Constraints on microbial communities, decomposition and methane production in deep peat deposits
Abstract
Peatlands play outsized roles in the global carbon cycle. Despite occupying a rather small fraction of the terrestrial biosphere (~3%), these ecosystems account for roughly one third of the global soil carbon pool. This carbon is largely comprised of undecomposed deposits of plant material (peat) that may be meters thick. The fate of this deep carbon stockpile with ongoing and future climate change is thus of great interest and has large potential to induce positive feedback to climate warming. Recent in situ warming of an ombrotrophic peatland indicated that the deep peat microbial communities and decomposition rates were resistant to elevated temperatures. In this experiment, we sought to understand how nutrient and pH limitations may interact with temperature to limit microbial activity and community composition. Anaerobic microcosms of peat collected from 1.5 to 2 meters in depth were incubated at 6°C and 15°C with elevated pH, nitrogen (NH4Cl), and/or phosphorus (KH2PO4) in a full factorial design. The production of CO2 and CH4 was significantly greater in microcosms incubated at 15°C, although the structure of the microbial community did not differ between the two temperatures. Increasing the pH from ~3.5 to ~5.5 altered microbial community structure, however increases in CH4 productionmore »
- Authors:
- 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:
- 1598371
- Alternate Identifier(s):
- OSTI ID: 1607318
- Grant/Contract Number:
- 3ERKP788; AC05-00OR22725
- Resource Type:
- Published Article
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Name: PLoS ONE Journal Volume: 15 Journal Issue: 2; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; wetlands; community structure; carbon dioxide; Archaean biology; methanogenes; bogs; spruces; ribosomal RNA
Citation Formats
Kluber, Laurel A., Johnston, Eric R., Allen, Samantha A., Hendershot, J. Nicholas, Hanson, Paul J., Schadt, Christopher W., and Kang, ed., Hojeong. Constraints on microbial communities, decomposition and methane production in deep peat deposits. United States: N. p., 2020.
Web. doi:10.1371/journal.pone.0223744.
Kluber, Laurel A., Johnston, Eric R., Allen, Samantha A., Hendershot, J. Nicholas, Hanson, Paul J., Schadt, Christopher W., & Kang, ed., Hojeong. Constraints on microbial communities, decomposition and methane production in deep peat deposits. United States. https://doi.org/10.1371/journal.pone.0223744
Kluber, Laurel A., Johnston, Eric R., Allen, Samantha A., Hendershot, J. Nicholas, Hanson, Paul J., Schadt, Christopher W., and Kang, ed., Hojeong. Thu .
"Constraints on microbial communities, decomposition and methane production in deep peat deposits". United States. https://doi.org/10.1371/journal.pone.0223744.
@article{osti_1598371,
title = {Constraints on microbial communities, decomposition and methane production in deep peat deposits},
author = {Kluber, Laurel A. and Johnston, Eric R. and Allen, Samantha A. and Hendershot, J. Nicholas and Hanson, Paul J. and Schadt, Christopher W. and Kang, ed., Hojeong},
abstractNote = {Peatlands play outsized roles in the global carbon cycle. Despite occupying a rather small fraction of the terrestrial biosphere (~3%), these ecosystems account for roughly one third of the global soil carbon pool. This carbon is largely comprised of undecomposed deposits of plant material (peat) that may be meters thick. The fate of this deep carbon stockpile with ongoing and future climate change is thus of great interest and has large potential to induce positive feedback to climate warming. Recent in situ warming of an ombrotrophic peatland indicated that the deep peat microbial communities and decomposition rates were resistant to elevated temperatures. In this experiment, we sought to understand how nutrient and pH limitations may interact with temperature to limit microbial activity and community composition. Anaerobic microcosms of peat collected from 1.5 to 2 meters in depth were incubated at 6°C and 15°C with elevated pH, nitrogen (NH4Cl), and/or phosphorus (KH2PO4) in a full factorial design. The production of CO2 and CH4 was significantly greater in microcosms incubated at 15°C, although the structure of the microbial community did not differ between the two temperatures. Increasing the pH from ~3.5 to ~5.5 altered microbial community structure, however increases in CH4 production were non-significant. Contrary to expectations, N and P additions did not increase CO2 and CH4 production, indicating that nutrient availability was not a primary constraint in microbial decomposition of deep peat. Our findings indicate that temperature is a key factor limiting the decomposition of deep peat, however other factors such as the availability of O2 or alternative electron donors and high concentrations of phenolic compounds, may also exert constraints. Continued experimental peat warming studies will be necessary to assess if the deep peat carbon bank is susceptible to increased temperatures over the longer time scales.},
doi = {10.1371/journal.pone.0223744},
journal = {PLoS ONE},
number = 2,
volume = 15,
place = {United States},
year = {2020},
month = {2}
}
https://doi.org/10.1371/journal.pone.0223744
Works referenced in this record:
High sensitivity of peat decomposition to climate change through water-table feedback
journal, October 2008
- Ise, Takeshi; Dunn, Allison L.; Wofsy, Steven C.
