Plant root exudates increase methane emissions through direct and indirect pathways

Waldo, Nicholas B.; Hunt, Brianna K.; Fadely, Eleanor C.; Moran, James J.; Neumann, Rebecca B.

doi:10.1007/s10533-019-00600-6

Title: Plant root exudates increase methane emissions through direct and indirect pathways

Journal Article · 19 September 2019 · Biogeochemistry

DOI: https://doi.org/10.1007/s10533-019-00600-6 · OSTI ID:1598837

^[1]; Hunt, Brianna K. ^[1]; Fadely, Eleanor C. ^[1];

^[2];

^[1]

Univ. of Washington, Seattle, WA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

We report that the largest natural source of methane (CH₄) to the atmosphere is wetlands, which produce 20% to 50% of total global emissions. Vascular plants play a key role regulating wetland CH₄ emissions through multiple mechanisms. They often contain aerenchymatous tissues which act as a diffusive pathway for CH₄ to travel from the anoxic soil to the atmosphere and for O₂ to diffuse into the soil and enable methanotrophy. Plants also exude carbon from their roots which stimulates microbial activity and fuels methanogenesis. This study investigated these mechanisms in a laboratory experiment utilizing rootboxes containing either Carex aquatilis plants, silicone tubes that simulated aerenchymatous gas transfer, or only soil as a control. CH₄ emissions were over 50 times greater from planted boxes than from control boxes or simulated plants, indicating that the physical transport pathway of aerenchyma was of little importance when not paired with other effects of plant biology. Plants were exposed to ¹³CO₂ at two time-points and subsequent enrichment of root tissue, rhizosphere soil, and emitted CH4 was used in an isotope mixing model to determine the proportion of plant-derived versus soil-derived carbon supporting methanogenesis. Results showed that carbon exuded by plants was converted to CH₄ but also that planted boxes emitted 28 times more soil-derived carbon than the other experimental treatments. At the end of the experiment, emissions of excess soil-derived carbon from planted boxes exceeded the emission of plant-derived carbon. Finally, this result signifies that plants and root exudates altered the soil chemical environment, increased microbial metabolism, and/or changed the microbial community such that microbial utilization of soil carbon was increased (e.g. microbial priming) and/or oxidation of soil-derived CH₄ was decreased (e.g., by microbial competition for oxygen).

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of Washington, Seattle, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Workforce Development for Teachers and Scientists (WDTS)

Grant/Contract Number:: SC0010338; AC05-76RL01830; SC0014664

OSTI ID:: 1598837

Journal Information:: Biogeochemistry, Vol. 145, Issue 1-2; ISSN 0168-2563

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 43 works

Citation information provided by
Web of Science

References (56)

