Thaw Transitions and Redox Conditions Drive Methane Oxidation in a Permafrost Peatland

Perryman, Clarice R.; McCalley, Carmody K.; Malhotra, Avni; Fahnestock, M. Florencia; Kashi, Natalie N.; Bryce, Julia G.; Giesler, Reiner; Varner, Ruth K.

doi:10.1029/2019jg005526

Title: Thaw Transitions and Redox Conditions Drive Methane Oxidation in a Permafrost Peatland

Journal Article · Wed Mar 18 00:00:00 EDT 2020 · Journal of Geophysical Research. Biogeosciences

DOI:https://doi.org/10.1029/2019jg005526· OSTI ID:1802991

^[1];

^[2]; Malhotra, Avni ^[3]; Fahnestock, M. Florencia ^[4]; Kashi, Natalie N. ^[5]; Bryce, Julia G. ^[4]; Giesler, Reiner ^[6];

^[1]

Univ. of New Hampshire, Durham, NH (United States); Univ. of New Hampshire, Durham, NH (United States). Inst. for the Study of Earth, Oceans, and Space
Rochester Inst. of Technology, Rochester, NY (United States)
Stanford Univ., CA (United States)
Univ. of New Hampshire, Durham, NH (United States)
Univ. of New Hampshire, Durham, NH (United States). Inst. for the Study of Earth, Oceans, and Space
Umeå Univ. (Sweden). Climate Impacts Research Centre

Abstract Permafrost peatlands are a significant source of methane (CH ₄ ) emissions to the atmosphere and could emit more CH ₄ with continued permafrost thaw. Aerobic methane‐oxidizing bacteria may attenuate a substantial fraction of CH ₄ emissions in thawing permafrost peatlands; however, the impact of permafrost thaw on CH ₄ oxidation is uncertain. We measured potential CH ₄ oxidation rates (hereafter, CH ₄ oxidation) and their predictors using laboratory incubations and in situ porewater redox chemistry across a permafrost thaw gradient of eight thaw stages at Stordalen Mire, a permafrost peatland complex in northernmost Sweden. Methane oxidation rates increased across a gradient of permafrost thaw and differed in transitional thaw stages relative to end‐member stages. Oxidation was consistently higher in submerged fens than in bogs or palsas across a range of CH ₄ concentrations. We also observed that CH ₄ oxidation increased with decreasing in situ redox potential and was highest in sites with lower redox potential (Eh < 10 mV) and high water table. Our results suggest that redox potential can be used as an important predictor of CH ₄ oxidation, especially in thawed permafrost peatlands. Our results also highlight the importance of considering transitional thaw stages when characterizing landscape‐scale CH ₄ dynamics, because these transitional areas have different rates and controls of CH ₄ oxidation relative to intact or completely thawed permafrost areas. As permafrost thaw increases the total area of semiwet and wet thaw stages in permafrost peatlands, CH ₄ oxidation represents an important control on CH ₄ emissions to the atmosphere.

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Research Organization:: The Ohio State Univ., Columbus, OH (United States)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE), Renewable Power Office. Solar Energy Technologies Office; National Science Foundation (NSF)

Grant/Contract Number:: SC0016440; DGE145027; EAR 1063037; DE‐SC0016440

OSTI ID:: 1802991

Alternate ID(s):: OSTI ID: 1605456

Journal Information:: Journal of Geophysical Research. Biogeosciences, Vol. 125, Issue 3; ISSN 2169-8953

Publisher:: American Geophysical UnionCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 16 works

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References (66)