- Nature Geoscience, Vol. 1, Issue 11
Temperature-Induced Increase in Methane Release from Peat Bogs: A Mesocosm Experiment
journal, June 2012
- van Winden, Julia F.; Reichart, Gert-Jan; McNamara, Niall P.
- PLoS ONE, Vol. 7, Issue 6
pH controls over anaerobic carbon mineralization, the efficiency of methane production, and methanogenic pathways in peatlands across an ombrotrophic–minerotrophic gradient
journal, November 2012
- Ye, Rongzhong; Jin, Qusheng; Bohannan, Brendan
- Soil Biology and Biochemistry, Vol. 54
The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate
journal, January 1992
- Raich, J. W.; Schlesinger, W. H.
- Tellus B: Chemical and Physical Meteorology, Vol. 44, Issue 2
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
Temperature sensitivity of soil respiration rates enhanced by microbial community response
journal, September 2014
- Karhu, Kristiina; Auffret, Marc D.; Dungait, Jennifer A. J.
- Nature, Vol. 513, Issue 7516
Stoichiometry and temperature sensitivity of methanogenesis and CO 2 production from saturated polygonal tundra in Barrow, Alaska
journal, November 2014
- Roy Chowdhury, Taniya; Herndon, Elizabeth M.; Phelps, Tommy J.
- Global Change Biology, Vol. 21, Issue 2
Cutadapt removes adapter sequences from high-throughput sequencing reads
journal, May 2011
- Martin, Marcel
- EMBnet.journal, Vol. 17, Issue 1
Soil carbon pools and world life zones
journal, July 1982
- Post, Wilfred M.; Emanuel, William R.; Zinke, Paul J.
- Nature, Vol. 298, Issue 5870
Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA.
journal, January 1993
- Muyzer, G.; de Waal, E. C.; Uitterlinden, A. G.
- Applied and Environmental Microbiology, Vol. 59, Issue 3
PyNAST: a flexible tool for aligning sequences to a template alignment
journal, November 2009
- Caporaso, J. G.; Bittinger, K.; Bushman, F. D.
- Bioinformatics, Vol. 26, Issue 2
Evidence for Anaerobic CH 4 Oxidation in Freshwater Peatlands
journal, December 2007
- Smemo, Kurt A.; Yavitt, Joseph B.
- Geomicrobiology Journal, Vol. 24, Issue 7-8
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
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
Acetoclastic and hydrogenotrophic methane production and methanogenic populations in an acidic West-Siberian peat bog
journal, November 2004
- Kotsyurbenko, Oleg R.; Chin, Kuk-Jeong; Glagolev, Mikhail V.
- Environmental Microbiology, Vol. 6, Issue 11
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea
journal, December 2011
- McDonald, Daniel; Price, Morgan N.; Goodrich, Julia
- The ISME Journal, Vol. 6, Issue 3
Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing
journal, December 2012
- Bokulich, Nicholas A.; Subramanian, Sathish; Faith, Jeremiah J.
- Nature Methods, Vol. 10, Issue 1
Global prevalence of methane oxidation by symbiotic bacteria in peat-moss ecosystems
journal, August 2010
- Kip, Nardy; van Winden, Julia F.; Pan, Yao
- Nature Geoscience, Vol. 3, Issue 9
Microbial Community Stratification Linked to Utilization of Carbohydrates and Phosphorus Limitation in a Boreal Peatland at Marcell Experimental Forest, Minnesota, USA
journal, March 2014
- Lin, Xueju; Tfaily, Malak M.; Steinweg, J. Megan
- Applied and Environmental Microbiology, Vol. 80, Issue 11
Ecoenzymatic stoichiometry and microbial processing of organic matter in northern bogs and fens reveals a common P-limitation between peatland types
journal, May 2014
- Hill, Brian H.; Elonen, Colleen M.; Jicha, Terri M.