Composition and concentration of root exudate analogues regulate greenhouse gas fluxes from tropical peat Girkin, N. T.; Turner, B. L.; Ostle, N. Soil Biology and Biochemistry, Vol. 127 https://doi.org/10.1016/j.soilbio.2018.09.033	journal	December 2018
Temperature effect on biomass production and root/shoot biomass ratios in two arctic sedges under controlled environmental conditions Kummerow, Jochen; Ellis, Barbara A. Canadian Journal of Botany, Vol. 62, Issue 10 https://doi.org/10.1139/b84-294	journal	October 1984
Do Root Exudates Enhance Peat Decomposition? Basiliko, Nathan; Stewart, Heather; Roulet, Nigel T. Geomicrobiology Journal, Vol. 29, Issue 4 https://doi.org/10.1080/01490451.2011.568272	journal	May 2012
The effect of rice straw on the priming of soil organic matter and methane production in peat soils Ye, Rongzhong; Doane, Timothy A.; Morris, Jenifer Soil Biology and Biochemistry, Vol. 81 https://doi.org/10.1016/j.soilbio.2014.11.007	journal	February 2015
Variations in the 13C/12C ratios of plants in relation to the pathway of photosynthetic carbon dioxide fixation Bender, Margaret M. Phytochemistry, Vol. 10, Issue 6 https://doi.org/10.1016/S0031-9422(00)84324-1	journal	June 1971
Linking rhizospheric CH4 oxidation and net CH4 emissions in an arctic wetland based on 13CH4 labeling of mesocosms Nielsen, Cecilie Skov; Michelsen, Anders; Ambus, Per Plant and Soil, Vol. 412, Issue 1-2 https://doi.org/10.1007/s11104-016-3061-4	journal	September 2016
Root exudate analogues accelerate CO 2 and CH 4 production in tropical peat Girkin, N. T.; Turner, B. L.; Ostle, N. Soil Biology and Biochemistry, Vol. 117 https://doi.org/10.1016/j.soilbio.2017.11.008	journal	February 2018
Effects of atmospheric CO2 enrichment on plant growth: the interactive role of air temperature Idso, S. B.; Kimball, B. A.; Anderson, M. G. Agriculture, Ecosystems & Environment, Vol. 20, Issue 1 https://doi.org/10.1016/0167-8809(87)90023-5	journal	November 1987
Below ground carbon turnover and greenhouse gas exchanges in a sub-arctic wetland Ström, Lena; Christensen, Torben R. Soil Biology and Biochemistry, Vol. 39, Issue 7 https://doi.org/10.1016/j.soilbio.2007.01.019	journal	July 2007
Priming effects: Interactions between living and dead organic matter Kuzyakov, Yakov Soil Biology and Biochemistry, Vol. 42, Issue 9 https://doi.org/10.1016/j.soilbio.2010.04.003	journal	September 2010
Dynamics of oxygen and carbon dioxide in rhizospheres of Lobelia dortmanna - a planar optode study of belowground gas exchange between plants and sediment Lenzewski, Nikola; Mueller, Peter; Meier, Robert Johannes New Phytologist, Vol. 218, Issue 1 https://doi.org/10.1111/nph.14973	journal	January 2018
Emerging role of wetland methane emissions in driving 21st century climate change Zhang, Zhen; Zimmermann, Niklaus E.; Stenke, Andrea Proceedings of the National Academy of Sciences, Vol. 114, Issue 36 https://doi.org/10.1073/pnas.1618765114	journal	August 2017
Modeling CH4 and CO2 cycling using porewater stable isotopes in a thermokarst bog in Interior Alaska: results from three conceptual reaction networks Neumann, Rebecca B.; Blazewicz, Steven J.; Conaway, Christopher H. Biogeochemistry, Vol. 127, Issue 1 https://doi.org/10.1007/s10533-015-0168-2	journal	December 2015
Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency Carvalhais, Lilia C.; Dennis, Paul G.; Fedoseyenko, Dmitri Journal of Plant Nutrition and Soil Science, Vol. 174, Issue 1 https://doi.org/10.1002/jpln.201000085	journal	December 2010
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
