Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions
Abstract
The current paradigm, widely incorporated in soil biogeochemical models, is that microbial methanogenesis can only occur in anoxic habitats. In contrast, here we show clear geochemical and biological evidence for methane production in well-oxygenated soils of a freshwater wetland. A comparison of oxic to anoxic soils reveal up to ten times greater methane production and nine times more methanogenesis activity in oxygenated soils. Metagenomic and metatranscriptomic sequencing recover the first near-complete genomes for a novel methanogen species, and show acetoclastic production from this organism was the dominant methanogenesis pathway in oxygenated soils. This organism, Candidatus Methanothrix paradoxum, is prevalent across methane emitting ecosystems, suggesting a global significance. Moreover, in this wetland, we estimate that up to 80% of methane fluxes could be attributed to methanogenesis in oxygenated soils. Together, our findings challenge a widely held assumption about methanogenesis, with significant ramifications for global methane estimates and Earth system modeling.
- Authors:
-
[1];
[3];
[2];
[1];
- The Ohio State Univ., Columbus, OH (United States)
- Univ. of Colorado, Denver, CO (United States)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1419456
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES
Citation Formats
Angle, Jordan C., Morin, Timothy H., Solden, Lindsey M., Narrowe, Adrienne B., Smith, Garrett J., Borton, Mikayla A., Rey-Sanchez, Camilo, Daly, Rebecca A., Mirfenderesgi, Golnazalsdat, Hoyt, David W., Riley, William J., Miller, Christopher S., Bohrer, Gil, and Wrighton, Kelly C. Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions. United States: N. p., 2017.
Web. doi:10.1038/s41467-017-01753-4.
Angle, Jordan C., Morin, Timothy H., Solden, Lindsey M., Narrowe, Adrienne B., Smith, Garrett J., Borton, Mikayla A., Rey-Sanchez, Camilo, Daly, Rebecca A., Mirfenderesgi, Golnazalsdat, Hoyt, David W., Riley, William J., Miller, Christopher S., Bohrer, Gil, & Wrighton, Kelly C. Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions. United States. https://doi.org/10.1038/s41467-017-01753-4
Angle, Jordan C., Morin, Timothy H., Solden, Lindsey M., Narrowe, Adrienne B., Smith, Garrett J., Borton, Mikayla A., Rey-Sanchez, Camilo, Daly, Rebecca A., Mirfenderesgi, Golnazalsdat, Hoyt, David W., Riley, William J., Miller, Christopher S., Bohrer, Gil, and Wrighton, Kelly C. Thu .
"Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions". United States. https://doi.org/10.1038/s41467-017-01753-4. https://www.osti.gov/servlets/purl/1419456.
@article{osti_1419456,
title = {Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions},
author = {Angle, Jordan C. and Morin, Timothy H. and Solden, Lindsey M. and Narrowe, Adrienne B. and Smith, Garrett J. and Borton, Mikayla A. and Rey-Sanchez, Camilo and Daly, Rebecca A. and Mirfenderesgi, Golnazalsdat and Hoyt, David W. and Riley, William J. and Miller, Christopher S. and Bohrer, Gil and Wrighton, Kelly C.},
abstractNote = {The current paradigm, widely incorporated in soil biogeochemical models, is that microbial methanogenesis can only occur in anoxic habitats. In contrast, here we show clear geochemical and biological evidence for methane production in well-oxygenated soils of a freshwater wetland. A comparison of oxic to anoxic soils reveal up to ten times greater methane production and nine times more methanogenesis activity in oxygenated soils. Metagenomic and metatranscriptomic sequencing recover the first near-complete genomes for a novel methanogen species, and show acetoclastic production from this organism was the dominant methanogenesis pathway in oxygenated soils. This organism, Candidatus Methanothrix paradoxum, is prevalent across methane emitting ecosystems, suggesting a global significance. Moreover, in this wetland, we estimate that up to 80% of methane fluxes could be attributed to methanogenesis in oxygenated soils. Together, our findings challenge a widely held assumption about methanogenesis, with significant ramifications for global methane estimates and Earth system modeling.},
doi = {10.1038/s41467-017-01753-4},
journal = {Nature Communications},
number = 1,
volume = 8,
place = {United States},
year = {Thu Nov 16 00:00:00 EST 2017},
month = {Thu Nov 16 00:00:00 EST 2017}
}
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- FEMS Microbiology Ecology, Vol. 94, Issue 6
Microbial community structure and microbial networks correspond to nutrient gradients within coastal wetlands of the Laurentian Great Lakes
journal, March 2019
- Horton, Dean J.; Theis, Kevin R.; Uzarski, Donald G.
