Search Menu
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information
Search Scholarly Publications

Title: Microbial Community Analyses Inform Geochemical Reaction Network Models for Predicting Pathways of Greenhouse Gas Production

Abstract

The mechanisms, pathways, and rates of CO2 and CH4 production are central to understanding carbon cycling and greenhouse gas flux in wetlands. Thawing permafrost regions are of particular interest because they are disproportionally affected by climate warming and store large reservoirs of organic C that may be readily converted to CO2 and CH4 upon thaw. This conversion is accomplished by a community of microorganisms interacting in complex ways to transform large organic compounds into fatty acids and ultimately CO2 and CH4. While the central role of microbes in this process is well-known, geochemical rate models rarely integrate microbiological information. With this, we expanded the geochemical rate model of Neumann et al., (2016, Biogeochemistry 127: 57–87) to incorporate a Bayesian probability analysis and applied the result to quantifying rates of CO2, CH4, and acetate production in closed-system incubations of peat collected from three habitats along a permafrost thaw gradient. The goals of this analysis were twofold. First, we integrated microbial community analyses with geochemical rate modeling by using microbial data to inform the best model choice among equally mathematically feasible model variants. Second, based on model results, we described changes in organic carbon transformation among habitats to understand the changing pathwaysmore » of greenhouse gas production along the permafrost thaw gradient. We found that acetoclasty, hydrogenotrophy, CO2 production, and homoacetogenesis were the important reactions in this system, with little evidence for anaerobic CH4 oxidation. There was a distinct transition in the reactions across the thaw gradient. The collapsed palsa stage presents an initial disequilibrium where the abrupt (physically and temporally) change in elevation introduces freshly fixed carbon into anoxic conditions then fermentation products build up over time as the system transitions through the acid phase and electron acceptors are depleted. In the bog, fermentation slows, while methanogenesis increases. In the fully thawed fen, most of the terminal electron acceptors are depleted and the system becomes increasingly methanogenic. This suggests that as permafrost regions thaw and dry palsas transition into wet fens, CH4 emissions will rise, increasing the warming potential of these systems and accelerating climate warming feedbacks.« less

Authors:
; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Univ. of Arizona, Tucson, AZ (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division
OSTI Identifier:
1504282
Alternate Identifier(s):
OSTI ID: 1506088
Grant/Contract Number:  
SC- 0010338; SC0010580; SC0016440; AC02-05CH11231; AC05-76RL01830; SC0010338
Resource Type:
Published Article
Journal Name:
Frontiers in Earth Science
Additional Journal Information:
Journal Name: Frontiers in Earth Science Journal Volume: 7; Journal ID: ISSN 2296-6463
Publisher:
Frontiers Media SA
Country of Publication:
Switzerland
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 58 GEOSCIENCES; greenhouse gas flux; peatlands; organic matter decomposition; climate warming; carbon cycling