Ecological controls on methane emissions from a Northern Peatland Complex in the zone of discontinuous permafrost, Manitoba, Canada Bubier, Jill L.; Moore, Tim R.; Bellisario, Lianne Global Biogeochemical Cycles, Vol. 9, Issue 4 https://doi.org/10.1029/95GB02379	journal	December 1995
Improved quantification of microbial CH ₄ oxidation efficiency in arctic wetland soils using carbon isotope fractionation Preuss, I.; Knoblauch, C.; Gebert, J. Biogeosciences, Vol. 10, Issue 4 https://doi.org/10.5194/bg-10-2539-2013	journal	January 2013
The influence of temperature and water table position on carbon dioxide and methane emissions from laboratory columns of peatland soils Moore, T. R.; Dalva, M. Journal of Soil Science, Vol. 44, Issue 4 https://doi.org/10.1111/j.1365-2389.1993.tb02330.x	journal	December 1993
CH4 production, oxidation and emission in a U.K. ombrotrophic peat bog: Influence of SO42− from acid rain Nedwell, David B.; Watson, Andrea Soil Biology and Biochemistry, Vol. 27, Issue 7 https://doi.org/10.1016/0038-0717(95)00018-A	journal	July 1995
Dynamics of redox processes in a minerotrophic fen exposed to a water table manipulation Knorr, Klaus-Holger; Lischeid, Gunnar; Blodau, Christian Geoderma, Vol. 153, Issue 3-4 https://doi.org/10.1016/j.geoderma.2009.08.023	journal	November 2009
Methanotrophic symbionts provide carbon for photosynthesis in peat bogs Raghoebarsing, Ashna A.; Smolders, Alfons J. P.; Schmid, Markus C. Nature, Vol. 436, Issue 7054 https://doi.org/10.1038/nature03802	journal	August 2005
Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw Mackelprang, Rachel; Waldrop, Mark P.; DeAngelis, Kristen M. Nature, Vol. 480, Issue 7377 https://doi.org/10.1038/nature10576	journal	November 2011
Regulation of methane production, oxidation, and emission by vascular plants and bryophytes in ponds of the northeast Siberian polygonal tundra Knoblauch, Christian; Spott, Oliver; Evgrafova, Svetlana Journal of Geophysical Research: Biogeosciences, Vol. 120, Issue 12 https://doi.org/10.1002/2015JG003053	journal	December 2015
Methane fluxes and the functional groups of methanotrophs and methanogens in a young Arctic landscape on Disko Island, West Greenland Christiansen, Jesper Riis; Romero, Alejandro Jose Barrera; Jørgensen, Niels O. G. Biogeochemistry, Vol. 122, Issue 1 https://doi.org/10.1007/s10533-014-0026-7	journal	August 2014
CH ₄ oxidation by tundra wetlands as measured by a selective inhibitor technique Moosavi, Sadredin C.; Crill, Patrick M. Journal of Geophysical Research: Atmospheres, Vol. 103, Issue D22 https://doi.org/10.1029/97JD03519	journal	November 1998
Circumpolar distribution and carbon storage of thermokarst landscapes Olefeldt, D.; Goswami, S.; Grosse, G. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13043	journal	October 2016
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
Evidence for Anaerobic CH ₄ Oxidation in Freshwater Peatlands Smemo, Kurt A.; Yavitt, Joseph B. Geomicrobiology Journal, Vol. 24, Issue 7-8 https://doi.org/10.1080/01490450701672083	journal	December 2007
A new climate era in the sub-Arctic: Accelerating climate changes and multiple impacts: CHANGING CLIMATE IN THE SUB-ARCTIC Callaghan, Terry V.; Bergholm, Fredrik; Christensen, Torben R. Geophysical Research Letters, Vol. 37, Issue 14 https://doi.org/10.1029/2009GL042064	journal	July 2010
Major Biogeochemical Processes in Soils-A Microcosm Incubation from Reducing to Oxidizing Conditions Yu, Kewei; Böhme, Frank; Rinklebe, Jörg Soil Science Society of America Journal, Vol. 71, Issue 4 https://doi.org/10.2136/sssaj2006.0155	journal	January 2007