- FEMS Microbiology Ecology, Vol. 95, Issue 4
Chemical and microbial diversity covary in fresh water to influence ecosystem functioning
journal, November 2019
- Tanentzap, Andrew J.; Fitch, Amelia; Orland, Chloe
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 49
Humid Subtropical Forests Constitute a Net Methane Source: A Catchment‐Scale Study
journal, September 2019
- Yu, Longfei; Zhu, Jing; Zhang, Xiaoshan
- Journal of Geophysical Research: Biogeosciences, Vol. 124, Issue 9
Methane and Biogenic Volatile Organic Compound Emissions in Eastern Siberia
book, January 2019
- van Huissteden, Jacobus
- Ecological Studies
Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales
journal, June 2018
- Borton, Mikayla A.; Hoyt, David W.; Roux, Simon
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 28
Carbon Sequestration by Wetlands: A Critical Review of Enhancement Measures for Climate Change Mitigation
journal, April 2019
- Were, David; Kansiime, Frank; Fetahi, Tadesse
- Earth Systems and Environment, Vol. 3, Issue 2
Chemical and microbial diversity covary in fresh water to influence ecosystem functioning
text, January 2019
- Tanentzap, Andrew; Fitch, Amelia; Orland, Chloe
- Apollo - University of Cambridge Repository
Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils
journal, December 2019
- Narrowe, Adrienne B.; Borton, Mikayla A.; Hoyt, David W.
- mSystems, Vol. 4, Issue 6
Wetland methane emissions dominated by plant‐mediated fluxes: Contrasting emissions pathways and seasons within a shallow freshwater subtropical wetland
journal, March 2019
- Jeffrey, Luke C.; Maher, Damien T.; Johnston, Scott G.
- Limnology and Oceanography, Vol. 64, Issue 5
Comparative genomics and physiology of the genus Methanohalophilus , a prevalent methanogen in hydraulically fractured shale
journal, December 2018
- Borton, Mikayla A.; Daly, Rebecca A.; O'Banion, Bridget
- Environmental Microbiology, Vol. 20, Issue 12
Soil properties and sediment accretion modulate methane fluxes from restored wetlands
journal, April 2018
- Chamberlain, Samuel D.; Anthony, Tyler L.; Silver, Whendee L.
- Global Change Biology, Vol. 24, Issue 9
Hopanoid lipids may facilitate aerobic nitrogen fixation in the ocean
journal, August 2019
- Cornejo-Castillo, Francisco M.; Zehr, Jonathan P.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 37
Co-cultivation of the strictly anaerobic methanogen Methanosarcina barkeri with aerobic methanotrophs in an oxygen-limited membrane bioreactor
journal, May 2018
- in ’t Zandt, Michiel H.; van den Bosch, Tijs J. M.; Rijkers, Ruud
- Applied Microbiology and Biotechnology, Vol. 102, Issue 13
Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales
journal, June 2018
- Borton, Mikayla A.; Hoyt, David W.; Roux, Simon
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 28
Hopanoid lipids may facilitate aerobic nitrogen fixation in the ocean
journal, August 2019
- Cornejo-Castillo, Francisco M.; Zehr, Jonathan P.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 37
Aquatic and terrestrial cyanobacteria produce methane
journal, January 2020
- Bižić, M.; Klintzsch, T.; Ionescu, D.
- Science Advances, Vol. 6, Issue 3
Impact of Warming on Greenhouse Gas Production and Microbial Diversity in Anoxic Peat From a Sphagnum-Dominated Bog (Grand Rapids, Minnesota, United States)
journal, April 2019
- Kolton, Max; Marks, Ansley; Wilson, Rachel M.
- Frontiers in Microbiology, Vol. 10