Getting to the Root of Plant–Mediated Methane Emissions and Oxidation in a Thermokarst Bog
Abstract
Vascular plants are important in the wetland methane cycle, but their effect on production, oxidation, and transport has high uncertainty, limiting our ability to predict emissions. In a permafrost–thaw bog in Interior Alaska, we used plant manipulation treatments, field–deployed planar optical oxygen sensors, direct measurements of methane oxidation, and microbial DNA analyses to disentangle mechanisms by which vascular vegetation affect methane emissions. Vegetation operated on top of baseline methane emissions, which varied with proximity to the thawing permafrost margin. Emissions from vegetated plots increased over the season, resulting in cumulative seasonal methane emissions that were 4.1–5.2 g m–2 season–1 greater than unvegetated plots. Mass balance calculations signify these greater emissions were due to increased methane production (3.0–3.5 g m–2 season–1) and decreased methane oxidation (1.1–1.6 g m–2 season–1). Minimal oxidation occurred along the plant–transport pathway, and oxidation was suppressed outside the plant pathway. Our data indicate suppression of methane oxidation was stimulated by root exudates fueling competition among microbes for electron acceptors. This contention is supported by the fact that methane oxidation and relative abundance of methanotrophs decreased over the season in the presence of vegetation, but methane oxidation remained steady in unvegetated treatments; oxygen was not detected around plantmore »
- Authors:
-
[1];
[2];
[5];
[6];
[3]
- Univ. of Washington, Seattle, WA (United States); SMRU Consulting, Friday Harbor, WA (United States)
- Univ. of Washington, Seattle, WA (United States); Kansas State Univ., Manhattan, KS (United States)
- Univ. of Washington, Seattle, WA (United States)
- Univ. of Guelph, ON (Canada); Mackenzie Valley Environmental Impact Review Board, Yellowknife, NT (United States)
- U.S. Geological Survey, Menlo Park, CA (United States)
- Univ. of Guelph, ON (Canada); Univ. of Colorado, Boulder, CO (United States)
- Publication Date:
- Research Org.:
- Univ. of Washington, Seattle, WA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division; Joint Genome Institute; National Science Foundation (NSF); USDA Forest Service, Pacific Northwest Research Station
- Contributing Org.:
- USGS Land Change Science Program. Bonanza Creek LTER Program, which is jointly funded by NSF (DEB 1026415) and the USDA Forest Service, Pacific Northwest Research Station (PNW01‐ JV112619320‐16)
- OSTI Identifier:
- 1771151
- Grant/Contract Number:
- SC0010338; 1445; DEB 1026415; PNW01‐JV112619320‐16
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Geophysical Research. Biogeosciences
- Additional Journal Information:
- Journal Volume: 125; Journal Issue: 11; Journal ID: ISSN 2169-8953
- Publisher:
- American Geophysical Union
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 58 GEOSCIENCES; root exudates; thermokarst; aerenchyma; permafrost; wetland; Carex vascular vegetation
Citation Formats
Turner, Jesse C., Moorberg, Colby J., Wong, Andrea, Shea, Kathleen, Waldrop, Mark P., Turetsky, Merritt R., and Neumann, Rebecca B. Getting to the Root of Plant–Mediated Methane Emissions and Oxidation in a Thermokarst Bog. United States: N. p., 2020.
Web. doi:10.1029/2020jg005825.
Turner, Jesse C., Moorberg, Colby J., Wong, Andrea, Shea, Kathleen, Waldrop, Mark P., Turetsky, Merritt R., & Neumann, Rebecca B. Getting to the Root of Plant–Mediated Methane Emissions and Oxidation in a Thermokarst Bog. United States. https://doi.org/10.1029/2020jg005825
Turner, Jesse C., Moorberg, Colby J., Wong, Andrea, Shea, Kathleen, Waldrop, Mark P., Turetsky, Merritt R., and Neumann, Rebecca B. Thu .