- Biogeochemistry, Vol. 120, Issue 1-3
A pan-Arctic synthesis of CH 4 and CO 2 production from anoxic soil incubations
journal, March 2015
- Treat, Claire C.; Natali, Susan M.; Ernakovich, Jessica
- Global Change Biology, Vol. 21, Issue 7
Nitrogen Deposition Effects on Carbon Dioxide and Methane Emissions from Temperate Peatland Soils
journal, January 1999
- Aerts, Rien; de Caluwe, Hannie
- Oikos, Vol. 84, Issue 1
Practical innovations for high-throughput amplicon sequencing
journal, September 2013
- Lundberg, Derek S.; Yourstone, Scott; Mieczkowski, Piotr
- Nature Methods, Vol. 10, Issue 10
Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale
journal, June 2009
- Lauber, C. L.; Hamady, M.; Knight, R.
- Applied and Environmental Microbiology, Vol. 75, Issue 15
Anaerobic Oxidization of Methane in a Minerotrophic Peatland: Enrichment of Nitrite-Dependent Methane-Oxidizing Bacteria
journal, October 2012
- Zhu, Baoli; van Dijk, Gijs; Fritz, Christian
- Applied and Environmental Microbiology, Vol. 78, Issue 24
Peatland succession induces a shift in the community composition of Sphagnum -associated active methanotrophs
journal, April 2014
- Putkinen, Anuliina; Larmola, Tuula; Tuomivirta, Tero
- FEMS Microbiology Ecology, Vol. 88, Issue 3
Long-term warming alters the composition of Arctic soil microbial communities
journal, April 2012
- Deslippe, Julie R.; Hartmann, Martin; Simard, Suzanne W.
- FEMS Microbiology Ecology, Vol. 82, Issue 2
Nitrogen supply differentially affects litter decomposition rates and nitrogen dynamics of sub-arctic bog species
journal, September 2005
- Aerts, R.; Logtestijn, R. S. P. van; Karlsson, P. S.
- Oecologia, Vol. 146, Issue 4
Compositional and Functional Shifts in Microbial Communities Due to Soil Warming
journal, January 1997
- Zogg, Gregory P.; Zak, Donald R.; Ringelberg, David B.
- Soil Science Society of America Journal, Vol. 61, Issue 2
Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world
journal, October 2017
- Melillo, J. M.; Frey, S. D.; DeAngelis, K. M.
- Science, Vol. 358, Issue 6359
Methane Production in Minnesota Peatlands
journal, January 1984
- Williams, Richard T.; Crawford, Ronald L.
- Applied and Environmental Microbiology, Vol. 47, Issue 6
Patterns and Processes of Microbial Community Assembly
journal, September 2013
- Nemergut, D. R.; Schmidt, S. K.; Fukami, T.
- Microbiology and Molecular Biology Reviews, Vol. 77, Issue 3
Microbial Metabolic Potential for Carbon Degradation and Nutrient (Nitrogen and Phosphorus) Acquisition in an Ombrotrophic Peatland
journal, March 2014
- Lin, Xueju; Tfaily, Malak M.; Green, Stefan J.
- Applied and Environmental Microbiology, Vol. 80, Issue 11
UPARSE: highly accurate OTU sequences from microbial amplicon reads
journal, August 2013
- Edgar, Robert C.
- Nature Methods, Vol. 10, Issue 10
Intermediate-scale community-level flux of CO2 and CH4 in a Minnesota peatland: putting the SPRUCE project in a global context
journal, August 2016
- Hanson, P. J.; Gill, A. L.; Xu, X.
- Biogeochemistry, Vol. 129, Issue 3, p. 255-272
Ammonia inhibition in anaerobic digestion: A review
journal, May 2013
- Yenigün, Orhan; Demirel, Burak
- Process Biochemistry, Vol. 48, Issue 5-6
High rates of anaerobic methane oxidation in freshwater wetlands reduce potential atmospheric methane emissions
journal, June 2015
- Segarra, K. E. A.; Schubotz, F.; Samarkin, V.
- Nature Communications, Vol. 6, Issue 1
Anaerobic oxidation of methane: an underappreciated aspect of methane cycling in peatland ecosystems?
journal, January 2011
- Smemo, K. A.; Yavitt, J. B.
- Biogeosciences, Vol. 8, Issue 3
Microbial Community Structure and Activity Linked to Contrasting Biogeochemical Gradients in Bog and Fen Environments of the Glacial Lake Agassiz Peatland
journal, July 2012
- Lin, X.; Green, S.; Tfaily, M. M.