Citation Formats

Wilson, Rachel M., Neumann, Rebecca B., Crossen, Kelsey B., Raab, Nicole M., Hodgkins, Suzanne B., Saleska, Scott R., Bolduc, Ben, Woodcroft, Ben J., Tyson, Gene W., Chanton, Jeffrey P., and Rich, Virginia I. Microbial Community Analyses Inform Geochemical Reaction Network Models for Predicting Pathways of Greenhouse Gas Production. Switzerland: N. p., 2019. Web. doi:10.3389/feart.2019.00059.
Copy to clipboard
Wilson, Rachel M., Neumann, Rebecca B., Crossen, Kelsey B., Raab, Nicole M., Hodgkins, Suzanne B., Saleska, Scott R., Bolduc, Ben, Woodcroft, Ben J., Tyson, Gene W., Chanton, Jeffrey P., & Rich, Virginia I. Microbial Community Analyses Inform Geochemical Reaction Network Models for Predicting Pathways of Greenhouse Gas Production. Switzerland. https://doi.org/10.3389/feart.2019.00059
Copy to clipboard
Wilson, Rachel M., Neumann, Rebecca B., Crossen, Kelsey B., Raab, Nicole M., Hodgkins, Suzanne B., Saleska, Scott R., Bolduc, Ben, Woodcroft, Ben J., Tyson, Gene W., Chanton, Jeffrey P., and Rich, Virginia I. Fri . "Microbial Community Analyses Inform Geochemical Reaction Network Models for Predicting Pathways of Greenhouse Gas Production". Switzerland. https://doi.org/10.3389/feart.2019.00059.
Copy to clipboard
@article{osti_1504282,
title = {Microbial Community Analyses Inform Geochemical Reaction Network Models for Predicting Pathways of Greenhouse Gas Production},
author = {Wilson, Rachel M. and Neumann, Rebecca B. and Crossen, Kelsey B. and Raab, Nicole M. and Hodgkins, Suzanne B. and Saleska, Scott R. and Bolduc, Ben and Woodcroft, Ben J. and Tyson, Gene W. and Chanton, Jeffrey P. and Rich, Virginia I.},
abstractNote = {The mechanisms, pathways, and rates of CO2 and CH4 production are central to understanding carbon cycling and greenhouse gas flux in wetlands. Thawing permafrost regions are of particular interest because they are disproportionally affected by climate warming and store large reservoirs of organic C that may be readily converted to CO2 and CH4 upon thaw. This conversion is accomplished by a community of microorganisms interacting in complex ways to transform large organic compounds into fatty acids and ultimately CO2 and CH4. While the central role of microbes in this process is well-known, geochemical rate models rarely integrate microbiological information. With this, we expanded the geochemical rate model of Neumann et al., (2016, Biogeochemistry 127: 57–87) to incorporate a Bayesian probability analysis and applied the result to quantifying rates of CO2, CH4, and acetate production in closed-system incubations of peat collected from three habitats along a permafrost thaw gradient. The goals of this analysis were twofold. First, we integrated microbial community analyses with geochemical rate modeling by using microbial data to inform the best model choice among equally mathematically feasible model variants. Second, based on model results, we described changes in organic carbon transformation among habitats to understand the changing pathways of greenhouse gas production along the permafrost thaw gradient. We found that acetoclasty, hydrogenotrophy, CO2 production, and homoacetogenesis were the important reactions in this system, with little evidence for anaerobic CH4 oxidation. There was a distinct transition in the reactions across the thaw gradient. The collapsed palsa stage presents an initial disequilibrium where the abrupt (physically and temporally) change in elevation introduces freshly fixed carbon into anoxic conditions then fermentation products build up over time as the system transitions through the acid phase and electron acceptors are depleted. In the bog, fermentation slows, while methanogenesis increases. In the fully thawed fen, most of the terminal electron acceptors are depleted and the system becomes increasingly methanogenic. This suggests that as permafrost regions thaw and dry palsas transition into wet fens, CH4 emissions will rise, increasing the warming potential of these systems and accelerating climate warming feedbacks.},
doi = {10.3389/feart.2019.00059},
journal = {Frontiers in Earth Science},
number = ,
volume = 7,
place = {Switzerland},
year = {Fri Mar 29 00:00:00 EDT 2019},
month = {Fri Mar 29 00:00:00 EDT 2019}
}
Copy to clipboard
Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.3389/feart.2019.00059
Copyright Statement
Other availability
Search WorldCat Search WorldCat to find libraries that may hold this journal
Citation Metrics:
Cited by: 11 works
Citation information provided by
Web of Science
Save / Share:
Export Metadata
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.

Works referenced in this record:

Small differences in ombrotrophy control regional-scale variation in methane cycling among Sphagnum-dominated peatlands
journal, June 2018

Methanogenic degradation of organic matter by anaerobic bacteria at low temperature
journal, November 1993

Microbial network, phylogenetic diversity and community membership in the active layer across a permafrost thaw gradient
journal, July 2017

  • Mondav, Rhiannon; McCalley, Carmody K.; Hodgkins, Suzanne B.
  • Environmental Microbiology, Vol. 19, Issue 8
  • DOI: 10.1111/1462-2920.13809

Characterization of subsurface methane production and release over 3years at a New Hampshire wetland
journal, August 2012

Ecosystem responses to increased precipitation and permafrost decay in subarctic Sweden inferred from peat and lake sediments
journal, July 2009

Host-linked soil viral ecology along a permafrost thaw gradient
journal, July 2018

Influence of temperature on energetics of hydrogen metabolism in homoacetogenic, methanogenic, and other anaerobic bacteria
journal, December 1990

  • Conrad, Ralf; Wetter, Bettina
  • Archives of Microbiology, Vol. 155, Issue 1
  • DOI: 10.1007/BF00291281

Uncoupling of acetate degradation from methane formation in Alaskan wetlands: Connections to vegetation distribution: PATHWAYS OF METHANOGENESIS IN WETLANDS
journal, May 2008

  • Hines, Mark E.; Duddleston, Khrystyne N.; Rooney-Varga, Juliette N.
  • Global Biogeochemical Cycles, Vol. 22, Issue 2
  • DOI: 10.1029/2006GB002903

Modeling CH4 and CO2 cycling using porewater stable isotopes in a thermokarst bog in Interior Alaska: results from three conceptual reaction networks
journal, December 2015

  • Neumann, Rebecca B.; Blazewicz, Steven J.; Conaway, Christopher H.
  • Biogeochemistry, Vol. 127, Issue 1
  • DOI: 10.1007/s10533-015-0168-2

Surface production fuels deep heterotrophic respiration in northern peatlands: HETEROTROPHIC RESPIRATION IN PEATLANDS
journal, December 2013

  • Elizabeth Corbett, J.; Burdige, David J.; Tfaily, Malak M.
  • Global Biogeochemical Cycles, Vol. 27, Issue 4
  • DOI: 10.1002/2013GB004677

The Bog Landforms of Continental Western Canada in Relation to Climate and Permafrost Patterns
journal, February 1994

  • Vitt, Dale H.; Halsey, Linda A.; Zoltai, Stephen C.
  • Arctic and Alpine Research, Vol. 26, Issue 1
  • DOI: 10.2307/1551870

Methanogenic population dynamics during start-up of anaerobic digesters treating municipal solid waste and biosolids
journal, February 1998

CopyRighter: a rapid tool for improving the accuracy of microbial community profiles through lineage-specific gene copy number correction
journal, April 2014

  • Angly, Florent E.; Dennis, Paul G.; Skarshewski, Adam
  • Microbiome, Vol. 2, Issue 1
  • DOI: 10.1186/2049-2618-2-11

Permafrost Degradation and Ecological Changes Associated with a WarmingClimate in Central Alaska
journal, March 2001

  • Jorgenson, M. Torre; Racine, Charles H.; Walters, James C.
  • Climatic Change, Vol. 48, Issue 4, p. 551-579
  • DOI: 10.1023/A:1005667424292

Microbiomes in light of traits: A phylogenetic perspective
journal, November 2015

Electron shuttling via humic acids in microbial iron(III) reduction in a freshwater sediment
journal, January 2004

Humic substances as electron acceptors for microbial respiration
journal, August 1996

  • Lovley, Derek R.; Coates, John D.; Blunt-Harris, Elizabeth L.
  • Nature, Vol. 382, Issue 6590
  • DOI: 10.1038/382445a0

Acetogenic Prokaryotes
book, January 2006

Soil incubations reproduce field methane dynamics in a subarctic wetland
journal, October 2015

  • Hodgkins, Suzanne B.; Chanton, Jeffrey P.; Langford, Lauren C.
  • Biogeochemistry, Vol. 126, Issue 1-2
  • DOI: 10.1007/s10533-015-0142-z

Methanogenesis at low temperatures by microflora of tundra wetland soil
journal, January 1996

  • Kotsyurbenko, O. R.; Nozhevnikova, A. N.; Soloviova, T. I.
  • Antonie van Leeuwenhoek, Vol. 69, Issue 1
  • DOI: 10.1007/BF00641614