"Getting to the Root of Plant–Mediated Methane Emissions and Oxidation in a Thermokarst Bog". United States. https://doi.org/10.1029/2020jg005825. https://www.osti.gov/servlets/purl/1771151.
@article{osti_1771151,
title = {Getting to the Root of Plant–Mediated Methane Emissions and Oxidation in a Thermokarst Bog},
author = {Turner, Jesse C. and Moorberg, Colby J. and Wong, Andrea and Shea, Kathleen and Waldrop, Mark P. and Turetsky, Merritt R. and Neumann, Rebecca B.},
abstractNote = {Vascular plants are important in the wetland methane cycle, but their effect on production, oxidation, and transport has high uncertainty, limiting our ability to predict emissions. In a permafrost–thaw bog in Interior Alaska, we used plant manipulation treatments, field–deployed planar optical oxygen sensors, direct measurements of methane oxidation, and microbial DNA analyses to disentangle mechanisms by which vascular vegetation affect methane emissions. Vegetation operated on top of baseline methane emissions, which varied with proximity to the thawing permafrost margin. Emissions from vegetated plots increased over the season, resulting in cumulative seasonal methane emissions that were 4.1–5.2 g m–2 season–1 greater than unvegetated plots. Mass balance calculations signify these greater emissions were due to increased methane production (3.0–3.5 g m–2 season–1) and decreased methane oxidation (1.1–1.6 g m–2 season–1). Minimal oxidation occurred along the plant–transport pathway, and oxidation was suppressed outside the plant pathway. Our data indicate suppression of methane oxidation was stimulated by root exudates fueling competition among microbes for electron acceptors. This contention is supported by the fact that methane oxidation and relative abundance of methanotrophs decreased over the season in the presence of vegetation, but methane oxidation remained steady in unvegetated treatments; oxygen was not detected around plant roots but was detected around silicone tubes mimicking aerenchyma; and oxygen injection experiments suggested that oxygen consumption was faster in the presence of vascular vegetation. In conclusion, root exudates are known to fuel methane production, and our work provides evidence they also decrease methane oxidation.},
doi = {10.1029/2020jg005825},
journal = {Journal of Geophysical Research. Biogeosciences},
number = 11,
volume = 125,
place = {United States},
year = {Thu Oct 15 00:00:00 EDT 2020},
month = {Thu Oct 15 00:00:00 EDT 2020}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Methane Emissions to the Atmosphere Through Aquatic Plants1
journal, January 1985
- Sebacher, Daniel I.; Harriss, Robert C.; Bartlett, Karen B.
- Journal of Environment Quality, Vol. 14, Issue 1
Regulation of root-associated methanotrophy by oxygen availability in the rhizosphere of two aquatic macrophytes.
journal, January 1997
- Calhoun, A.; King, G. M.
- Applied and environmental microbiology, Vol. 63, Issue 8
Plant-dependent CH 4 emission in a subarctic Canadian fen
journal, September 1992
- Whiting, Gary J.; Chanton, Jeffrey P.
- Global Biogeochemical Cycles, Vol. 6, Issue 3
Regulation of methane production, oxidation, and emission by vascular plants and bryophytes in ponds of the northeast Siberian polygonal tundra
journal, December 2015
- Knoblauch, Christian; Spott, Oliver; Evgrafova, Svetlana
- Journal of Geophysical Research: Biogeosciences, Vol. 120, Issue 12
CH 4 oxidation by tundra wetlands as measured by a selective inhibitor technique
journal, November 1998
- Moosavi, Sadredin C.; Crill, Patrick M.
- Journal of Geophysical Research: Atmospheres, Vol. 103, Issue D22
Plant species traits regulate methane production in freshwater wetland soils
journal, February 2011
- Sutton-Grier, Ariana E.; Megonigal, J. Patrick
- Soil Biology and Biochemistry, Vol. 43, Issue 2
Modeling methane fluxes in wetlands with gas-transporting plants: 2. Soil layer scale
journal, February 2001
- Segers, Reinoud; Rappoldt, Cornelis; Leffelaar, Peter A.
