal, November 2008
- Turetsky, Merritt R.; Crow, Susan E.; Evans, Robert J.
- Journal of Ecology, Vol. 96, Issue 6
Forest Harvesting and Water: the lake States Experience
journal, December 1986
- Veny, Elon S.
- Journal of the American Water Resources Association, Vol. 22, Issue 6
Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils
journal, July 2009
- Wallenstein, Matthew D.; Mcmahon, Shawna K.; Schimel, Joshua P.
- Global Change Biology, Vol. 15, Issue 7
Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes
journal, September 2008
- Wallenstein, Matthew D.; Weintraub, Michael N.
- Soil Biology and Biochemistry, Vol. 40, Issue 9
No effects of experimental warming but contrasting seasonal patterns for soil peptidase and glycosidase enzymes in a sub-arctic peat bog
journal, June 2013
- Weedon, James T.; Aerts, Rien; Kowalchuk, George A.
- Biogeochemistry, Vol. 117, Issue 1
Summer warming accelerates sub-arctic peatland nitrogen cycling without changing enzyme pools or microbial community structure
journal, October 2011
- T. Weedon, James; A. Kowalchuk, George; Aerts, Rien
- Global Change Biology, Vol. 18, Issue 1
The seasonal dynamics of amino acids and other nutrients in Alaskan Arctic tundra soils
journal, April 2005
- Weintraub, Michael N.; Schimel, Joshua P.
- Biogeochemistry, Vol. 73, Issue 2
Effects of soil warming and drying on methane cycling in a northern peatland mesocosm study
journal, January 2008
- White, Jeffrey R.; Shannon, Robert D.; Weltzin, Jake F.
- Journal of Geophysical Research, Vol. 113
Microbial diversity of Minnesota peatlands
journal, October 1983
- Williams, Richard T.; Crawford, Ronald L.
- Microbial Ecology, Vol. 9, Issue 3
Stability of peatland carbon to rising temperatures
journal, December 2016
- Wilson, R. M.; Hopple, A. M.; Tfaily, M. M.
- Nature Communications, Vol. 7, Article No. 13723
Substrate and environmental controls on microbial assimilation of soil organic carbon: a framework for Earth system models
journal, February 2014
- Xu, Xiaofeng; Schimel, Joshua P.; Thornton, Peter E.
- Ecology Letters, Vol. 17, Issue 5
Soil chemistry versus environmental controls on production of CH4 and CO2 in northern peatlands
journal, April 2005
- Yavitt, J. B.; Williams, C. J.; Wieder, R. K.
- European Journal of Soil Science, Vol. 56, Issue 2
Works referencing / citing this record:
Constraints on microbial communities, decomposition and methane production in deep peat deposits
journal, February 2020
- Kluber, Laurel A.; Johnston, Eric R.; Allen, Samantha A.
- PLOS ONE, Vol. 15, Issue 2
Warming changes soil N and P supplies in model tropical forests
journal, July 2019
- Lie, Zhiyang; Lin, Wei; Huang, Wenjuan
- Biology and Fertility of Soils, Vol. 55, Issue 7
Figures / Tables found in this record: