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

Abstract

The mechanisms, pathways, and rates of CO 2 and CH 4 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 CO 2 and CH 4 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 CO 2 and CH 4. 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 CO 2, CH 4, 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 carbonmore » transformation among habitats to understand the changing pathways of greenhouse gas production along the permafrost thaw gradient. We found that acetoclasty, hydrogenotrophy, CO 2 production, and homoacetogenesis were the important reactions in this system, with little evidence for anaerobic CH 4 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, CH 4 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:
Journal Article: 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.
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
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.
@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},
url = {https://www.osti.gov/biblio/1504282}, journal = {Frontiers in Earth Science},
issn = {2296-6463},
number = ,
volume = 7,
place = {Switzerland},
year = {2019},
month = {3}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at https://doi.org/10.3389/feart.2019.00059

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Works referenced in this record:

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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


Potential carbon emissions dominated by carbon dioxide from thawed permafrost soils
journal, June 2016


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


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


Organic matter transformation in the peat column at Marcell Experimental Forest: Humification and vertical stratification: Organic matter dynamics
journal, April 2014


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


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


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


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


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


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


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


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


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


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


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


Methanotrophy across a natural permafrost thaw environment
journal, June 2018


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


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


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


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