- Journal of Geophysical Research: Atmospheres, Vol. 106, Issue D4
Effects of permafrost thaw on nitrogen availability and plant–soil interactions in a boreal Alaskan lowland
journal, July 2016
- Finger, Rebecca A.; Turetsky, Merritt R.; Kielland, Knut
- Journal of Ecology, Vol. 104, Issue 6
The effects of spatial and temporal variations in acetate and sulfate on methane cycling in two Michigan peatlands
journal, May 1996
- Shannon, Robert D.; White, Jeffrey R.
- Limnology and Oceanography, Vol. 41, Issue 3
Seasonal variation in methane oxidation by the rhizosphere of Phragmites australis and Scirpus lacustris
journal, June 1998
- van der Nat, Frans-Jaco W. A.; Middelburg, Jack J.
- Aquatic Botany, Vol. 61, Issue 2
Emerging role of wetland methane emissions in driving 21st century climate change
journal, August 2017
- Zhang, Zhen; Zimmermann, Niklaus E.; Stenke, Andrea
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 36
Rhizosphere feedbacks in elevated CO2
journal, April 1999
- Cheng, W.
- Tree Physiology, Vol. 19, Issue 4-5
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
- Neumann, Rebecca B.; Blazewicz, Steven J.; Conaway, Christopher H.
- Biogeochemistry, Vol. 127, Issue 1
Species effects and seasonal trends on plant efflux quantity and quality in a spruce swamp forest
journal, March 2018
- Edwards, Keith R.; Kaštovská, Eva; Borovec, Jakub
- Plant and Soil, Vol. 426, Issue 1-2
Effect of Carex rostrata on seasonal and interannual variability in peatland methane emissions: EFFECT OF C. ROSTRATA ON CH 4 EMISSIONS
journal, January 2014
- Noyce, Genevieve L.; Varner, Ruth K.; Bubier, Jill L.
- Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 1
Variation in methane production pathways associated with permafrost decomposition in collapse scar bogs of Alberta, Canada: VARIATION IN METHANE PRODUCTION
journal, October 2007
- Prater, James L.; Chanton, Jeffrey P.; Whiting, Gary J.
- Global Biogeochemical Cycles, Vol. 21, Issue 4
Methane efflux in relation to plant biomass and sediment characteristics in stands of three common emergent macrophytes in boreal mesoeutrophic lakes
journal, January 2005
- Kankaala, Paula; Kaki, Tiina; Makela, Suvi
- Global Change Biology, Vol. 11, Issue 1
How Roots Control the flux of Carbon to the Rhizosphere
journal, April 2003
- Farrar, John; Hawes, Martha; Jones, Davey
- Ecology, Vol. 84, Issue 4
Seasonal Patterns and Plant-Mediated Controls of Subsurface Wetland Biogeochemistry
journal, December 2005
- Neubauer, Scott C.; Givler, Kim; Valentine, SarahKeith
- Ecology, Vol. 86, Issue 12
Uncertainties in modelling CH 4 emissions from northern wetlands in glacial climates: the role of vegetation parameters
journal, January 2011
- Berrittella, C.; van Huissteden, J.
- Climate of the Past, Vol. 7, Issue 4
Summertime variation of methane oxidation in the rhizosphere of a Carex dominated freshwater marsh
journal, August 2004
- Ding, Weixin; Cai, Zucong; Tsuruta, Haruo
- Atmospheric Environment, Vol. 38, Issue 25
Changes in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma
journal, November 2000
- Visser, E. J. W.; Colmer, T. D.; Blom, C. W. P. M.
- Plant, Cell and Environment, Vol. 23, Issue 11
Correlations between substrate availability, dissolved CH 4 , and CH 4 emissions in an arctic wetland subject to warming and plant removal: Arctic Wetland CH 4 Dynamics
journal, March 2017
- Nielsen, Cecilie Skov; Michelsen, Anders; Strobel, Bjarne W.