How northern peatlands influence the Earth's radiative budget: Sustained methane emission versus sustained carbon sequestration
journal, January 2006

  • Frolking, Steve; Roulet, Nigel; Fuglestvedt, Jan
  • Journal of Geophysical Research, Vol. 111, Issue G1
  • DOI: 10.1029/2005JG000091

Changes in peat chemistry associated with permafrost thaw increase greenhouse gas production
journal, April 2014

  • Hodgkins, S. B.; Tfaily, M. M.; McCalley, C. K.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 16
  • DOI: 10.1073/pnas.1314641111

Pathways of anaerobic carbon cycling across an ombrotrophic-minerotrophic peatland gradient
journal, January 2007

Chemolithotrophic acetogenic H2/CO2 utilization in Italian rice field soil
journal, March 2011

Methane-producing bacteria: natural fractionations of the stable carbon isotopes
journal, August 1978

Carbon isotope fractionation during bacterial methanogenesis by CO2 reduction
journal, December 1996

Metabolism of homoacetogens
journal, January 1994

  • Diekert, Gabriele; Wohlfarth, Gert
  • Antonie van Leeuwenhoek, Vol. 66, Issue 1-3
  • DOI: 10.1007/BF00871640

Pathways for Methanogenesis and Diversity of Methanogenic Archaea in Three Boreal Peatland Ecosystems
journal, April 2005

Moving Beyond Global Warming Potentials to Quantify the Climatic Role of Ecosystems
journal, May 2015

The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum)
journal, July 2008

Seasonal patterns of carbon dioxide and water fluxes in three representative tundra ecosystems in northern Alaska
journal, January 2012

  • Euskirchen, E. S.; Bret-Harte, M. S.; Scott, G. J.
  • Ecosphere, Vol. 3, Issue 1
  • DOI: 10.1890/ES11-00202.1

Genome-centric view of carbon processing in thawing permafrost
journal, July 2018

Acetogenesis from CO 2 in an anoxic marine sediment
journal, May 1999

  • Hoehler, Tori M.; Albert, Daniel B.; Alperin, Marc J.
  • Limnology and Oceanography, Vol. 44, Issue 3
  • DOI: 10.4319/lo.1999.44.3.0662

Primary production control of methane emission from wetlands
journal, August 1993

  • Whiting, G. J.; Chanton, J. P.
  • Nature, Vol. 364, Issue 6440
  • DOI: 10.1038/364794a0

Experimental factors affecting PCR-based estimates of microbial species richness and evenness
journal, January 2010

  • Engelbrektson, Anna; Kunin, Victor; Wrighton, Kelly C.
  • The ISME Journal, Vol. 4, Issue 5
  • DOI: 10.1038/ismej.2009.153

Vegetation, climatic changes and net carbon sequestration in a North-Scandinavian subarctic mire over 30 years
journal, October 2005

Greenhouse gas balance over thaw-freeze cycles in discontinuous zone permafrost: C Balance of Permafrost Peat
journal, February 2017

  • Wilson, R. M.; Fitzhugh, L.; Whiting, G. J.
  • Journal of Geophysical Research: Biogeosciences, Vol. 122, Issue 2
  • DOI: 10.1002/2016JG003600

Anaerobic microbial biogeochemistry in a northern bog: Acetate as a dominant metabolic end product: ANAEROBIC MICROBIAL BIOGEOCHEMISTRY IN A NORTHERN BOG
journal, October 2002

  • Duddleston, Khrystyne N.; Kinney, Monica A.; Kiene, Ronald P.
  • Global Biogeochemical Cycles, Vol. 16, Issue 4
  • DOI: 10.1029/2001GB001402

Extracellular electron transfer through microbial reduction of solid-phase humic substances
journal, May 2010

  • Roden, Eric E.; Kappler, Andreas; Bauer, Iris
  • Nature Geoscience, Vol. 3, Issue 6
  • DOI: 10.1038/ngeo870

Homoacetogenesis: A potentially underappreciated carbon pathway in peatlands
journal, January 2014

