Simultaneous Oxidation of Atmospheric Methane, Carbon Monoxide and Hydrogen for Bacterial Growth

Abstract

The second largest sink for atmospheric methane (CH4) is atmospheric methane oxidizing-bacteria (atmMOB). How atmMOB are able to sustain life on the low CH4 concentrations in air is unknown. Here, we show that during growth, with air as its only source for energy and carbon, the recently isolated atmospheric methane-oxidizer Methylocapsa gorgona MG08 (USCα) oxidizes three atmospheric energy sources: CH4, carbon monoxide (CO), and hydrogen (H2) to support growth. The cell-specific CH4 oxidation rate of M. gorgona MG08 was estimated at ~0.7 × 10−18 mol cell−1 h−1, which, together with the oxidation of CO and H2, supplies 0.38 kJ Cmol−1 h−1 during growth in air. This is seven times lower than previously assumed necessary to support bacterial maintenance. We conclude that atmospheric methane-oxidation is supported by a metabolic flexibility that enables the simultaneous harvest of CH4, H2 and CO from air, but the key characteristic of atmospheric CH4 oxidizing bacteria might be very low energy requirements.

The Influence of Above-Ground Herbivory on the Response of Arctic Soil Methanotrophs to Increasing CH4 Concentrations and Temperatures

“…To consider the different solubility of CH 4 in pore water at 8 • C and 15 • C, the CH 4 oxidation rates for the same dissolved concentrations of CH 4 were estimated. Assuming first-order rate kinetics, as previously shown in [44], we log-transformed the decline in CH 4 over time and fitted linear regression models to the transformed plots. The slopes of the linear models correspond to the rate constants.…”

“…Assuming first-order rate kinetics, as previously shown in [44], we log-transformed the cell-normalized decline in CH 4 over time and fitted linear regression models to the transformed plots. The slopes of the linear models correspond to the rate constants.…”

“…The slopes of the linear models correspond to the rate constants. By multiplying the respective rate constant by the desired concentration of CH 4 , we obtained the rates of oxidation at these concentrations [44]. The fit of the linear models was evaluated and considered to have satisfactory coefficients of determination, giving the following values: R 2 -8 • C = 0.83-0.99, R 2 -15 • C = 0.72-0.99; 24 of the 28 linear models had an R 2 of > 0.9.…”

“…Some of the "unconditional bioindicator OTUs" for 1% CH 4 clustered with high-Arctic Methylobacter isolates retrieved from CH 4 -rich ecosystems [31,32], while the phylogenetic clusters containing the "unconditional bioindicator OTUs" for 0.1% CH 4 did not contain closely related isolates. Atmospheric MOB are phylogenetically distinct but closely related to conventional MOB [24,64] and are characterized by a more efficient energy metabolism [44]. Similarly, phylogenetically different populations of ammonia-oxidizing Archaea are associated with different ammonia oxidation uptake rates [65,66], and different ammonia oxidation kinetics reflect different life strategies [65].…”

Out of Thin Air? Astrobiology and Atmospheric Chemotrophy

“…The newly discovered assimilatory type 1h [Ni-Fe]-hydrogenases appear to be uniquely involved in scavenging of atmospheric H 2 for energy generation (Constant et al, 2010 ; Greening et al, 2014 , 2015 , 2016; Liot and Constant, 2016 ). Along with carbon monoxide dehydrogenases, these enzymes enable the use of H 2 and CO as electron donors for the aerobic respiratory chain, primarily to support cellular survival, but also in some cases growth (Jordaan et al, 2020 ; Tveit et al, 2021 ). To date, assimilatory hydrogenases have been identified in taxonomically diverse species of prokaryotes, with organisms harboring [NiFe]-hydrogenase encoding genes distributed across a significant number of soil taxa, currently spanning 36 bacterial and 6 archaeal phyla (Vignais and Billoud, 2007 ; Greening et al, 2016 ).…”