- Journal of Geophysical Research: Biogeosciences, Vol. 122, Issue 3
Oxidation of methane in peat: Kinetics of CH4 and O2 removal and the role of plant roots
journal, August 1997
- Watson, Andrea; Stephen, Karl D.; Nedwell, David B.
- Soil Biology and Biochemistry, Vol. 29, Issue 8
What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2: Tansley review
journal, November 2004
- Ainsworth, Elizabeth A.; Long, Stephen P.
- New Phytologist, Vol. 165, Issue 2
Methane emissions from wetlands in the zone of discontinuous permafrost: Fort Simpson, Northwest Territories, Canada
journal, December 1997
- Liblik, L. K.; Moore, T. R.; Bubier, J. L.
- Global Biogeochemical Cycles, Vol. 11, Issue 4
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
journal, June 2010
- Caporaso, J. G.; Lauber, C. L.; Walters, W. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
Environmental and vegetation controls on the spatial variability of CH4 emission from wet-sedge and tussock tundra ecosystems in the Arctic
journal, January 2015
- McEwing, Katherine Rose; Fisher, James Paul; Zona, Donatella
- Plant and Soil, Vol. 388, Issue 1-2
Pathways for Methanogenesis and Diversity of Methanogenic Archaea in Three Boreal Peatland Ecosystems
journal, April 2005
- Galand, P. E.; Fritze, H.; Conrad, R.
- Applied and Environmental Microbiology, Vol. 71, Issue 4
Environmental and physical controls on northern terrestrial methane emissions across permafrost zones
journal, November 2012
- Olefeldt, David; Turetsky, Merritt R.; Crill, Patrick M.
- Global Change Biology, Vol. 19, Issue 2
A mechanistic model on methane oxidation in a rice rhizosphere
journal, September 2001
- Van Bodegom, Peter; Goudriaan, Jan; Leffelaar, Peter
- Biogeochemistry, Vol. 55, Issue 2, p. 145-177
Quantitative imaging of radial oxygen loss from Valisneria spiralis roots with a fluorescent planar optode
journal, November 2016
- Han, Chao; Ren, Jinghua; Tang, Hao
- Science of The Total Environment, Vol. 569-570
Species-specific Effects of Vascular Plants on Carbon Turnover and Methane Emissions from Wetlands
journal, August 2005
- Ström, Lena; Mastepanov, Mikhail; Christensen, Torben R.
- Biogeochemistry, Vol. 75, Issue 1
Oxygen dynamics in the rhizosphere of Zostera marina: A two-dimensional planar optode study
journal, March 2006
- Frederiksen, Morten S.; Glud, Ronnie N.
- Limnology and Oceanography, Vol. 51, Issue 2
Sensitivity analysis of a wetland methane emission model based on temperate and arctic wetland sites
journal, January 2009
- van Huissteden, J.; Petrescu, A. M. R.; Hendriks, D. M. D.
- Biogeosciences, Vol. 6, Issue 12
Methane emission from natural wetlands: interplay between emergent macrophytes and soil microbial processes. A mini-review
journal, August 2009
- Laanbroek, Hendrikus J.
- Annals of Botany, Vol. 105, Issue 1
Elevated dissolved organic carbon biodegradability from thawing and collapsing permafrost: Permafrost carbon biodegradability
journal, October 2014
- Abbott, Benjamin W.; Larouche, Julia R.; Jones, Jeremy B.
- Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 10
Vegetation Type Dominates the Spatial Variability in CH4 Emissions Across Multiple Arctic Tundra Landscapes
journal, May 2016
- Davidson, Scott J.; Sloan, Victoria L.; Phoenix, Gareth K.
- Ecosystems, Vol. 19, Issue 6
Climate-CH 4 feedback from wetlands and its interaction with the climate-CO 2 feedback
journal, January 2011
- Ringeval, B.; Friedlingstein, P.; Koven, C.
