TY - JOUR
T1 - Microbial community analyses inform geochemical reaction network models for predicting pathways of greenhouse gas production
AU - Wilson, Rachel M.
AU - Neumann, Rebecca B.
AU - Crossen, Kelsey B.
AU - Raab, Nicole M.
AU - Hodgkins, Suzanne B.
AU - Saleska, Scott R.
AU - Bolduc, Ben
AU - Woodcroft, Ben J.
AU - Tyson, Gene W.
AU - Chanton, Jeffrey P.
AU - Rich, Virginia I.
N1 - Funding Information:
This work was supported, in part by the Genomic Science Program of the United States Department of Energy, Office of Science, Office of Biological and Environmental Research, grants DE-SC0010580 and DE-SC0016440 to VR, SS, JC, and GT, and by grant DE-SC0010338 to RN. Additional support was provided by the Genomic Science Program of the United States DOE Office of Biological and Environmental Research, grants DE-SC0010580 and DE-SC0016440. A portion of the research was performed using the Environmental Molecular Sciences Laboratory (EMSL) (EMSL proposal ID 48467) a DOE Office of Science User Facility and a further portion was performed under the Facilities Integrating Collaborations for User Science (FICUS) initiative (EMSL proposal ID 49521) with resources at the EMSL and the DOE Joint Genome Institute a second DOE Office of Science User Facility. Both facilities are sponsored by the Office of Biological and environmental Research and operated under contract numbers DE-AC02-05CH11231 (JGI) and DE-AC05-76RL01830 (EMSL).
Funding Information:
We would like to thank L. Claire Wilson for analytical assistance and Dylan Cronin for assistance with copy number correction of the 16S microbial data. Funding. This work was supported, in part by the Genomic Science Program of the United States Department of Energy, Office of Science, Office of Biological and Environmental Research, grants DE-SC0010580 and DE-SC0016440 to VR, SS, JC, and GT, and by grant DE-SC0010338 to RN. Additional support was provided by the Genomic Science Program of the United States DOE Office of Biological and Environmental Research, grants DE-SC0010580 and DE-SC0016440. A portion of the research was performed using the Environmental Molecular Sciences Laboratory (EMSL) (EMSL proposal ID 48467) a DOE Office of Science User Facility and a further portion was performed under the Facilities Integrating Collaborations for User Science (FICUS) initiative (EMSL proposal ID 49521) with resources at the EMSL and the DOE Joint Genome Institute a second DOE Office of Science User Facility. Both facilities are sponsored by the Office of Biological and environmental Research and operated under contract numbers DE-AC02-05CH11231 (JGI) and DE-AC05-76RL01830 (EMSL).
Publisher Copyright:
© 2019 Wilson, Neumann, Crossen, Raab, Hodgkins, Saleska, Bolduc, Woodcroft, Tyson, Chanton and Rich.
PY - 2019/2/26
Y1 - 2019/2/26
N2 - 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.
AB - 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.
KW - Carbon cycling
KW - Climate warming
KW - Greenhouse gas flux
KW - Organic matter decomposition
KW - Peatlands
UR - http://www.scopus.com/inward/record.url?scp=85064196429&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85064196429&partnerID=8YFLogxK
U2 - 10.3389/feart.2019.00059
DO - 10.3389/feart.2019.00059
M3 - Article
AN - SCOPUS:85064196429
SN - 2296-6463
VL - 7
JO - Frontiers in Earth Science
JF - Frontiers in Earth Science
M1 - 59
ER -