- Applied and Environmental Microbiology, Vol. 78, Issue 19
Temperature sensitivity of extracellular enzymes differs with peat depth but not with season in an ombrotrophic bog
journal, October 2018
- Steinweg, J. Megan; Kostka, Joel E.; Hanson, Paul J.
- Soil Biology and Biochemistry, Vol. 125
A meta-analysis of responses of soil biota to global change
journal, January 2011
- Blankinship, Joseph C.; Niklaus, Pascal A.; Hungate, Bruce A.
- Oecologia, Vol. 165, Issue 3
Responses of tundra soil microbial communities to half a decade of experimental warming at two critical depths
journal, July 2019
- Johnston, Eric R.; Hatt, Janet K.; He, Zhili
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 30
Using 13C isotopes to explore denitrification-dependent anaerobic methane oxidation in a paddy-peatland
journal, January 2017
- Shi, Yao; Wang, Zhongqiang; He, Chunguang
- Scientific Reports, Vol. 7, Issue 1
Nutrient limitations on microbial respiration in peat soils with different total phosphorus content
journal, June 1993
- Amador, JoséA.; Jones, Ronald D.
- Soil Biology and Biochemistry, Vol. 25, Issue 6
The Biological Observation Matrix (BIOM) format or: how I learned to stop worrying and love the ome-ome
journal, July 2012
- McDonald, Daniel; Clemente, Jose C.; Kuczynski, Justin
- GigaScience, Vol. 1, Issue 1
Tropical peatland carbon storage linked to global latitudinal trends in peat recalcitrance
journal, September 2018
- Hodgkins, Suzanne B.; Richardson, Curtis J.; Dommain, René
- Nature Communications, Vol. 9, Issue 1
Archaeal rRNA diversity and methane production in deep boreal peat: Archaeal rRNA in deep boreal peat
journal, October 2009
- Putkinen, Anuliina; Juottonen, Heli; Juutinen, Sari
- FEMS Microbiology Ecology, Vol. 70, Issue 1
QIIME allows analysis of high-throughput community sequencing data
journal, April 2010
- Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
- Nature Methods, Vol. 7, Issue 5
Control of carbon mineralization to CH4 and CO2 in anaerobic,Sphagnum-derived peat from Big Run Bog, West Virginia
journal, June 1987
- Yavitt, Joseph B.; Lang, Gerald E.; Wieder, R. Kelman
- Biogeochemistry, Vol. 4, Issue 2
Ecophysiological adaptations of anaerobic bacteria to low pH: analysis of anaerobic digestion in acidic bog sediments.
journal, January 1987
- Goodwin, S.; Zeikus, J. G.
- Applied and Environmental Microbiology, Vol. 53, Issue 1
The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome
journal, February 2018
- Cregger, M. A.; Veach, A. M.; Yang, Z. K.
- Microbiome, Vol. 6, Issue 1
Long-term forest soil warming alters microbial communities in temperate forest soils
journal, February 2015
- DeAngelis, Kristen M.; Pold, Grace; Topçuoğlu, Begüm D.
- Frontiers in Microbiology, Vol. 6
Litter quality versus soil microbial community controls over decomposition: a quantitative analysis
journal, September 2013
- Cleveland, Cory C.; Reed, Sasha C.; Keller, Adrienne B.
- Oecologia, Vol. 174, Issue 1
Changes in bacterial and archaeal community assemblages along an ombrotrophic peat bog profile
journal, January 2014
- Puglisi, Edoardo; Zaccone, Claudio; Cappa, Fabrizio
- Biology and Fertility of Soils, Vol. 50, Issue 5
Present state of global wetland extent and wetland methane modelling: conclusions from a model inter-comparison project (WETCHIMP)
journal, January 2013
- Melton, J. R.; Wania, R.; Hodson, E. L.
- Biogeosciences, Vol. 10, Issue 2
Rapid loss of an ecosystem engineer: Sphagnum decline in an experimentally warmed bog
journal, October 2019
- Norby, Richard J.; Childs, Joanne; Hanson, Paul J.
- Ecology and Evolution, Vol. 9, Issue 22
The diversity and biogeography of soil bacterial communities
journal, January 2006
- Fierer, N.; Jackson, R. B.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 3
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix
journal, April 2009
- Price, M. N.; Dehal, P. S.; Arkin, A. P.
- Molecular Biology and Evolution, Vol. 26, Issue 7
Atmospheric nitrogen deposition promotes carbon loss from peat bogs
journal, December 2006
- Bragazza, L.; Freeman, C.; Jones, T.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 51
Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction
journal, January 2005
- Yu, Youngseob; Lee, Changsoo; Kim, Jaai
- Biotechnology and Bioengineering, Vol. 89, Issue 6
Inhibition of anaerobic digestion process: A review
journal, July 2008
- Chen, Ye; Cheng, Jay J.; Creamer, Kurt S.