- Biogeosciences, Vol. 8, Issue 8
Methane emissions proportional to permafrost carbon thawed in Arctic lakes since the 1950s
journal, August 2016
- Walter Anthony, Katey; Daanen, Ronald; Anthony, Peter
- Nature Geoscience, Vol. 9, Issue 9
Primary production control of methane emission from wetlands
journal, August 1993
- Whiting, G. J.; Chanton, J. P.
- Nature, Vol. 364, Issue 6440
Zero methane emission bogs: extreme rhizosphere oxygenation by cushion plants in Patagonia
journal, January 2011
- Fritz, Christian; Pancotto, Veronica A.; Elzenga, Josephus T. M.
- New Phytologist, Vol. 190, Issue 2
Methane emission and transport by arctic sedges in Alaska: Results of a vegetation removal experiment
journal, November 1998
- King, Jennifer Y.; Reeburgh, William S.; Regli, Shannon K.
- Journal of Geophysical Research: Atmospheres, Vol. 103, Issue D22
Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE
journal, April 2009
- Leakey, Andrew D. B.; Ainsworth, Elizabeth A.; Bernacchi, Carl J.
- Journal of Experimental Botany, Vol. 60, Issue 10
Evaluation of methane oxidation in therhizosphere of a Carex dominated fen in northcentral Alberta, Canada
journal, January 2000
- Popp, Trevor J.; Chanton, Jeffrey P.; Whiting, Gary J.
- Biogeochemistry, Vol. 51, Issue 3, p. 259-281
Oxygen Distribution in Wetland Plant Roots and Permeability Barriers to Gas-exchange with the Rhizosphere: a Microelectrode and Modelling Study with Phragmites australis
journal, September 2000
- Armstrong, W.
- Annals of Botany, Vol. 86, Issue 3
The effect of vascular plants on carbon turnover and methane emissions from a tundra wetland
journal, August 2003
- Strom, Lena; Ekberg, Anna; Mastepanov, Mikhail
- Global Change Biology, Vol. 9, Issue 8
A frozen feast: thawing permafrost increases plant-available nitrogen in subarctic peatlands
journal, March 2012
- Keuper, Frida; Bodegom, Peter M.; Dorrepaal, Ellen
- Global Change Biology, Vol. 18, Issue 6
Methane dynamics in the subarctic tundra: combining stable isotope analyses, plot- and ecosystem-scale flux measurements
journal, January 2016
- Marushchak, M. E.; Friborg, T.; Biasi, C.
- Biogeosciences, Vol. 13, Issue 2
Quantification of methane oxidation in the rhizosphere of emergent aquatic macrophytes: defining upper limits
journal, June 1993
- Gerard, Ghislain; Chanton, Jeffrey
- Biogeochemistry, Vol. 23, Issue 2
Significance of stomatal control on methane release from -dominated wetlands
journal, January 1993
- Morrissey, L. A.; Zobel, D. B.; Livingston, G. P.
- Chemosphere, Vol. 26, Issue 1-4
Root systems and root:mass ratio-carbon allocation under current and projected atmospheric conditions in arable crops
journal, July 1995
- Gregory, P. J.; Palta, J. A.; Batts, G. R.
- Plant and Soil, Vol. 187, Issue 2
Elevated CO2 and water depth regulation of methane emissions: Comparison of woody and non-woody wetland plant species
journal, April 2003
- Vann, Cheryl D.
- Biogeochemistry, Vol. 63, Issue 2, p. 117-134
A process-based, climate-sensitive model to derive methane emissions from natural wetlands: Application to five wetland sites, sensitivity to model parameters, and climate
journal, September 2000
- Walter, Bernadette P.; Heimann, Martin
- Global Biogeochemical Cycles, Vol. 14, Issue 3
Methane fluxes between terrestrial ecosystems and the atmosphere at northern high latitudes during the past century: A retrospective analysis with a process-based biogeochemistry model: METHANE EMISSIONS FROM NORTHERN HIGH LATITUDES
journal, August 2004
- Zhuang, Q.; Melillo, J. M.; Kicklighter, D. W.
