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Waterfalls enhance regional methane emissions by enabling dissolved methane to bypass microbial oxidation
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ABSTRACT Biological nitrogen fixation is catalyzed by the enzyme nitrogenase. Two forms of this metalloenzyme, the vanadium (V)- and iron (Fe)-only nitrogenases, were recently found to reduce small amounts of carbon dioxide (CO 2 ) into the potent greenhouse gas methane (CH 4 ). Here, we report carbon ( 13 C/ 12 C) and hydrogen ( 2 H/ 1 H) stable isotopic compositions and fractionations of methane generated by V- and Fe-only nitrogenases in the metabolically versatile nitrogen fixer Rhodopseudomonas palustris . The stable carbon isotope fractionation imparted by both forms of alternative nitrogenase are within the range observed for hydrogenotrophic methanogenesis ( 13 α CO2/CH4 = 1.051 ± 0.002 for V-nitrogenase and 1.055 ± 0.001 for Fe-only nitrogenase; values are means ± standard errors). In contrast, the hydrogen isotope fractionations ( 2 α H2O/CH4 = 2.071 ± 0.014 for V-nitrogenase and 2.078 ± 0.018 for Fe-only nitrogenase) are the largest of any known biogenic or geogenic pathway. The large 2 α H2O/CH4 shows that the reaction pathway nitrogenases use to form methane strongly discriminates against 2 H, and that 2 α H2O/CH4 distinguishes nitrogenase-derived methane from all other known biotic and abiotic sources. These findings on nitrogenase-derived methane will help constrain carbon and nitrogen flows in microbial communities and the role of the alternative nitrogenases in global biogeochemical cycles. IMPORTANCE All forms of life require nitrogen for growth. Many different kinds of microbes living in diverse environments make inert nitrogen gas from the atmosphere bioavailable using a special enzyme, nitrogenase. Nitrogenase has a wide substrate range, and, in addition to producing bioavailable nitrogen, some forms of nitrogenase also produce small amounts of the greenhouse gas methane. This is different from other microbes that produce methane to generate energy. Until now, there was no good way to determine when microbes with nitrogenases are making methane in nature. Here, we present an isotopic fingerprint that allows scientists to distinguish methane from microbes making it for energy versus those making it as a by-product of nitrogen acquisition. With this new fingerprint, it will be possible to improve our understanding of the relationship between methane production and nitrogen acquisition in nature.more » « less
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Abstract The ongoing global temperature rise enhances permafrost thaw in the Arctic, allowing Pleistocene‐aged frozen soil organic matter to become available for microbial degradation and production of greenhouse gases, particularly methane. Here, we examined the extent and mechanism of anaerobic oxidation of methane (AOM) in the sediments of four interior Alaska thermokarst lakes, which formed and continue to expand as a result of ice‐rich permafrost thaw. In cores of surface (~ 1 m) lake sediments we quantified methane production (methanogenesis) and AOM rates using anaerobic incubation experiments in low (4°C) and high (16°C) temperatures. Methanogenesis rates were measured by the accumulation of methane over ~ 90 d, whereas AOM rates were measured by adding labeled‐13CH4and measuring the produced dissolved inorganic13C. Our results demonstrate that while methanogenesis was vigorous in these anoxic sediments, AOM was lower by two orders of magnitude. In almost all sediment depths and temperatures, AOM rates remained less than 2% of the methanogenesis rates. Experimental evidence indicates that the AOM is strongly related to methanogens, as the addition of a methanogens' inhibitor prevented AOM. Variety of electron acceptor additions did not stimulate AOM, and methanotrophs were scarcely detected. These observations suggest that the AOM signals in the incubation experiments might be a result of enzymatic reversibility (“back‐flux”) during CH4production, rather than thermodynamically favorable AOM. Regardless of the mechanism, the quantitative results show that near surface (< 1‐m) thermokarst sediments in interior Alaska have little to no buffer mechanisms capable of attenuating methane production in a warming climate.more » « less
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null (Ed.)Reports of biogenic methane (CH 4 ) synthesis associated with a range of organisms have steadily accumulated in the literature. This has not happened without controversy and in most cases the process is poorly understood at the gene and enzyme levels. In marine and freshwater environments, CH 4 supersaturation of oxic surface waters has been termed the “methane paradox” because biological CH 4 synthesis is viewed to be a strictly anaerobic process carried out by O 2 -sensitive methanogens. Interest in this phenomenon has surged within the past decade because of the importance of understanding sources and sinks of this potent greenhouse gas. In our work on Yellowstone Lake in Yellowstone National Park, we demonstrate microbiological conversion of methylamine to CH 4 and isolate and characterize an Acidovorax sp. capable of this activity. Furthermore, we identify and clone a gene critical to this process (encodes pyridoxylamine phosphate-dependent aspartate aminotransferase) and demonstrate that this property can be transferred to Escherichia coli with this gene and will occur as a purified enzyme. This previously unrecognized process sheds light on environmental cycling of CH 4 , suggesting that O 2 -insensitive, ecologically relevant aerobic CH 4 synthesis is likely of widespread distribution in the environment and should be considered in CH 4 modeling efforts.more » « less
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Abstract Tidal salt marshes produce and emit CH4. Therefore, it is critical to understand the biogeochemical controls that regulate CH4spatial and temporal dynamics in wetlands. The prevailing paradigm assumes that acetoclastic methanogenesis is the dominant pathway for CH4production, and higher salinity concentrations inhibit CH4production in salt marshes. Recent evidence shows that CH4is produced within salt marshes via methylotrophic methanogenesis, a process not inhibited by sulfate reduction. To further explore this conundrum, we performed measurements of soil–atmosphere CH4and CO2fluxes coupled with depth profiles of soil CH4and CO2pore water gas concentrations, stable and radioisotopes, pore water chemistry, and microbial community composition to assess CH4production and fate within a temperate tidal salt marsh. We found unexpectedly high CH4concentrations up to 145,000 μmol mol−1positively correlated with S2−(salinity range: 6.6–14.5 ppt). Despite large CH4production within the soil, soil–atmosphere CH4fluxes were low but with higher emissions and extreme variability during plant senescence (84.3 ± 684.4 nmol m−2 s−1). CH4and CO2within the soil pore water were produced from young carbon, with most Δ14C‐CH4and Δ14C‐CO2values at or above modern. We found evidence that CH4within soils was produced by methylotrophic and hydrogenotrophic methanogenesis. Several pathways exist after CH4is produced, including diffusion into the atmosphere, CH4oxidation, and lateral export to adjacent tidal creeks; the latter being the most likely dominant flux. Our findings demonstrate that CH4production and fluxes are biogeochemically heterogeneous, with multiple processes and pathways that can co‐occur and vary in importance over the year. This study highlights the potential for high CH4production, the need to understand the underlying biogeochemical controls, and the challenges of evaluating CH4budgets and blue carbon in salt marshes.more » « less