Effect of Carex rostrata on seasonal and interannual variability in peatland methane emissions: EFFECT OF C. ROSTRATA ON CH ₄ EMISSIONS Noyce, Genevieve L.; Varner, Ruth K.; Bubier, Jill L. Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 1 https://doi.org/10.1002/2013JG002474	journal	January 2014
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
Summertime variation of methane oxidation in the rhizosphere of a Carex dominated freshwater marsh Ding, Weixin; Cai, Zucong; Tsuruta, Haruo Atmospheric Environment, Vol. 38, Issue 25 https://doi.org/10.1016/j.atmosenv.2004.04.022	journal	August 2004
Methane and carbon dioxide exchange potentials of peat soils in aerobic and anaerobic laboratory incubations Moore, T. R.; Dalva, M. Soil Biology and Biochemistry, Vol. 29, Issue 8 https://doi.org/10.1016/S0038-0717(97)00037-0	journal	August 1997
Oxidation of methane in peat: Kinetics of CH4 and O2 removal and the role of plant roots Watson, Andrea; Stephen, Karl D.; Nedwell, David B. Soil Biology and Biochemistry, Vol. 29, Issue 8 https://doi.org/10.1016/S0038-0717(97)00016-3	journal	August 1997
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
Erratum: Effect of permafrost thaw on CO ₂ and CH ₄ exchange in a western Alaska peatland chronosequence (2013 Environ. Res. Lett. 9 085004) Johnston, Carmel E.; Ewing, Stephanie A.; Harden, Jennifer W. Environmental Research Letters, Vol. 9, Issue 10 https://doi.org/10.1088/1748-9326/9/10/109601	journal	October 2014
Micro-aerobic bacterial methane oxidation in the chemocline and anoxic water column of deep south-Alpine Lake Lugano (Switzerland) Blees, Jan; Niemann, Helge; Wenk, Christine B. Limnology and Oceanography, Vol. 59, Issue 2 https://doi.org/10.4319/lo.2014.59.2.0311	journal	January 2014
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
Oxidation of methane in boreal forest soils: a comparison of seven measures Whalen, StephenC.; Reeburgh, WilliamS.; Barber, ValerieA. Biogeochemistry, Vol. 16, Issue 3 https://doi.org/10.1007/BF00002818	journal	January 1992
Isotopic insights into methane production, oxidation, and emissions in Arctic polygon tundra Vaughn, Lydia J. S.; Conrad, Mark E.; Bill, Markus Global Change Biology, Vol. 22, Issue 10 https://doi.org/10.1111/gcb.13281	journal	June 2016
Methane Oxidation and the Competition for Oxygen in the Rice Rhizosphere van Bodegom, P.; Stams, F.; Mollema, L. Applied and Environmental Microbiology, Vol. 67, Issue 8 https://doi.org/10.1128/AEM.67.8.3586-3597.2001	journal	August 2001
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
Plant-induced changes in the redox potentials of rice rhizospheres Flessa, H.; Fischer, W. R. Plant and Soil, Vol. 143, Issue 1 https://doi.org/10.1007/BF00009128	journal	June 1992
Methanotrophy potential versus methane supply by pore water diffusion in peatlands Hornibrook, E. R. C.; Bowes, H. L.; Culbert, A. Biogeosciences, Vol. 6, Issue 8 https://doi.org/10.5194/bg-6-1491-2009	journal	January 2009
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
Methane Oxidation, Production, and Emission at Contrasting Sites in a Boreal Bog Geomicrobiology Journal, Vol. 17, Issue 3 https://doi.org/10.1080/01490450050121198	journal	July 2000
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
Evaluation of methane oxidation in therhizosphere of a Carex dominated fen in northcentral Alberta, Canada Popp, Trevor J.; Chanton, Jeffrey P.; Whiting, Gary J. Biogeochemistry, Vol. 51, Issue 3, p. 259-281 https://doi.org/10.1023/A:1006452609284	journal	January 2000
The role of Sphagnum mosses in the methane cycling of a boreal mire Larmola, Tuula; Tuittila, Eeva-Stiina; Tiirola, Marja Ecology, Vol. 91, Issue 8 https://doi.org/10.1890/09-1343.1	journal	August 2010
