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Title: 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 » 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.« less

Authors:
 [1];  [2]; ORCiD logo [3]; ORCiD logo [4]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Roanoke College, Salem, VA (United States)
  2. Georgia Inst. of Technology, Atlanta, GA (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. 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}
}

Journal Article:

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Cited by: 16 works
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Figures / Tables:

Table 1 Table 1: Extracellular enzymes assayed and their role in microbial nutrient acquisition.

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Works referenced in this record:

Responses of extracellular enzymes to simple and complex nutrient inputs
journal, May 2005


Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes
journal, October 2006


Microbial communities in natural and disturbed peatlands: A review
journal, February 2013


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
  • DOI: 10.3791/50961

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
  • DOI: 10.1029/2011JG001688

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
  • DOI: 10.1139/cjfr-2014-0100

Carbon Accumulation in Peatland
journal, March 1998

  • Clymo, R. S.; Turunen, J.; Tolonen, K.
  • Oikos, Vol. 81, Issue 2
  • DOI: 10.2307/3547057

Temperature and soil organic matter decomposition rates - synthesis of current knowledge and a way forward
journal, August 2011


Annual variations of phenoloxidase activities in an evergreen oak litter: influence of certain biotic and abiotic factors
journal, October 2000


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


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
  • DOI: 10.1021/es901669z

Soil organic matter turnover is governed by accessibility not recalcitrance
journal, March 2012


Methodologies for Extracellular Enzyme Assays from Wetland Soils
journal, August 2013


Hydrological effects on the diversity of phenolic degrading bacteria in a peatland: implications for carbon cycling
journal, July 2005


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
  • DOI: 10.1007/BF02413020

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
  • DOI: 10.1007/BF00015418

An enzymic 'latch' on a global carbon store
journal, January 2001

  • Freeman, Chris; Ostle, Nick; Kang, Hojeong
  • Nature, Vol. 409, Issue 6817
  • DOI: 10.1038/35051650

Depth related diversity of methanogen Archaea in Finnish oligotrophic fen
journal, December 2002


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
  • DOI: 10.2136/sssaj2016.12.0422

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
  • DOI: 10.5194/bg-14-861-2017

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
  • DOI: 10.1007/s11104-017-3231-z

Phenoloxidase and peroxidase activities in Sphagnum-dominated peatland in a warming climate
journal, March 2012


Enzyme activities related to litter decomposition in forests of different age and altitude in North East India
journal, March 1992


Changes in Soil Microbial Community Structure and Function in an Alpine Dry Meadow Following Spring Snow Melt
journal, May 2002


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
  • DOI: 10.1017/RDC.2018.37

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
  • DOI: 10.4141/S96-030

Considerations in the storage of soil samples for enzyme activity analysis
journal, November 2012


Effect of clay minerals on the activity of polysaccharide cleaving soil enzymes
journal, January 1982


Temperature the dominant control on the enzyme-latch across a range of temperate peatland types
journal, June 2016


Understanding drivers of peatland extracellular enzyme activity in the PEATcosm experiment: mixed evidence for enzymic latch hypothesis
journal, December 2015


Seasonal Dynamics of Previously Unknown Fungal Lineages in Tundra Soils
journal, September 2003


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
  • DOI: 10.1890/06-0219

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
  • DOI: 10.1038/nature08632

Resource allocation to extracellular enzyme production: A model for nitrogen and phosphorus control of litter decomposition
journal, October 1994


Microbial responses to multi-factor climate change: effects on soil enzymes
journal, January 2013


Activation Energy of Extracellular Enzymes in Soils from Different Biomes
journal, March 2013


Modeling the effects of temperature and moisture on soil enzyme activity: Linking laboratory assays to continuous field data
journal, December 2012


Snow removal alters soil microbial biomass and enzyme activity in a Tibetan alpine forest
journal, April 2014


Thermodynamic parameters of enzymes in grassland soils from Galicia, NW Spain
journal, January 2007


Trade-offs in resource allocation among moss species control decomposition in boreal peatlands
journal, November 2008


Forest Harvesting and Water: the lake States Experience
journal, December 1986


Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils
journal, July 2009


Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes
journal, September 2008


No effects of experimental warming but contrasting seasonal patterns for soil peptidase and glycosidase enzymes in a sub-arctic peat bog
journal, June 2013


Summer warming accelerates sub-arctic peatland nitrogen cycling without changing enzyme pools or microbial community structure
journal, October 2011


The seasonal dynamics of amino acids and other nutrients in Alaskan Arctic tundra soils
journal, April 2005


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
  • DOI: 10.1029/2007JG000609

Microbial diversity of Minnesota peatlands
journal, October 1983

  • Williams, Richard T.; Crawford, Ronald L.
  • Microbial Ecology, Vol. 9, Issue 3
  • DOI: 10.1007/BF02097737

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
  • DOI: 10.1038/ncomms13723

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
  • DOI: 10.1111/ele.12254

Soil chemistry versus environmental controls on production of CH4 and CO2 in northern peatlands
journal, April 2005


Works referencing / citing this record:

Constraints on microbial communities, decomposition and methane production in deep peat deposits
journal, February 2020


Warming changes soil N and P supplies in model tropical forests
journal, July 2019


Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.