Stable carbon isotope fractionation during methanogenesis in three boreal peatland ecosystems Galand, P. E.; Yrjälä, K.; Conrad, R. Biogeosciences, Vol. 7, Issue 11 https://doi.org/10.5194/bg-7-3893-2010	journal	January 2010
Organic acids and ethanol inhibit the oxidation of methane by mire methanotrophs: Organic compounds alter methanotroph activity in fen soil Wieczorek, Adam S.; Drake, Harold L.; Kolb, Steffen FEMS Microbiology Ecology, Vol. 77, Issue 1 https://doi.org/10.1111/j.1574-6941.2011.01080.x	journal	April 2011
Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories Chen, Ruirui; Senbayram, Mehmet; Blagodatsky, Sergey Global Change Biology, Vol. 20, Issue 7 https://doi.org/10.1111/gcb.12475	journal	April 2014
Peatland vascular plant functional types affect dissolved organic matter chemistry Robroek, Bjorn J. M.; Albrecht, Remy J. H.; Hamard, Samuel Plant and Soil, Vol. 407, Issue 1-2 https://doi.org/10.1007/s11104-015-2710-3	journal	October 2015
Carbon Storage and Fluxes within Freshwater Wetlands: a Critical Review Kayranli, Birol; Scholz, Miklas; Mustafa, Atif Wetlands, Vol. 30, Issue 1 https://doi.org/10.1007/s13157-009-0003-4	journal	December 2009
Plants mediate soil organic matter decomposition in response to sea level rise Mueller, Peter; Jensen, Kai; Megonigal, James Patrick Global Change Biology, Vol. 22, Issue 1 https://doi.org/10.1111/gcb.13082	journal	December 2015
Methane-producing bacteria: natural fractionations of the stable carbon isotopes Games, Larry M.; HayesRobert, J. M.; Gunsalus, P. Geochimica et Cosmochimica Acta, Vol. 42, Issue 8 https://doi.org/10.1016/0016-7037(78)90123-0	journal	August 1978
Diurnal variation in methane emissions in relation to plants and environmental variables in the Inner Mongolia marshes Wang, Zhi-Ping; Han, Xing-Guo Atmospheric Environment, Vol. 39, Issue 34 https://doi.org/10.1016/j.atmosenv.2005.07.010	journal	November 2005
Northern peatland carbon stocks and dynamics: a review Yu, Z. C. Biogeosciences, Vol. 9, Issue 10 https://doi.org/10.5194/bg-9-4071-2012	journal	January 2012
Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation Rasse, Daniel P.; Rumpel, Cornelia; Dignac, Marie-France Plant and Soil, Vol. 269, Issue 1-2 https://doi.org/10.1007/s11104-004-0907-y	journal	February 2005
Influence of plant developmental stage on microbial community structure and activity in the rhizosphere of three field crops: Plant and growth stage effects on microbial populations Houlden, Ashley; Timms-Wilson, Tracey M.; Day, Martin J. FEMS Microbiology Ecology, Vol. 65, Issue 2 https://doi.org/10.1111/j.1574-6941.2008.00535.x	journal	August 2008
Zero methane emission bogs: extreme rhizosphere oxygenation by cushion plants in Patagonia Fritz, Christian; Pancotto, Veronica A.; Elzenga, Josephus T. M. New Phytologist, Vol. 190, Issue 2 https://doi.org/10.1111/j.1469-8137.2010.03604.x	journal	January 2011
The effect of vascular plants on carbon turnover and methane emissions from a tundra wetland Strom, Lena; Ekberg, Anna; Mastepanov, Mikhail Global Change Biology, Vol. 9, Issue 8 https://doi.org/10.1046/j.1365-2486.2003.00655.x	journal	August 2003
The global methane cycle: recent advances in understanding the microbial processes involved: Global methane cycle Conrad, Ralf Environmental Microbiology Reports, Vol. 1, Issue 5 https://doi.org/10.1111/j.1758-2229.2009.00038.x	journal	June 2009
In Situ Stable Isotope Probing of Methanogenic Archaea in the Rice Rhizosphere Lu, Y. Science, Vol. 309, Issue 5737 https://doi.org/10.1126/science.1113435	journal	August 2005