- Global Biogeochemical Cycles, Vol. 18, Issue 3
Peatland vascular plant functional types affect methane dynamics by altering microbial community structure
journal, May 2015
- Robroek, Bjorn J. M.; Jassey, Vincent E. J.; Kox, Martine A. R.
- Journal of Ecology, Vol. 103, Issue 4
Differential response of carbon fluxes to climate in three peatland ecosystems that vary in the presence and stability of permafrost: Carbon fluxes and permafrost thaw
journal, August 2014
- Euskirchen, E. S.; Edgar, C. W.; Turetsky, M. R.
- Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 8
O2 dynamics in the rhizosphere of young rice plants (Oryza sativa L.) as studied by planar optodes
journal, February 2015
- Larsen, Morten; Santner, Jakob; Oburger, Eva
- Plant and Soil, Vol. 390, Issue 1-2
Plant transport and methane production as controls on methane flux from arctic wet meadow tundra
journal, March 1995
- Schimel, Joshua P.
- Biogeochemistry, Vol. 28, Issue 3
Barriers to predicting changes in global terrestrial methane fluxes: analyses using CLM4Me, a methane biogeochemistry model integrated in CESM
journal, January 2011
- Riley, W. J.; Subin, Z. M.; Lawrence, D. M.
- Biogeosciences, Vol. 8, Issue 7
Regulation of methane oxidation in a freshwater wetland by water table changes and anoxia
journal, February 1996
- Roslev, Peter; King, Gary M.
- FEMS Microbiology Ecology, Vol. 19, Issue 2
Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales
journal, February 2013
- Bridgham, Scott D.; Cadillo-Quiroz, Hinsby; Keller, Jason K.
- Global Change Biology, Vol. 19, Issue 5
Implementation and evaluation of a new methane model within a dynamic global vegetation model: LPJ-WHyMe v1.3.1
journal, January 2010
- Wania, R.; Ross, I.; Prentice, I. C.
- Geoscientific Model Development, Vol. 3, Issue 2
Present state of global wetland extent and wetland methane modelling: conclusions from a model inter-comparison project (WETCHIMP)
journal, January 2013
- Melton, J. R.; Wania, R.; Hodson, E. L.
- Biogeosciences, Vol. 10, Issue 2
RESPONSE OF CO 2 AND CH 4 EMISSIONS FROM PEATLANDS TO WARMING AND WATER TABLE MANIPULATION
journal, April 2001
- Updegraff, Karen; Bridgham, Scott D.; Pastor, John
- Ecological Applications, Vol. 11, Issue 2
A Plant-Soil-Atmosphere Microcosm for Tracing Radiocarbon from Photosynthesis through Methanogenesis
journal, January 1999
- Megonigal, J. P.; Whalen, S. C.; Tissue, D. T.
- Soil Science Society of America Journal, Vol. 63, Issue 3
Vascular plant controls on methane emissions from northern peatforming wetlands
journal, October 1999
- Joabsson, Anna; Christensen, Torben Røjle; Wallén, Bo
- Trends in Ecology & Evolution, Vol. 14, Issue 10
Biogeochemistry of Methane Exchange between Natural Wetlands and the Atmosphere
journal, January 2005
- Whalen, S. C.
- Environmental Engineering Science, Vol. 22, Issue 1
Controls on methane released through ebullition in peatlands affected by permafrost degradation: Ebullition in peatlands with thermokarst
journal, March 2014
- Klapstein, Sara J.; Turetsky, Merritt R.; McGuire, A. David
- Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 3
The dynamics of oxygen concentration, pH value, and organic acids in the rhizosphere of Juncus spp.
journal, June 2011
- Blossfeld, Stephan; Gansert, Dirk; Thiele, Björn
- Soil Biology and Biochemistry, Vol. 43, Issue 6
Warming Effects of Spring Rainfall Increase Methane Emissions From Thawing Permafrost
journal, February 2019
- Neumann, Rebecca B.; Moorberg, Colby J.; Lundquist, Jessica D.
- Geophysical Research Letters, Vol. 46, Issue 3