Divergent methyl-coenzyme M reductase genes in a deep-subseafloor Archaeoglobi

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.

Genomic and Transcriptomic Evidence Supports Methane Metabolism in Archaeoglobi

“…However, it should be noted that despite the largely congruent branching order in the MCR tree and genome tree for most members, incongruent positions were also observed for some traditional methanogens in this study ( Fig. 2B and C) and in several other studies (16,17). Further analysis revealed that the mcr operons in this lineage contain two extra genes, mcrC and mcrD, with unknown function (27).…”

“…The previous discovery of the basal member of Archaeoglobi, "Ca. Polytropus marinifundus," suggests the acquisition of the divergent MCR complex through a HGT event (17). In this study, however, we expanded the current knowledge by showing that (i) two separate HGT events of different types of MCR complexes, from different donors, may have occurred ( Fig.…”

“…Newly assembled Archaeoglobi MAGs, including MAGs of "Ca. Polytropus marinifundus" (Juan de Fuca Ridge, Northeast Pacific Ocean), Archaeoglobi WYZ-LMO1 (Washburn Spring, WY, USA), WYZ-LMO2 (Obsidian Pool, WY, USA), and WYZ-LMO3 (Obsidian Pool, WY, USA), were retrieved from previous studies (7,17).…”

Functional interactions between posttranslationally modified amino acids of methyl-coenzyme M reductase in Methanosarcina acetivorans

“…Although originally believed to be limited to a few taxa within the Euryarchaoeta [8], recent studies have broadened the diversity of MCR-encoding organisms to encompass all major phyla within the Archaea, including the Asgardarchaeaota, the closest known relatives to eukaryotes [9][10][11][12]. MCR homologs in some of these uncultivated organisms are thought to be involved in the anaerobic catabolism of short-chain alkanes [1,11,13,14].…”

Early acquisition of conserved, lineage-specific proteins currently lacking functional predictions were central to the rise and diversification of archaea

“…Interestingly, we recovered mcr subunits in lineages that are not considered as canonical methanogenic lineages (Evans et al 2019). These include two genomes of Bathyarchaeota related to BA1 and BA2 (GCA_002509245.1 and GCA_001399805.1) (Evans et al 2015), and one Archaeoglobi genome related to JdFR-42 (GCA_002010305) (Boyd et al 2019;Wang et al 2019). These genomes have been described as having divergent MCR genes.…”