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

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...

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Published in:Frontiers in Earth Science
Main Authors: 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.
Other Authors: Univ Arizona, Dept Soil Water & Environm Sci
Format: Article in Journal/Newspaper
Language:English
Published: FRONTIERS MEDIA SA 2019
Subjects:
Online Access:http://hdl.handle.net/10150/633927
https://doi.org/10.3389/feart.2019.00059
id ftunivarizona:oai:repository.arizona.edu:10150/633927
record_format openpolar
institution Open Polar
collection The University of Arizona: UA Campus Repository
op_collection_id ftunivarizona
language English
topic greenhouse gas flux
peatlands
organic matter decomposition
climate warming
carbon cycling
spellingShingle greenhouse gas flux
peatlands
organic matter decomposition
climate warming
carbon cycling
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
topic_facet greenhouse gas flux
peatlands
organic matter decomposition
climate warming
carbon cycling
description 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. Herein, 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. Genomic Science Program of the United States Department of Energy, Office of Science, Office of Biological and Environmental Research [DE-SC0010580, DE-SC0016440, DE-SC0010338]; Genomic Science Program of the United States DOE Office of Biological and Environmental Research [DE-SC0010580, DE-SC0016440]; Office of Biological and environmental Research; [DE-AC02-05CH11231]; [DE-AC05-76RL01830] Open access journal This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at repository@u.library.arizona.edu.
author2 Univ Arizona, Dept Soil Water & Environm Sci
format Article in Journal/Newspaper
author 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.
author_facet 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.
author_sort Wilson, Rachel M.
title Microbial Community Analyses Inform Geochemical Reaction Network Models for Predicting Pathways of Greenhouse Gas Production
title_short Microbial Community Analyses Inform Geochemical Reaction Network Models for Predicting Pathways of Greenhouse Gas Production
title_full Microbial Community Analyses Inform Geochemical Reaction Network Models for Predicting Pathways of Greenhouse Gas Production
title_fullStr Microbial Community Analyses Inform Geochemical Reaction Network Models for Predicting Pathways of Greenhouse Gas Production
title_full_unstemmed Microbial Community Analyses Inform Geochemical Reaction Network Models for Predicting Pathways of Greenhouse Gas Production
title_sort microbial community analyses inform geochemical reaction network models for predicting pathways of greenhouse gas production
publisher FRONTIERS MEDIA SA
publishDate 2019
url http://hdl.handle.net/10150/633927
https://doi.org/10.3389/feart.2019.00059
genre palsa
palsas
permafrost
genre_facet palsa
palsas
permafrost
op_source 7
op_relation Wilson RM, Neumann RB, Crossen KB, Raab NM, Hodgkins SB, Saleska SR, Bolduc B, Woodcroft BJ, Tyson GW, Chanton JP and Rich VI (2019) Microbial Community Analyses Inform Geochemical Reaction Network Models for Predicting Pathways of Greenhouse Gas Production. Front. Earth Sci. 7:59. doi:10.3389/feart.2019.00059
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doi:10.3389/feart.2019.00059
http://hdl.handle.net/10150/633927
FRONTIERS IN EARTH SCIENCE
op_rights Copyright © 2019 Wilson, Neumann, Crossen, Raab, Hodgkins, Saleska, Bolduc, Woodcroft, Tyson, Chanton and Rich. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
op_rightsnorm CC-BY
op_doi https://doi.org/10.3389/feart.2019.00059
container_title Frontiers in Earth Science
container_volume 7
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spelling ftunivarizona:oai:repository.arizona.edu:10150/633927 2023-05-15T17:54:28+02:00 Microbial Community Analyses Inform Geochemical Reaction Network Models for Predicting Pathways of Greenhouse Gas Production 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. Univ Arizona, Dept Soil Water & Environm Sci 2019-03-29 http://hdl.handle.net/10150/633927 https://doi.org/10.3389/feart.2019.00059 en eng FRONTIERS MEDIA SA Wilson RM, Neumann RB, Crossen KB, Raab NM, Hodgkins SB, Saleska SR, Bolduc B, Woodcroft BJ, Tyson GW, Chanton JP and Rich VI (2019) Microbial Community Analyses Inform Geochemical Reaction Network Models for Predicting Pathways of Greenhouse Gas Production. Front. Earth Sci. 7:59. doi:10.3389/feart.2019.00059 2296-6463 doi:10.3389/feart.2019.00059 http://hdl.handle.net/10150/633927 FRONTIERS IN EARTH SCIENCE Copyright © 2019 Wilson, Neumann, Crossen, Raab, Hodgkins, Saleska, Bolduc, Woodcroft, Tyson, Chanton and Rich. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. CC-BY 7 greenhouse gas flux peatlands organic matter decomposition climate warming carbon cycling Article 2019 ftunivarizona https://doi.org/10.3389/feart.2019.00059 2020-06-14T08:17:46Z 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. Herein, 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. Genomic Science Program of the United States Department of Energy, Office of Science, Office of Biological and Environmental Research [DE-SC0010580, DE-SC0016440, DE-SC0010338]; Genomic Science Program of the United States DOE Office of Biological and Environmental Research [DE-SC0010580, DE-SC0016440]; Office of Biological and environmental Research; [DE-AC02-05CH11231]; [DE-AC05-76RL01830] Open access journal This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at repository@u.library.arizona.edu. Article in Journal/Newspaper palsa palsas permafrost The University of Arizona: UA Campus Repository Frontiers in Earth Science 7