Microbial Nitrogen Limitation Increases Decomposition Craine, Joseph M.; Morrow, Carl; Fierer, Noah Ecology, Vol. 88, Issue 8 https://doi.org/10.1890/06-1847.1	journal	August 2007
Carbon Isotopes in Photosynthesis O'Leary, Marion H. BioScience, Vol. 38, Issue 5 https://doi.org/10.2307/1310735	journal	May 1988
CH4 and CO2 production below two contrasting peatland micro-relief forms: An inhibitor and δ13C study Krohn, Johannes; Lozanovska, Ivana; Kuzyakov, Yakov Science of The Total Environment, Vol. 586 https://doi.org/10.1016/j.scitotenv.2017.01.192	journal	May 2017
Determination of Methane Oxidation in the Rhizosphere of Sagittaria lancifolia Using Methyl Fluoride Schipper, Louis A.; Reddy, K. R. Soil Science Society of America Journal, Vol. 60, Issue 2 https://doi.org/10.2136/sssaj1996.03615995006000020039x	journal	January 1996
Carbon and hydrogen isotope fractionation by moderately thermophilic methanogens 1 1Associate editor: N. E. Ostrom Valentine, David L.; Chidthaisong, Amnat; Rice, Andrew Geochimica et Cosmochimica Acta, Vol. 68, Issue 7 https://doi.org/10.1016/j.gca.2003.10.012	journal	April 2004
Radial Oxygen Losses from Intact Rice Roots as Affected by Distance from the Apex, Respiration and Waterlogging Armstrong, W. Physiologia Plantarum, Vol. 25, Issue 2 https://doi.org/10.1111/j.1399-3054.1971.tb01427.x	journal	October 1971
A simple and inexpensive high resolution color ratiometric planar optode imaging approach: application to oxygen and pH sensing.: A simple RGB based planar optode imaging approach Larsen, Morten; Borisov, Sergey M.; Grunwald, Björn Limnology and Oceanography: Methods, Vol. 9, Issue 9 https://doi.org/10.4319/lom.2011.9.348	journal	August 2011
Trace-gas metabolic versatility of the facultative methanotroph Methylocella silvestris Crombie, Andrew T.; Murrell, J. Colin Nature, Vol. 510, Issue 7503 https://doi.org/10.1038/nature13192	journal	April 2014
Stable carbon isotope fractionation between substrates and products of Methanosarcina barkeri Londry, Kathleen L.; Dawson, Kathleen G.; Grover, Heather D. Organic Geochemistry, Vol. 39, Issue 5 https://doi.org/10.1016/j.orggeochem.2008.03.002	journal	May 2008
Factors influencing organic carbon preservation in marine sediments Canfield, Donald E. Chemical Geology, Vol. 114, Issue 3-4 https://doi.org/10.1016/0009-2541(94)90061-2	journal	June 1994
Barriers to predicting changes in global terrestrial methane fluxes: analyses using CLM4Me, a methane biogeochemistry model integrated in CESM Riley, W. J.; Subin, Z. M.; Lawrence, D. M. Biogeosciences, Vol. 8, Issue 7 https://doi.org/10.5194/bg-8-1925-2011	journal	January 2011
Enhanced seasonal CO2 exchange caused by amplified plant productivity in northern ecosystems Forkel, M.; Carvalhais, N.; Rodenbeck, C. Science, Vol. 351, Issue 6274 https://doi.org/10.1126/science.aac4971	journal	January 2016
Effect of redox potential on methanogenesis by Methanosarcina barkeri Fetzer, Silke; Conrad, Ralf Archives of Microbiology, Vol. 160, Issue 2 https://doi.org/10.1007/bf00288711	journal	August 1993
New Guidelines for δ ¹³ C Measurements Coplen, Tyler B.; Brand, Willi A.; Gehre, Matthias Analytical Chemistry, Vol. 78, Issue 7 https://doi.org/10.1021/ac052027c	journal	April 2006
Temperature-mediated changes in microbial carbon use efficiency and ¹³ C discrimination Lehmeier, Christoph A.; Ballantyne IV, Ford; Min, Kyungjin Biogeosciences, Vol. 13, Issue 11 https://doi.org/10.5194/bg-13-3319-2016	journal	January 2016