- Bioresource Technology, Vol. 99, Issue 10
Estimating carbon accumulation rates of undrained mires in Finland–application to boreal and subarctic regions
journal, January 2002
- Turunen, Jukka; Tomppo, Erkki; Tolonen, Kimmo
- The Holocene, Vol. 12, Issue 1
Dynamic Vertical Profiles of Peat Porewater Chemistry in a Northern Peatland
journal, October 2016
- Griffiths, Natalie A.; Sebestyen, Stephen D.
- Wetlands, Vol. 36, Issue 6, p. 1119-1130
Patterns of Change in the Carbon Balance of Organic Soil-Wetlands of the Temperate Zone
journal, September 1986
- Armentano, T. V.; Menges, E. S.
- The Journal of Ecology, Vol. 74, Issue 3
Impact of training sets on classification of high-throughput bacterial 16s rRNA gene surveys
journal, June 2011
- Werner, Jeffrey J.; Koren, Omry; Hugenholtz, Philip
- The ISME Journal, Vol. 6, Issue 1
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
journal, December 2005
- Lozupone, C.; Knight, R.
- Applied and Environmental Microbiology, Vol. 71, Issue 12
Carbon respiration from subsurface peat accelerated by climate warming in the subarctic
journal, July 2009
- Dorrepaal, Ellen; Toet, Sylvia; van Logtestijn, Richard S. P.
- Nature, Vol. 460, Issue 7255
Dynamics of Soil Carbon During Deglaciation of the Laurentide Ice Sheet
journal, December 1992
- Harden, J. W.; Mark, R. K.; Sundquist, E. T.
- Science, Vol. 258, Issue 5090
Effects of nutrient addition on vegetation and carbon cycling in an ombrotrophic bog
journal, June 2007
- Bubier, Jill L.; Moore, Tim R.; Bledzki, Leszek A.
- Global Change Biology, Vol. 13, Issue 6
Organic matter transformation in the peat column at Marcell Experimental Forest: Humification and vertical stratification: Organic matter dynamics
journal, April 2014
- Tfaily, Malak M.; Cooper, William T.; Kostka, Joel E.
- Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 4
Nutritional controls on carbon dioxide and methane emission from Carex-dominated peat soils
journal, November 1997
- Aerts, Rien; Toet, Sylvia
- Soil Biology and Biochemistry, Vol. 29, Issue 11-12
A most beautiful polar low. A case study of a polar low development in the Bear Island region
journal, March 1992
- Nordeng, Thor Erik; Rasmussen, Erik A.
- Tellus A, Vol. 44, Issue 2
The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill b
journal, November 2002
- Luton, Philip E.; Wayne, Jonathan M.; Sharp, Richard J.
- Microbiology, Vol. 148, Issue 11
Links between methane flux and transcriptional activities of methanogens and methane oxidizers in a blanket peat bog: Methane flux and transcriptional activities in a peat bog
journal, March 2010
- Freitag, Thomas E.; Toet, Sylvia; Ineson, Phil
- FEMS Microbiology Ecology
The Sphagnum microbiome: new insights from an ancient plant lineage
journal, February 2016
- Kostka, Joel E.; Weston, David J.; Glass, Jennifer B.
- New Phytologist, Vol. 211, Issue 1
The carbon balance of North American wetlands
journal, December 2006
- Bridgham, Scott D.; Megonigal, J. Patrick; Keller, Jason K.
- Wetlands, Vol. 26, Issue 4
Northern Peatlands: Role in the Carbon Cycle and Probable Responses to Climatic Warming
journal, May 1991
- Gorham, Eville
- Ecological Applications, Vol. 1, Issue 2
SPRUCE Peat Physical and Chemical Characteristics from Experimental Plot Cores, 2012
dataset, January 2014
- Iversen, C.; Hanson, P.; Brice, D.
- SPRUCE (Spruce and Peatland Responses Under Changing Environments)
SPRUCE Deep Peat Heating (DPH) Peat Water Content and Temperature Profiles for Experimental Plot Cores, June 2014 through June 2015
dataset, January 2016
- Kluber, Lauren; Phillips, Jana; Hanson, Paul
- ORNLTESSFA (Oak Ridge National Lab's Terrestrial Ecosystem Science Scientific Focus Area (ORNL TES SFA))