Hydrogen turnover by psychrotrophic homoacetogenic and mesophilic methanogenic bacteria in anoxic paddy soil and lake sediment
journal, August 1989

Using Respiration Rates and Stable Carbon Isotopes to Monitor the Biodegradation of Orimulsion by Marine Benthic Bacteria
journal, June 1999

  • Lapham, Laura; Proctor, Lita; Chanton, Jeffrey
  • Environmental Science & Technology, Vol. 33, Issue 12
  • DOI: 10.1021/es981158a

Methane transport and emissions from soil as affected by water table and vascular plants
journal, January 2013

Anaerobic oxidation of methane: an underappreciated aspect of methane cycling in peatland ecosystems?
journal, January 2011

A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane
journal, January 2014

  • Rotaru, Amelia-Elena; Shrestha, Pravin Malla; Liu, Fanghua
  • Energy Environ. Sci., Vol. 7, Issue 1
  • DOI: 10.1039/C3EE42189A

Partitioning pathways of CO2 production in peatlands with stable carbon isotopes
journal, December 2012

  • Corbett, J. Elizabeth; Tfaily, Malak M.; Burdige, David J.
  • Biogeochemistry, Vol. 114, Issue 1-3
  • DOI: 10.1007/s10533-012-9813-1

Carbon Isotope Fractionation of 11 Acetogenic Strains Grown on H 2 and CO 2
journal, December 2012

  • Blaser, Martin B.; Dreisbach, Lisa K.; Conrad, Ralf
  • Applied and Environmental Microbiology, Vol. 79, Issue 6
  • DOI: 10.1128/AEM.03203-12

Nutrients and Hydrology Indicate the Driving Mechanisms of Peatland Surface Patterning
journal, June 2009

  • Eppinga, Maarten B.; de Ruiter, Peter C.; Wassen, Martin J.
  • The American Naturalist, Vol. 173, Issue 6
  • DOI: 10.1086/598487

CO 2 and CH 4 isotope compositions and production pathways in a tropical peatland : δ13C in CH4 and CO2 in tropical peat
journal, January 2015

  • Holmes, M. Elizabeth; Chanton, Jeffrey P.; Tfaily, Malak M.
  • Global Biogeochemical Cycles, Vol. 29, Issue 1
  • DOI: 10.1002/2014GB004951

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
  • DOI: 10.1002/2013JG002492

Genome-centric resolution of microbial diversity, metabolism and interactions in anaerobic digestion: Genome-centric resolution through deep metagenomics
journal, July 2016

  • Vanwonterghem, Inka; Jensen, Paul D.; Rabaey, Korneel
  • Environmental Microbiology, Vol. 18, Issue 9
  • DOI: 10.1111/1462-2920.13382

Carbon and hydrogen isotope fractionation by moderately thermophilic methanogens 1 1Associate editor: N. E. Ostrom
journal, April 2004

  • Valentine, David L.; Chidthaisong, Amnat; Rice, Andrew
  • Geochimica et Cosmochimica Acta, Vol. 68, Issue 7
  • DOI: 10.1016/j.gca.2003.10.012

Decadal vegetation changes in a northern peatland, greenhouse gas fluxes and net radiative forcing
journal, December 2006

Anaerobic benzene biodegradation—a new era
journal, December 2002

Old Acetogens, New Light
journal, March 2008

  • Drake, Harold L.; Gößner, Anita S.; Daniel, Steven L.
  • Annals of the New York Academy of Sciences, Vol. 1125, Issue 1, p. 100-128
  • DOI: 10.1196/annals.1419.016

Stable carbon isotope fractionation between substrates and products of Methanosarcina barkeri
journal, May 2008

A new data set for estimating organic carbon storage to 3 m depth in soils of the northern circumpolar permafrost region
journal, January 2013

  • Hugelius, G.; Bockheim, J. G.; Camill, P.
  • Earth System Science Data, Vol. 5, Issue 2
  • DOI: 10.5194/essd-5-393-2013

Solid-phase organic matter reduction regulates anaerobic decomposition in bog soil
journal, May 2013

