Abstract
Consumption of methane by aerobic and anaerobic microbes governs the atmospheric level of this powerful greenhouse gas. Whereas a biochemical understanding of aerobic methanotrophy is well developed, a mechanistic understanding of anaerobic methanotrophy has been prevented by the unavailability of pure cultures. Here we report a biochemical investigation of Methanosarcina acetivorans, a methane-producing species capable of anaerobic methanotrophic growth dependent on reduction of Fe(III). Our findings support a pathway anchored by Fe(III)-dependent mechanisms for energy conservation driving endergonic reactions that are key to methanotrophic growth. The pathway is remarkably similar to pathways hypothesized for uncultured anaerobic methanotrophic archaea. The results contribute to an improved understanding of the methane cycle that is paramount to understanding human interventions influencing Earth’s climate. Finally, the pathway enables advanced development and optimization of biotechnologies converting methane to value-added products through metabolic engineering of M. acetivorans.
Highlights
Consumption of methane by aerobic and anaerobic microbes governs the atmospheric level of this powerful greenhouse gas
Based on environmental metagenomic and transcriptomic analyses, anaerobic oxidation of methane (AOM) pathways are proposed for ANME that include membrane-bound components involved in energy conservation (Rnf and Fpo complexes), electron transport (CoMS-SCoB heterodisulfide reductase (HdrDE); multi-heme c-type cytochromes (MHC); and methanophenazine (MP)) and methyl transfer (methyl-tetrahydrosarcinapterin:coenzyme M methyltransferase (Mtr))[5,6,19,20,21]
Driving endergonic methane oxidation to the methyl level. The finding that both acetate and CO2 are produced during trace methane oxidation (TMO) and AOM by M. acetivorans indicates a dependence on reversal of aescseetnoctilaalstmic oadnidficCaOtio2n-rse1d3u–1c5in. gThmeetfihrasntotgweonicrepaactthiownasysr,eaqlubierietdwfiothr reversal are methane oxidation yielding methyl-coenzyme M (CH3SCoM) and transfer of the methyl group to tetrahydrosarcinapterin (H4SPT)
Summary
Consumption of methane by aerobic and anaerobic microbes governs the atmospheric level of this powerful greenhouse gas. We report a biochemical investigation of Methanosarcina acetivorans, a methane-producing species capable of anaerobic methanotrophic growth dependent on reduction of Fe(III). The anaerobic oxidation of methane (AOM) requires reduction of electron acceptors (Fe(III), Mn(IV), nitrate or sulfate) to be thermodynamically favorable[5,6]. It was thought that AOM in marine sediments required a symbiosis of anaerobic methanotrophic archaea (ANME) and sulfate-reducing species for which the latter utilizes reductant produced by the former to make the overall reaction thermodynamically favorable. We report a biochemical investigation of wild-type M. acetivorans that supports an AOM pathway anchored by Fe(III)-dependent respiration generating ion gradients that supply the energy to drive endergonic reactions essential for AOM and growth. The results provide a deeper mechanistic understanding of AOM and iron cycling in Nature, and a guide for optimization of methane-based biotechnologies
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