The Biochemistry and Physiology of Respiratory-Driven Reversed Methanogenesis
In situ ecological and metagenomic investigations have provided a wealth of information setting the stage for advanced mechanistic understanding of the anaerobic oxidation of methane (AOM). These studies infer that anaerobic methylotrophic (ANME) species of the domain Archaea are capable of growth by reducing electron acceptors such as Fe(III) and nitrate. However, the unavailability of axenic cultures has impeded a mechanistic understanding of nitrate-dependent AOM. Nonetheless, the reconstructed genomes from nitrate-reducing AOM environments predict pathways consistent with reversal of methanogenic pathways. The methane-producing archaeon Methanosarcina acetivorans is capable of AOM dependent on reduction of Fe(III) for which a pathway is proposed. The pathway is consistent with the reversal of methanogenesis pathways deduced from the reconstructed genomes derived from metagenomes of environments where Fe(III)-dependent ANME are expected. Roles are indicated for electron bifurcation by HdrABC family enzymes and the Rnf complex which appears to be a universal requirement for energy conservation during AOM. An updated genome-scale metabolic model of M. acetivorans correctly captures the observed energy requirements and electron flow mechanism during AOM and predicts the interplay between Fe(III) availability and the partitioning of the incoming carbon flux from methane into acetate and carbon dioxide. The model also predicts a plausible switching mechanism for ATP production between chemiosmotic and substrate-level phosphorylations depending on the availability of Fe(III).
Research in the laboratories of CDM and JGF was supported by the US Department of Energy ARPA-e grant 0881-1525.
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