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Title: 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 habitats1-4. In contrast, here porewater and greenhouse-gas flux measurements show clear evidence for methane production in well-oxygenated soils from a freshwater wetland. A comparison of oxic to anoxic soils revealed up to ten times greater methane production and nine times more methanogenesis activity in oxygenated soils. Metagenomic and metatranscriptomic sequencing recovered the first near complete genomes for a novel methanogen species, and showed acetoclastic production from this organism was the dominant methanogenesis pathway in oxygenated soils. This organism, Candidatus Methanosaeta oxydurans, is prevalent across methane emitting ecosystems, suggesting a global significance. Moreover, in this wetland, we estimated that a dominant fraction 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:
; ; ; ; ORCiD logo; ; ; ; ; ORCiD logo; ; ORCiD logo; ORCiD logo;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1411889
Report Number(s):
PNNL-SA-125731
Journal ID: ISSN 2041-1723; 48859; KP1704020
DOE Contract Number:
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Nature Communications; Journal Volume: 8; Journal Issue: 1
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; Environmental Molecular Sciences Laboratory

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. 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, and Wrighton, Kelly C. 2017. "Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions". United States. doi:10.1038/s41467-017-01753-4.
@article{osti_1411889,
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 habitats1-4. In contrast, here porewater and greenhouse-gas flux measurements show clear evidence for methane production in well-oxygenated soils from a freshwater wetland. A comparison of oxic to anoxic soils revealed up to ten times greater methane production and nine times more methanogenesis activity in oxygenated soils. Metagenomic and metatranscriptomic sequencing recovered the first near complete genomes for a novel methanogen species, and showed acetoclastic production from this organism was the dominant methanogenesis pathway in oxygenated soils. This organism, Candidatus Methanosaeta oxydurans, is prevalent across methane emitting ecosystems, suggesting a global significance. Moreover, in this wetland, we estimated that a dominant fraction 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 = 2017,
month =
}
  • 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 acrossmore » 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.« less
  • Tropical wetlands are one of the largest natural sources in the global methane budget due to high biological activities and the anaerobiosis in soil. We studied mineralization and gas production during the early stage of anaerobic decomposition of indigenous organic matters in soils of Narathiwat, southern Thailand, to clarify the significance of the substrate quality in controlling decomposition and methanogenesis in some different tropical wetland soils. The optimal temperature of decomposition was around 35{degrees}C, while methanogenesis did not proceed at 45{degrees}C. During the first 50 days of anaerobic incubation, 5 {approximately} 63% (carbon basis) of indigeneous plant leaves were mineralized.more » The mineralization rate was strongly and negatively correlated with the lignin and/or fiber contents, but not the C/N ratio, of the substrate plant materials. Difference in {delta}{sup 13}C between the substrate, indicating that H{sub 2} as opposed to acetate becomes a more important metabolic intermediate in the anaerobic food web when the decomposition rate is limited by substrate recalcitrance. Thus, the CH{sub 4} isotope signature may be used to evaluate the importance of new vs. old organic matter as CH{sub 4} isotope signature may be used to evaluate the importance of new vs. old organic matter as CH{sub 4} source in natural soils. The mineralization rate was higher, and the isotopic difference between the substrate and CH{sub 4} was smaller when plant materials were incubated with sulfate-contaminated soils than with native peat soils. The isotopic difference between the substrate and CH{sub 4} was significantly different between native peat soils. Results of a tracer experiment using {sup 13}C-labeled substrates indicated that these differences could be ascribed to difference in the mode of acetate metabolism between soils. 49 refs., 8 figs., 7 tabs.« less
  • The identity and distribution of substrates that support CH{sub 4} production in wetlands is poorly known at present. Organic compounds are the primary methanogenic precursor at all depths within anoxic wetland soils; however, the distribution of microbial processes by which these compounds are ultimately converted to CH{sub 4} is uncertain. Based on stable isotope measurements of CH{sub 4} and {Sigma}CO{sub 2} extracted from soil porewaters in two temperate zone wetlands, we present evidence that a systematic spatial distribution of microbial methanogenic pathways can exist in certain anoxic, organic-rich soils. CH{sub 4} production by the acetate fermentation pathway is favored inmore » the shallow subsurface. while methanogenesis from the reduction of CO{sub 2} with H{sub 2} becomes more predominant in older, less reactive peat at depth. This distribution can account for many of the reported CH{sub 4} emission characteristics of wetlands, in particular, their sensitivity to changes in primary productivity, temperature, and hydrology. These factors play an important role in controlling the short-term supply of labile substrates to fermentive methanogens in the shallow subsurface where the most intense CH{sub 4} production occurs. Predominance of the CO{sub 2}-reduction pathway at depth may help to explain reports of CH{sub 4} with a semifossil age in lower peat layers. 60 refs., 7 figs., 1 tab.« less
  • The spatial variability of methane flux was examined within a large regional wetland system, the Florida Everglades. Unit area methane flux to the atmosphere from water-saturated Everglades environments, measured in situ, varied over more than an order of magnitude (4.2 to 81.9 mg CH4/sq m/d) depending on which habitat component of the ecosystem was sampled. Use of high resolution, orbital remote sensing data helped reduce uncertainty in the emission inventory of the Everglades by directing in situ sampling efforts to important habitat types and by providing a means for calculating area-weighted mean flux for the system as a whole. Themore » results indicated that spatial variability in flux within a major wetland ecosystem can introduce significant uncertainty in extrapolations to larger areas, even if the extent of the major ecosystem itself is well known. The results also suggested that the response of total ecosystem flux to changing water level is not a linear function of flooded area, but is damped, with regional flux at lowered water levels decreasing proportionally less than flooded area.« less
  • Methane (CH{sub 4}) emissions from natural wetlands comprise about a quarter of the total annual atmospheric CH{sub 4} budget. Fluxes of CH{sub 4} from mid- latitude wetlands have received less attention than those from northern latitudes because of their relatively small surface areas and low carbon stores, and fluxes in prairie wetlands have never been measured. In order to do so, we developed a large (3m tall with 1m{sup 2} area), temperature controlled static chamber to assess fluxes of CH{sub 4} and CO{sub 2} in wetlands dominated by tall (3m) emergent plants such as Phragmites, Scirpus, and Typha. Based onmore » previous work indicating that CH{sub 4} production and emission is limited by substrate quantity and quality, we set up a replicated, modified latin square design field experiment in which we added low quality C (C, as wheat straw) and high quality C (C+N, as wheat straw plus urea) to evaluate their importance in controlling CH{sub 4} emissions In Ballard`s Marsh In northern Nebraska. We measured very high CH{sub 4} emission rates (over 40 mg m{sup -2} h{sup -1}) in control plots, while disturbance associated with treatment plot establishment decreased emissions by half. Relative to the disturbance controls, the C addition lowered emissions slightly, the C+N additions increased emissions slightly, and both additions increased the proportion of CH{sub 4} emitted through bubbles. Emission rates of CH{sub 4} therefore appeared to be constrained more by N availability or substrate quality than by substrate quantity.« less