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.

Fig. 1

McrA gene phylogeny and genome tree phylogeny. Maximum-likelihood trees of a McrA proteins, and b a concatenated alignment of 122 single copy archaeal marker genes from high quality archaeal RefSeq genomes (release 80). Hydrogenotrophic and acetoclastic methanogens are shaded blue, H₂-dependent methylotrophic methanogens are shaded green, known/putative methane oxidizers are shaded yellow, and lineages encoding divergent McrAs are shaded red. Bootstrap support was generated from 100 replicates, and white, gray and black nodes represent ≥50%, ≥75%, and ≥90% support, respectively

Fig. 2

Metabolic reconstruction of the Ca. P. marinifundus genome. Metabolic reconstruction of the Ca. P. marinifundus genome. a Respiratory and fermentative pathways are shaded blue and red, respectively. b Proposed CoM-S-S-CoB disulfide regeneration and membrane energetics of Ca. P. marinifundus are shown. Genes associated with the pathways shown can be found in Supplementary Table 1

Fig. 3

Operons encoding redox active complexes within Ca. P. marinifundus. White arrows represent hypothetical proteins. Networks are of MHCs and represent clusters of related proteins and their organism of origin

Fig. 4

Comparative genomics of the Ca. P. marinifundus genome. a PCA of the presence/absence of KEGG Orthologous (KO) genes in all archaea, b within the Euryarchaeota, with the exception of the Haloarchaea, and c within the Archaeoglobi