Investigating dissolved organic matter decomposition in northern peatlands using complimentary analytical techniques
journal, July 2013

Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane
journal, September 1999

Global inverse modeling of CH 4 sources and sinks: an overview of methods
journal, January 2017

  • Houweling, Sander; Bergamaschi, Peter; Chevallier, Frederic
  • Atmospheric Chemistry and Physics, Vol. 17, Issue 1
  • DOI: 10.5194/acp-17-235-2017

Acetate Oxidation Is the Dominant Methanogenic Pathway from Acetate in the Absence of Methanosaetaceae
journal, July 2006

  • Karakashev, D.; Batstone, D. J.; Trably, E.
  • Applied and Environmental Microbiology, Vol. 72, Issue 7
  • DOI: 10.1128/AEM.00489-06

Humic acids as electron acceptors in wetland decomposition
journal, July 2009

  • Keller, Jason K.; Weisenhorn, Pamela B.; Megonigal, J. Patrick
  • Soil Biology and Biochemistry, Vol. 41, Issue 7
  • DOI: 10.1016/j.soilbio.2009.04.008

Annual carbon gas budget for a subarctic peatland, Northern Sweden
journal, January 2010

  • Bäckstrand, K.; Crill, P. M.; Jackowicz-Korczyñski, M.
  • Biogeosciences, Vol. 7, Issue 1
  • DOI: 10.5194/bg-7-95-2010

Cyclic Development of Permafrost in the Peatlands of Northwestern Alberta, Canada
journal, August 1993

  • Zoltai, S. C.
  • Arctic and Alpine Research, Vol. 25, Issue 3
  • DOI: 10.2307/1551820

Competition between homoacetogenic bacteria and methanogenic archaea for hydrogen at low temperature
journal, December 2001

Catalysis of an isotopic exchange between CO2 and the carboxyl group of acetate by Methanosarcina barkeri grown on acetate
journal, August 1984

  • Eikmanns, Bernhard; Thauer, Rudolf K.
  • Archives of Microbiology, Vol. 138, Issue 4
  • DOI: 10.1007/BF00410905

Methane dynamics regulated by microbial community response to permafrost thaw
journal, October 2014

  • McCalley, Carmody K.; Woodcroft, Ben J.; Hodgkins, Suzanne B.
  • Nature, Vol. 514, Issue 7523
  • DOI: 10.1038/nature13798

Different types of methane monooxygenases produce similar carbon and hydrogen isotope fractionation patterns during methane oxidation
journal, March 2011

  • Feisthauer, Stefan; Vogt, Carsten; Modrzynski, Jakub
  • Geochimica et Cosmochimica Acta, Vol. 75, Issue 5
  • DOI: 10.1016/j.gca.2010.12.006

Hydrogenation of organic matter as a terminal electron sink sustains high CO2:CH4 production ratios during anaerobic decomposition
journal, October 2017

Methanotrophy across a natural permafrost thaw environment
journal, June 2018

  • Singleton, Caitlin M.; McCalley, Carmody K.; Woodcroft, Ben J.
  • The ISME Journal, Vol. 12, Issue 10
  • DOI: 10.1038/s41396-018-0065-5

Discovery of a novel methanogen prevalent in thawing permafrost
journal, February 2014

  • Mondav, Rhiannon; Woodcroft, Ben J.; Kim, Eun-Hae
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms4212

Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming
journal, April 2015

  • Tveit, Alexander Tøsdal; Urich, Tim; Frenzel, Peter
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 19
  • DOI: 10.1073/pnas.1420797112

Radiocarbon evidence for the substrates supporting methane formation within northern Minnesota peatlands
journal, September 1995

  • Chanton, Jeffrey P.; Bauer, James E.; Glaser, Paul A.
  • Geochimica et Cosmochimica Acta, Vol. 59, Issue 17
  • DOI: 10.1016/0016-7037(95)00240-Z

Manipulating ruminal fermentation: a microbial ecological perspective.
journal, January 1998

    Sort by:
    [ × clear filter / sort ]

    Similar Records in DOE PAGES and OSTI.GOV collections: