Methane Production Pathway Regulated Proximally by Substrate Availability and Distally by Temperature in a High-Latitude Mire Complex

Chang, Kuang‐Yu; Riley, William J.; Brodie, Eoin L.; McCalley, Carmody K.; Crill, Patrick M.; Grant, Robert F.

doi:10.1029/2019jg005355

Title: Methane Production Pathway Regulated Proximally by Substrate Availability and Distally by Temperature in a High-Latitude Mire Complex

Journal Article · 24 October 2019 · Journal of Geophysical Research. Biogeosciences

DOI: https://doi.org/10.1029/2019jg005355 · OSTI ID:1581106

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Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Rochester Inst. of Technology, Rochester, NY (United States)
Stockholm Univ. (Sweden)
Univ. of Alberta, Edmonton, AB (Canada)

Projected 21st century changes in high-latitude climate are expected to have significant impacts on permafrost thaw, which could cause substantial increases in emissions to the atmosphere of carbon dioxide (CO₂) and methane (CH₄, which has a global warming potential 28 times larger than CO₂ over a 100-year horizon). However, predicted CH₄ emission rates are very uncertain due to difficulties in modeling complex interactions among hydrological, thermal, biogeochemical, and plant processes. Methanogenic production pathways (i.e., acetoclastic [AM] and hydrogenotrophic [HM]) and the magnitude of CH₄ emissions may both change as permafrost thaws, but a mechanistic analysis of controls on such shifts in CH₄ dynamics is lacking. In this study, we reproduced observed shifts in CH₄ emissions and production pathways with a comprehensive biogeochemical model (ecosys) at the Stordalen Mire in subarctic Sweden. Our results demonstrate that soil temperature changes differently affect AM and HM substrate availability, which regulates magnitudes of AM, HM, and thereby net CH₄ emissions. We predict very large landscape-scale, vertical, and temporal variations in the modeled HM fraction, highlighting that measurement strategies for metrics that compare CH₄ production pathways could benefit from model informed scale of temporal and spatial variance. Finally, our findings suggest that the warming and wetting trends projected in northern peatlands could enhance peatland AM fraction and CH₄ emissions even without further permafrost degradation.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; SC0016440; AC02‐05CH11231

OSTI ID:: 1581106

Alternate ID(s):: OSTI ID: 1571704

Journal Information:: Journal of Geophysical Research. Biogeosciences, Vol. 124, Issue 10; ISSN 2169-8953

Publisher:: American Geophysical UnionCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 22 works

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References (60)