Potential aerobic methane oxidation in a Sphagnum-dominated peatland—Controlling factors and relation to methane emission Sundh, Ingvar; Mikkelä, Catharina; Nilsson, Mats Soil Biology and Biochemistry, Vol. 27, Issue 6 https://doi.org/10.1016/0038-0717(94)00222-M	journal	June 1995
Genomic Reconstruction of an Uncultured Hydrothermal Vent Gammaproteobacterial Methanotroph (Family Methylothermaceae) Indicates Multiple Adaptations to Oxygen Limitation Skennerton, Connor T.; Ward, Lewis M.; Michel, Alice Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01425	journal	December 2015
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
Plant functional group effects on peat carbon cycling in a boreal rich fen Rupp, Danielle; Kane, Evan S.; Dieleman, Catherine Biogeochemistry, Vol. 144, Issue 3 https://doi.org/10.1007/s10533-019-00590-5	journal	September 2019
Anaerobic oxidation of methane: an underappreciated aspect of methane cycling in peatland ecosystems? Smemo, K. A.; Yavitt, J. B. Biogeosciences, Vol. 8, Issue 3 https://doi.org/10.5194/bg-8-779-2011	journal	January 2011
Abundance, distribution and potential activity of methane oxidizing bacteria in permafrost soils from the Lena Delta, Siberia Liebner, Susanne; Wagner, Dirk Environmental Microbiology, Vol. 9, Issue 1 https://doi.org/10.1111/j.1462-2920.2006.01120.x	journal	January 2007
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
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
Determining Subarctic Peatland Vegetation Using an Unmanned Aerial System (UAS) Palace, Michael; Herrick, Christina; DelGreco, Jessica Remote Sensing, Vol. 10, Issue 9 https://doi.org/10.3390/rs10091498	journal	September 2018
Permafrost collapse is accelerating carbon release Turetsky, Merritt R.; Abbott, Benjamin W.; Jones, Miriam C. Nature, Vol. 569, Issue 7754 https://doi.org/10.1038/d41586-019-01313-4	journal	April 2019
Linking Soil O ₂ , CO ₂ , and CH ₄ Concentrations in a Wetland Soil: Implications for CO ₂ and CH ₄ Fluxes Elberling, Bo; Askaer, Louise; Jørgensen, Christian J. Environmental Science & Technology, Vol. 45, Issue 8 https://doi.org/10.1021/es103540k	journal	April 2011
Electron accepting capacity of dissolved and particulate organic matter control CO2 and CH4 formation in peat soils Gao, Chuanyu; Sander, Michael; Agethen, Svenja Geochimica et Cosmochimica Acta, Vol. 245 https://doi.org/10.1016/j.gca.2018.11.004	journal	January 2019
Methane production and oxidation potentials in relation to water table fluctuations in two boreal mires Kettunen, Anu; Kaitala, Veijo; Lehtinen, Armi Soil Biology and Biochemistry, Vol. 31, Issue 12 https://doi.org/10.1016/S0038-0717(99)00093-0	journal	October 1999
Net carbon accumulation of a high-latitude permafrost palsa mire similar to permafrost-free peatlands: CARBON BALANCE OF A SUBARCTIC PEATLAND Olefeldt, David; Roulet, Nigel T.; Bergeron, Onil Geophysical Research Letters, Vol. 39, Issue 3 https://doi.org/10.1029/2011GL050355	journal	February 2012
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
Water table control of CH ₄ emission enhancement by vascular plants in boreal peatlands Waddington, J. M.; Roulet, N. T.; Swanson, R. V. Journal of Geophysical Research: Atmospheres, Vol. 101, Issue D17 https://doi.org/10.1029/96JD02014	journal	October 1996
Boreal peatland C fluxes under varying permafrost regimes Turetsky, Merritt R.; Wieder, R. Kelman; Vitt, Dale H. Soil Biology and Biochemistry, Vol. 34, Issue 7 https://doi.org/10.1016/S0038-0717(02)00022-6	journal	July 2002
Long‐Term Measurements of Methane Ebullition From Thaw Ponds Burke, S. A.; Wik, M.; Lang, A. Journal of Geophysical Research: Biogeosciences, Vol. 124, Issue 7 https://doi.org/10.1029/2018JG004786	journal	July 2019