Are oxygen limitations under recognized regulators of organic carbon turnover in upland soils? Keiluweit, Marco; Nico, Peter S.; Kleber, Markus Biogeochemistry, Vol. 127, Issue 2-3 https://doi.org/10.1007/s10533-015-0180-6	journal	January 2016
Contribution of plant photosynthate to soil respiration and dissolved organic carbon in a naturally recolonising cutover peatland Trinder, Clare J.; Artz, Rebekka R. E.; Johnson, David Soil Biology and Biochemistry, Vol. 40, Issue 7 https://doi.org/10.1016/j.soilbio.2008.01.016	journal	July 2008
Different types of methane monooxygenases produce similar carbon and hydrogen isotope fractionation patterns during methane oxidation Feisthauer, Stefan; Vogt, Carsten; Modrzynski, Jakub Geochimica et Cosmochimica Acta, Vol. 75, Issue 5 https://doi.org/10.1016/j.gca.2010.12.006	journal	March 2011
Regulation of methane oxidation in the facultative methanotroph Methylocella silvestris BL2 : Methane oxidation in Methylocella Theisen, Andreas R.; Ali, M. Hanif; Radajewski, Stefan Molecular Microbiology, Vol. 58, Issue 3 https://doi.org/10.1111/j.1365-2958.2005.04861.x	journal	September 2005
A Plant-Soil-Atmosphere Microcosm for Tracing Radiocarbon from Photosynthesis through Methanogenesis Megonigal, J. P.; Whalen, S. C.; Tissue, D. T. Soil Science Society of America Journal, Vol. 63, Issue 3 https://doi.org/10.2136/sssaj1999.03615995006300030033x	journal	January 1999
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
Biogeochemistry of Methane Exchange between Natural Wetlands and the Atmosphere Whalen, S. C. Environmental Engineering Science, Vol. 22, Issue 1 https://doi.org/10.1089/ees.2005.22.73	journal	January 2005
Plant-mediated CH ₄ transport and contribution of photosynthates to methanogenesis at a boreal mire: a ¹⁴ C pulse-labeling study Dorodnikov, M.; Knorr, K. -H.; Kuzyakov, Y. Biogeosciences, Vol. 8, Issue 8 https://doi.org/10.5194/bg-8-2365-2011	journal	January 2011
Greenhouse gas emissions from a constructed wetland—Plants as important sources of carbon Picek, Tomáš; Čížková, Hana; Dušek, Jiří Ecological Engineering, Vol. 31, Issue 2 https://doi.org/10.1016/j.ecoleng.2007.06.008	journal	October 2007
Carbon isotope effects associated with aceticlastic methanogenesis. Gelwicks, J. T.; Risatti, J. B.; Hayes, J. M. Applied and Environmental Microbiology, Vol. 60, Issue 2 https://doi.org/10.1128/AEM.60.2.467-472.1994	journal	January 1994
Barriers to predicting changes in global terrestrial methane fluxes: analyses using CLM4Me, a methane biogeochemistry model integrated in CESM Riley, W. J.; Subin, Z. M.; Lawrence, D. M. Biogeosciences Discussions, Vol. 8, Issue 1 https://doi.org/10.5194/bgd-8-1733-2011	journal	January 2011

Similar Records

Plant Root Exudates Increase Methane Emissions through Direct and Indirect Pathways

Journal Article · 2019 · Biogeochemistry · OSTI ID:1574469

Waldo, Nicholas B.; Hunt, Brianna; Fadely, Eleanor; +2 more

Impacts of The Wetland Sedge Carex aquatilis on Microbial Community and Methane Metabolisms

Journal Article · 2021 · Plant and Soil · OSTI ID:1860255

Waldo, Nicholas B.; Chistoserdova, Ludmila; Hu, Dehong; +2 more

The importance of nutrients for microbial priming in a bog rhizosphere

Journal Article · 2021 · Biogeochemistry · OSTI ID:1767053

Waldo, Nicholas B.; Tfaily, Malak M.; Anderton, Christopher; +1 more

Related Subjects

54 ENVIRONMENTAL SCIENCES
Methane
Wetlands
Microbial priming
Root exudates
Climate change

Title: Plant root exudates increase methane emissions through direct and indirect pathways

Citation Formats

References (56)

Similar Records

Related Subjects