Methane efflux from boreal wetlands: Theory and testing of the ecosystem model Ecosys with chamber and tower flux measurements: METHANE EFFLUX FROM BOREAL WETLANDS Grant, R. F.; Roulet, N. T. Global Biogeochemical Cycles, Vol. 16, Issue 4 https://doi.org/10.1029/2001GB001702	journal	October 2002
pH controls over anaerobic carbon mineralization, the efficiency of methane production, and methanogenic pathways in peatlands across an ombrotrophic–minerotrophic gradient Ye, Rongzhong; Jin, Qusheng; Bohannan, Brendan Soil Biology and Biochemistry, Vol. 54 https://doi.org/10.1016/j.soilbio.2012.05.015	journal	November 2012
Evolution of Acetoclastic Methanogenesis in Methanosarcina via Horizontal Gene Transfer from Cellulolytic Clostridia Fournier, G. P.; Gogarten, J. P. Journal of Bacteriology, Vol. 190, Issue 3 https://doi.org/10.1128/JB.01382-07	journal	November 2007
LS3MIP (v1.0) contribution to CMIP6: the Land Surface, Snow and Soil moisture Model Intercomparison Project – aims, setup and expected outcome van den Hurk, Bart; Kim, Hyungjun; Krinner, Gerhard Geoscientific Model Development, Vol. 9, Issue 8 https://doi.org/10.5194/gmd-9-2809-2016	journal	January 2016
Climate change and the permafrost carbon feedback Schuur, E. A. G.; McGuire, A. D.; Schädel, C. Nature, Vol. 520, Issue 7546 https://doi.org/10.1038/nature14338	journal	April 2015
Effects of permafrost and hydrology on the composition and transport of dissolved organic carbon in a subarctic peatland complex: DOC IN A SUBARCTIC PEATLAND COMPLEX Olefeldt, David; Roulet, Nigel T. Journal of Geophysical Research: Biogeosciences, Vol. 117, Issue G1 https://doi.org/10.1029/2011JG001819	journal	January 2012
Dependence of the evolution of carbon dynamics in the northern permafrost region on the trajectory of climate change McGuire, A. David; Lawrence, David M.; Koven, Charles Proceedings of the National Academy of Sciences, Vol. 115, Issue 15 https://doi.org/10.1073/pnas.1719903115	journal	March 2018
Non-methane volatile organic compound flux from a subarctic mire in Northern Sweden Bäckstrand, Kristina; Crill, Patrick M.; Mastepanov, Mikhail Tellus B: Chemical and Physical Meteorology, Vol. 60, Issue 2 https://doi.org/10.1111/j.1600-0889.2007.00331.x	journal	January 2008
Uncoupling of acetate degradation from methane formation in Alaskan wetlands: Connections to vegetation distribution: PATHWAYS OF METHANOGENESIS IN WETLANDS Hines, Mark E.; Duddleston, Khrystyne N.; Rooney-Varga, Juliette N. Global Biogeochemical Cycles, Vol. 22, Issue 2 https://doi.org/10.1029/2006GB002903	journal	May 2008
Surface exchange of water vapour between an open sphagnum fen and the atmosphere Kim, Joon; Verma, Shashi B. Boundary-Layer Meteorology, Vol. 79, Issue 3 https://doi.org/10.1007/BF00119440	journal	May 1996
Impacts of temperature and soil characteristics on methane production and oxidation in Arctic tundra Zheng, Jianqiu; RoyChowdhury, Taniya; Yang, Ziming Biogeosciences, Vol. 15, Issue 21 https://doi.org/10.5194/bg-15-6621-2018	journal	January 2018
Total hydrocarbon flux dynamics at a subarctic mire in northern Sweden Bäckstrand, Kristina; Crill, Patrick M.; Mastepanov, Mikhail Journal of Geophysical Research, Vol. 113, Issue G3 https://doi.org/10.1029/2008JG000703	journal	January 2008
Methane production as key to the greenhouse gas budget of thawing permafrost Knoblauch, Christian; Beer, Christian; Liebner, Susanne Nature Climate Change, Vol. 8, Issue 4 https://doi.org/10.1038/s41558-018-0095-z	journal	March 2018
Assessing effects of permafrost thaw on C fluxes based on multiyear modeling across a permafrost thaw gradient at Stordalen, Sweden Deng, J.; Li, C.; Frolking, S. Biogeosciences, Vol. 11, Issue 17 https://doi.org/10.5194/bg-11-4753-2014	journal	January 2014
Adding stable carbon isotopes improves model representation of the role of microbial communities in peatland methane cycling Deng, Jia; McCalley, Carmody K.; Frolking, Steve Journal of Advances in Modeling Earth Systems, Vol. 9, Issue 2 https://doi.org/10.1002/2016MS000817	journal	May 2017
Changes in peat chemistry associated with permafrost thaw increase greenhouse gas production Hodgkins, S. B.; Tfaily, M. M.; McCalley, C. K. Proceedings of the National Academy of Sciences, Vol. 111, Issue 16 https://doi.org/10.1073/pnas.1314641111	journal	April 2014
Modeling Climate Change Impacts on an Arctic Polygonal Tundra: 2. Changes in CO ₂ and CH ₄ Exchange Depend on Rates of Permafrost Thaw as Affected by Changes in Vegetation and Drainage Grant, R. F.; Mekonnen, Z. A.; Riley, W. J. Journal of Geophysical Research: Biogeosciences, Vol. 124, Issue 5 https://doi.org/10.1029/2018JG004645	journal	May 2019
Modeling Climate Change Impacts on an Arctic Polygonal Tundra: 1. Rates of Permafrost Thaw Depend on Changes in Vegetation and Drainage Grant, R. F.; Mekonnen, Z. A.; Riley, W. J. Journal of Geophysical Research: Biogeosciences, Vol. 124, Issue 5 https://doi.org/10.1029/2018JG004644	journal	May 2019
The effect of gas transport on the isotope signature of methane in wetlands Chanton, Jeffrey P. Organic Geochemistry, Vol. 36, Issue 5 https://doi.org/10.1016/j.orggeochem.2004.10.007	journal	May 2005
Environmental and physical controls on northern terrestrial methane emissions across permafrost zones Olefeldt, David; Turetsky, Merritt R.; Crill, Patrick M. Global Change Biology, Vol. 19, Issue 2 https://doi.org/10.1111/gcb.12071	journal	November 2012
Moving Beyond Global Warming Potentials to Quantify the Climatic Role of Ecosystems Neubauer, Scott C.; Megonigal, J. Patrick Ecosystems, Vol. 18, Issue 6 https://doi.org/10.1007/s10021-015-9879-4	journal	May 2015
Effect of temperature on methane dynamics and evaluation of methane oxidation kinetics in shallow Arctic Alaskan lakes Lofton, Dendy D.; Whalen, Stephen C.; Hershey, Anne E. Hydrobiologia, Vol. 721, Issue 1 https://doi.org/10.1007/s10750-013-1663-x	journal	August 2013
Controls on moss evaporation in a boreal black spruce forest Heijmans, Monique M. P. D.; Arp, Wim J.; Chapin, F. Stuart Global Biogeochemical Cycles, Vol. 18, Issue 2 https://doi.org/10.1029/2003GB002128	journal	April 2004
Large tundra methane burst during onset of freezing Mastepanov, Mikhail; Sigsgaard, Charlotte; Dlugokencky, Edward J. Nature, Vol. 456, Issue 7222 https://doi.org/10.1038/nature07464	journal	December 2008
Genome-centric view of carbon processing in thawing permafrost Woodcroft, Ben J.; Singleton, Caitlin M.; Boyd, Joel A. Nature, Vol. 560, Issue 7716 https://doi.org/10.1038/s41586-018-0338-1	journal	July 2018
Vegetation, climatic changes and net carbon sequestration in a North-Scandinavian subarctic mire over 30 years Malmer, Nils; Johansson, Torbjorn; Olsrud, Maria Global Change Biology, Vol. 0, Issue 0 https://doi.org/10.1111/j.1365-2486.2005.01042.x	journal	October 2005
Mathematical Modelling of Arctic Polygonal Tundra with Ecosys: 2. Microtopography Determines How CO ₂ and CH ₄ Exchange Responds to Changes in Temperature and Precipitation : GHG Exchange in Arctic Polygonal Tundra Grant, R. F.; Mekonnen, Z. A.; Riley, W. J. Journal of Geophysical Research: Biogeosciences, Vol. 122, Issue 12 https://doi.org/10.1002/2017JG004037	journal	December 2017
Mathematical Modelling of Arctic Polygonal Tundra with Ecosys : 1. Microtopography Determines How Active Layer Depths Respond to Changes in Temperature and Precipitation : Active Layer Depth in Polygonal Tundra Grant, R. F.; Mekonnen, Z. A.; Riley, W. J. Journal of Geophysical Research: Biogeosciences, Vol. 122, Issue 12 https://doi.org/10.1002/2017JG004035	journal	December 2017
