Expanding anaerobic alkane metabolism in the domain of Archaea

Abstract

Methanogenesis and anaerobic methane oxidation through methyl-coenzyme M reductase (MCR) as a key enzyme have been suggested to be basal pathways of archaea 1 . How widespread MCR-based alkane metabolism is among archaea, where it occurs and how it evolved remain elusive. Here, we performed a global survey of MCR-encoding genomes based on metagenomic data from various environments. Eleven high-quality mcr-containing metagenomic-assembled genomes were obtained belonging to the Archaeoglobi in the Euryarchaeota, Hadesarchaeota and different TACK superphylum archaea, including the Nezhaarchaeota, Korarchaeota and Verstraetearchaeota. Archaeoglobi WYZ-LMO1 and WYZ-LMO3 and Korarchaeota WYZ-LMO9 encode both the (reverse) methanogenesis and the dissimilatory sulfate reduction pathway, suggesting that they have the genomic potential to couple both pathways in individual organisms. The Hadesarchaeota WYZ-LMO4-6 and Archaeoglobi JdFR-42 encode highly divergent MCRs, enzymes that may enable them to thrive on non-methane alkanes. The occurrence of mcr genes in different archaeal phyla indicates that MCR-based alkane metabolism is common in the domain of Archaea.Since the emergence of life on our planet, anaerobic methane metabolism, including methanogenesis and methane oxidation, has been a crucial element in the Earth's carbon cycle 1 , and both processes are key to the global methane budget. Methanogenic archaea produce ~500-600 Tg of methane per year 2 , whereas anaerobic methane-oxidizing archaea (ANME) oxidize a large portion of methane within the seafloor before it reaches the water column 3,4 . The metabolic pathways of methane formation and anaerobic oxidation of methane are largely identical, as both contain exclusively C 1 -compound-transforming enzymes that were described originally in the methanogenesis pathway [5][6][7] .Among these enzymes, methyl-coenzyme M (CoM) reductase (MCR) plays the crucial role 8 . In methanogens, MCR reduces CH 3 -CoM to CH 4 (refs. 9,10 ), whereas in ANMEs, this enzyme activates CH 4 to form CH 3 -CoM as the primary intermediate 5 . This canonical MCR type is highly conserved, and the gene encoding the α-subunit (mcrA) of the enzyme complex has been used as a diagnostic marker for the detection and phylogenetic classification of methanogens and ANMEs 11 . The presence of MCR was thought to be limited to the phylum Euryarchaeota, yet the occurrence of mcr genes in metagenome-assembled genomes (MAGs) of the Bathyarchaeota 12 and Verstraetearchaeota 13 has indicated a much wider distribution of this gene within archaea. In addition, highly divergent MCR types have been identified in two strains of the thermophilic Ca. Syntrophoarchaeum spp. that use the encoded enzymes to activate

Genomic and Transcriptomic Evidence Supports Methane Metabolism in Archaeoglobi

“…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).…”

“…1; see also Fig. 2A and C), were downloaded from the NCBI database and included into this study (7).…”

Spatiotemporal dynamics of the archaeal community in coastal sediments: assembly process and co-occurrence relationship

“…In particular, it has been found that archaea are functionally diverse, being capable of ammonia oxidation, methane metabolism, and organic matter degradation [6][7][8]. Novel archaeal phyla with unusual metabolic potentials are still being discovered, for example, Nezhaarchaeota and Helarchaeota, two new archaeal phyla identified in 2019, were found to possess the potential for anaerobic short-chain hydrocarbon cycling [9,10]. In contrast to the increasing knowledge gleaned from archaeal community composition and metabolic capacity characterization, much less is known about the spatiotemporal dynamics of archaeal community distribution, their assembly mechanism, and inter taxa association in sediments [11,12].…”

Thermogenic hydrocarbons fuel a redox stratified subseafloor microbiome in deep sea cold seep sediments

“…Notably, the recently described process of multi-carbon alkane oxidation by archaea co-occurs with anaerobic methane oxidation by ANME archaea. Previous observations of these phenomena have mainly featured hydrothermal vent environments 15, 22, 38 whereas this deep sea setting experiences permanently low temperatures. Methane oxidizers are most abundant, in agreement with the high concentration of methane; however, by investigating an environment that also has relatively high concentrations of C 2+ gases, the potential and importance of both GoM-Arc1- and Syntrophoarchaeaum - like archaea degrading thermogenic hydrocarbons in cold seep sediments is shown for the first time.…”

“…Numerous studies have focused on anaerobic oxidation of methane, since methane generally is the dominant hydrocarbon in cold seep fluids. This process is mediated by anaerobic methanotrophic archaea (ANME) through the reverse methanogenesis pathway, typically in syntrophy with bacteria that can reduce electron acceptors such as sulfate, nitrate, and metal oxides 8, 15, 16 . Investigations of enrichment cultures have also revealed anaerobic bacterial or archaeal oxidation of non-methane alkanes and aromatic hydrocarbons, including ethane (e.g.…”