Leu, Andy O

Abstract The methyl-coenzyme M reductase (MCR) complex is a key enzyme in archaeal methane generation and has recently been proposed to also be involved in the oxidation of short-chain hydrocarbons including methane, butane, and potentially propane. The number of archaeal clades encoding the MCR continues to grow, suggesting that this complex was inherited from an ancient ancestor, or has undergone extensive horizontal gene transfer. Expanding the representation of MCR-encoding lineages through metagenomic approaches will help resolve the evolutionary history of this complex. Here, a near-complete Archaeoglobi metagenome-assembled genome (MAG; Ca. Polytropus marinifundus gen. nov. sp. nov.) was recovered from the deep subseafloor along the Juan de Fuca Ridge flank that encodes two divergent McrABG operons similar to those found in Ca. Bathyarchaeota and Ca. Syntrophoarchaeum MAGs. Ca. P. marinifundus is basal to members of the class Archaeoglobi, and encodes the genes for β-oxidation, potentially allowing an alkanotrophic metabolism similar to that proposed for Ca. Syntrophoarchaeum. Ca. P. marinifundus also encodes a respiratory electron transport chain that can potentially utilize nitrate, iron, and sulfur compounds as electron acceptors. Phylogenetic analysis suggests that the Ca. P. marinifundus MCR operons were horizontally transferred, changing our understanding of the evolution and distribution of this complex in the Archaea.

Abstract Microbially mediated anaerobic oxidation of methane (AOM) is a key process in the regulation of methane emissions to the atmosphere. Iron can serve as an electron acceptor for AOM, and it has been suggested that Fe(III)-dependent AOM potentially comprises a major global methane sink. Although it has been proposed that anaerobic methanotrophic (ANME) archaea can facilitate this process, their active metabolic pathways have not been confirmed. Here we report the enrichment and characterisation of a novel archaeon in a laboratory-scale bioreactor fed with Fe(III) oxide (ferrihydrite) and methane. Long-term performance data, in conjunction with the 13C- and 57Fe-labelling batch experiments, demonstrated that AOM was coupled to Fe(III) reduction to Fe(II) in this bioreactor. Metagenomic analysis showed that this archaeon belongs to a novel genus within family Candidatus Methanoperedenaceae, and possesses genes encoding the “reverse methanogenesis” pathway, as well as multi-heme c-type cytochromes which are hypothesised to facilitate dissimilatory Fe(III) reduction. Metatranscriptomic analysis revealed upregulation of these genes, supporting that this archaeon can independently mediate AOM using Fe(III) as the terminal electron acceptor. We propose the name Candidatus “Methanoperedens ferrireducens” for this microorganism. The potential role of “M. ferrireducens” in linking the carbon and iron cycles in environments rich in methane and iron should be investigated in future research.