Accelerated Nutrient Cycling and Increased Light Competition Will Lead to 21st Century Shrub Expansion in North American Arctic Tundra Mekonnen, Zelalem A.; Riley, William J.; Grant, Robert F. Journal of Geophysical Research: Biogeosciences, Vol. 123, Issue 5 https://doi.org/10.1029/2017JG004319	journal	May 2018
Estimated stocks of circumpolar permafrost carbon with quantified uncertainty ranges and identified data gaps Hugelius, G.; Strauss, J.; Zubrzycki, S. Biogeosciences, Vol. 11, Issue 23 https://doi.org/10.5194/bg-11-6573-2014	journal	January 2014
Environmental correlates of peatland carbon fluxes in a thawing landscape: do transitional thaw stages matter? Malhotra, A.; Roulet, N. T. Biogeosciences, Vol. 12, Issue 10 https://doi.org/10.5194/bg-12-3119-2015	journal	January 2015
Thawing sub-arctic permafrost: Effects on vegetation and methane emissions Christensen, Torben R. Geophysical Research Letters, Vol. 31, Issue 4 https://doi.org/10.1029/2003GL018680	journal	January 2004
Stable Carbon Isotope Fractionation by Methylotrophic Methanogenic Archaea Penger, Jörn; Conrad, Ralf; Blaser, Martin Applied and Environmental Microbiology, Vol. 78, Issue 21 https://doi.org/10.1128/AEM.01773-12	journal	August 2012
Decadal vegetation changes in a northern peatland, greenhouse gas fluxes and net radiative forcing Johansson, TorbjÖRn; Malmer, Nils; Crill, Patrick M. Global Change Biology, Vol. 12, Issue 12 https://doi.org/10.1111/j.1365-2486.2006.01267.x	journal	December 2006
A History and Review of the Global Soil Wetness Project (GSWP) Dirmeyer, Paul A. Journal of Hydrometeorology, Vol. 12, Issue 5 https://doi.org/10.1175/JHM-D-10-05010.1	journal	October 2011
Spatial distribution of microbial methane production pathways in temperate zone wetland soils: Stable carbon and hydrogen isotope evidence Hornibrook, Edward R. C.; Longstaffe, Frederick J.; Fyfe, William S. Geochimica et Cosmochimica Acta, Vol. 61, Issue 4 https://doi.org/10.1016/S0016-7037(96)00368-7	journal	February 1997
The Twentieth Century Reanalysis Project Compo, G. P.; Whitaker, J. S.; Sardeshmukh, P. D. Quarterly Journal of the Royal Meteorological Society, Vol. 137, Issue 654 https://doi.org/10.1002/qj.776	journal	January 2011
Permafrost carbon-climate feedbacks accelerate global warming Koven, C. D.; Ringeval, B.; Friedlingstein, P. Proceedings of the National Academy of Sciences, Vol. 108, Issue 36 https://doi.org/10.1073/pnas.1103910108	journal	August 2011
Methanogenic archaea: ecologically relevant differences in energy conservation Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning Nature Reviews Microbiology, Vol. 6, Issue 8 https://doi.org/10.1038/nrmicro1931	journal	June 2008
Wetland development, permafrost history and nutrient cycling inferred from late Holocene peat and lake sediment records in subarctic Sweden Kokfelt, Ulla; Reuss, Nina; Struyf, Eric Journal of Paleolimnology, Vol. 44, Issue 1 https://doi.org/10.1007/s10933-010-9406-8	journal	February 2010
Surface vegetation controls on evapotranspiration from a sub-humid Western Boreal Plain wetland Brown, S. M.; Petrone, R. M.; Mendoza, C. Hydrological Processes, Vol. 24, Issue 8 https://doi.org/10.1002/hyp.7569	journal	April 2010
Shift from Acetoclastic to H2-Dependent Methanogenesis in a West Siberian Peat Bog at Low pH Values and Isolation of an Acidophilic Methanobacterium Strain Kotsyurbenko, O. R.; Friedrich, M. W.; Simankova, M. V. Applied and Environmental Microbiology, Vol. 73, Issue 7 https://doi.org/10.1128/AEM.02413-06	journal	February 2007
Annual carbon gas budget for a subarctic peatland, Northern Sweden Bäckstrand, K.; Crill, P. M.; Jackowicz-Korczyñski, M. Biogeosciences, Vol. 7, Issue 1 https://doi.org/10.5194/bg-7-95-2010	journal	January 2010
Large carbon cycle sensitivities to climate across a permafrost thaw gradient in subarctic Sweden Chang, Kuang-Yu; Riley, William J.; Crill, Patrick M. The Cryosphere, Vol. 13, Issue 2 https://doi.org/10.5194/tc-13-647-2019	journal	January 2019