Methane oxidation associated with submerged brown mosses reduces methane emissions from Siberian polygonal tundra: Moss-associated methane oxidation Liebner, Susanne; Zeyer, Josef; Wagner, Dirk Journal of Ecology, Vol. 99, Issue 4 https://doi.org/10.1111/j.1365-2745.2011.01823.x	journal	March 2011
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
Diversity and potential activity of methanotrophs in high methane-emitting permafrost thaw ponds Crevecoeur, Sophie; Vincent, Warwick F.; Comte, Jérôme PLOS ONE, Vol. 12, Issue 11 https://doi.org/10.1371/journal.pone.0188223	journal	November 2017
Post-thaw variability in litter decomposition best explained by microtopography at an ice-rich permafrost peatland Malhotra, Avni; Moore, Tim R.; Limpens, Juul Arctic, Antarctic, and Alpine Research, Vol. 50, Issue 1 https://doi.org/10.1080/15230430.2017.1415622	journal	January 2018
Methane emissions, groundwater levels and redox potentials of common wetland soils in a temperate-humid climate Fiedler, Sabine; Sommer, Michael Global Biogeochemical Cycles, Vol. 14, Issue 4 https://doi.org/10.1029/1999GB001255	journal	December 2000
In situ Methane Production from Acid Peat in Plant Communities with Different Moisture Regimes in a Subarctic Mire Svensson, Bo H.; Rosswall, Thomas Oikos, Vol. 43, Issue 3 https://doi.org/10.2307/3544151	journal	December 1984
Multiyear measurements of ebullitive methane flux from three subarctic lakes: METHANE EBULLITION FROM SUBARCTIC LAKES Wik, Martin; Crill, Patrick M.; Varner, Ruth K. Journal of Geophysical Research: Biogeosciences, Vol. 118, Issue 3 https://doi.org/10.1002/jgrg.20103	journal	July 2013
Anaerobic oxidation of methane in tropical and boreal soils: Ecological significance in terrestrial methane cycling: ANAEROBIC OXIDATION OF METHANE IN SOILS Blazewicz, Steven J.; Petersen, Dorthe G.; Waldrop, Mark P. Journal of Geophysical Research: Biogeosciences, Vol. 117, Issue G2 https://doi.org/10.1029/2011JG001864	journal	June 2012
Sources of spatial variation in methane emission from mires in northern Sweden: A mechanistic approach in statistical modeling Granberg, Gunnar; Mikkelä, Catharina; Sundh, Ingvar Global Biogeochemical Cycles, Vol. 11, Issue 2 https://doi.org/10.1029/96GB03352	journal	June 1997
Methanotrophy across a natural permafrost thaw environment Singleton, Caitlin M.; McCalley, Carmody K.; Woodcroft, Ben J. The ISME Journal, Vol. 12, Issue 10 https://doi.org/10.1038/s41396-018-0065-5	journal	June 2018
Redox dynamics in the active layer of an Arctic headwater catchment; examining the potential for transfer of dissolved methane from soils to stream water: Arctic Redox Dynamics and Soil Methane Street, Lorna E.; Dean, Joshua F.; Billett, Michael F. Journal of Geophysical Research: Biogeosciences, Vol. 121, Issue 11 https://doi.org/10.1002/2016JG003387	journal	November 2016
Emissions from thaw ponds largely offset the carbon sink of northern permafrost wetlands Kuhn, McKenzie; Lundin, Erik J.; Giesler, Reiner Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-27770-x	journal	June 2018
Radiocarbon evidence for the substrates supporting methane formation within northern Minnesota peatlands Chanton, Jeffrey P.; Bauer, James E.; Glaser, Paul A. Geochimica et Cosmochimica Acta, Vol. 59, Issue 17 https://doi.org/10.1016/0016-7037(95)00240-Z	journal	September 1995

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54 ENVIRONMENTAL SCIENCES
methane
peatland
permafrost
methanotrophs
redox

Title: Thaw Transitions and Redox Conditions Drive Methane Oxidation in a Permafrost Peatland

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