Methane dynamics regulated by microbial community response to permafrost thaw McCalley, Carmody K.; Woodcroft, Ben J.; Hodgkins, Suzanne B. Nature, Vol. 514, Issue 7523 https://doi.org/10.1038/nature13798	journal	October 2014
Towards a rain-dominated Arctic Bintanja, R.; Andry, O. Nature Climate Change, Vol. 7, Issue 4 https://doi.org/10.1038/nclimate3240	journal	March 2017
Variability in the sensitivity among model simulations of permafrost and carbon dynamics in the permafrost region between 1960 and 2009: MODELING PERMAFROST CARBON DYNAMICS McGuire, A. David; Koven, Charles; Lawrence, David M. Global Biogeochemical Cycles, Vol. 30, Issue 7 https://doi.org/10.1002/2016GB005405	journal	July 2016
Methane fluxes show consistent temperature dependence across microbial to ecosystem scales Yvon-Durocher, Gabriel; Allen, Andrew P.; Bastviken, David Nature, Vol. 507, Issue 7493 https://doi.org/10.1038/nature13164	journal	March 2014
Present state of global wetland extent and wetland methane modelling: methodology of a model inter-comparison project (WETCHIMP) Wania, R.; Melton, J. R.; Hodson, E. L. Geoscientific Model Development, Vol. 6, Issue 3 https://doi.org/10.5194/gmd-6-617-2013	journal	January 2013
Temperature Sensitivity of Methane Production in the Permafrost Active Layer at Stordalen, Sweden: A Comparison with Non-permafrost Northern Wetlands Lupascu, M.; Wadham, J. L.; Hornibrook, E. R. C. Arctic, Antarctic, and Alpine Research, Vol. 44, Issue 4 https://doi.org/10.1657/1938-4246-44.4.469	journal	November 2012
Discovery of a novel methanogen prevalent in thawing permafrost Mondav, Rhiannon; Woodcroft, Ben J.; Kim, Eun-Hae Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4212	journal	February 2014
Modelling changes in nitrogen cycling to sustain increases in forest productivity under elevated atmospheric CO ₂ and contrasting site conditions Grant, R. F. Biogeosciences, Vol. 10, Issue 11 https://doi.org/10.5194/bg-10-7703-2013	journal	January 2013
Reviews and syntheses: Four decades of modeling methane cycling in terrestrial ecosystems Xu, Xiaofeng; Yuan, Fengming; Hanson, Paul J. Biogeosciences, Vol. 13, Issue 12 https://doi.org/10.5194/bg-13-3735-2016	journal	January 2016
Annual carbon gas budget for a subarctic peatland, northern Sweden Bäckstrand, K.; Crill, P. M.; Jackowicz-Korczyñski, M. Biogeosciences Discussions, Vol. 6, Issue 3 https://doi.org/10.5194/bgd-6-5705-2009	journal	January 2009
A History and Review of the Global Soil Wetness Project (GSWP) Dirmeyer, Paul A. Journal of Hydrometeorology https://doi.org/10.1175/jhm-d-10-05010	journal	March 2011
Non-methane volatile organic compound flux from a subarctic mire in Northern Sweden Bäckstrand, Kristina; Crill, Patrick M.; Mastepanov, Mikhail Tellus B, Vol. 60, Issue 2 https://doi.org/10.3402/tellusb.v60i2.16917	journal	April 2008
Environmental correlates of peatland carbon fluxes in a thawing landscape: do transitional thaw stages matter? Malhotra, A.; Roulet, N. T. Biogeosciences Discussions, Vol. 12, Issue 1 https://doi.org/10.5194/bgd-12-445-2015	journal	January 2015
The Twentieth Century Reanalysis Project Compo, Gilbert P.; Whitaker, Jeffrey S.; Sardeshmudh, Prashant D. Royal Meteorological Society https://doi.org/10.7892/boris.9227	text	January 2011
Present state of global wetland extent and wetland methane modelling: methodology of a model inter-comparison project (WETCHIMP) Wania, R.; Melton, J. R.; Hodson, Elke L. ETH Zurich https://doi.org/10.3929/ethz-b-000070026	text	January 2013
LS3MIP (v1.0) contribution to CMIP6: The Land Surface, Snow and Soil moisture Model Intercomparison Project - Aims, setup and expected outcome Van Den Hurk, Bart; Kim, Hyungjun; Krinner, Gerhard ETH Zurich https://doi.org/10.3929/ethz-b-000120158	text	January 2016