Methanogenic archaea use a bacteria-like methyltransferase system to demethoxylate aromatic compounds

Abstract

Methane-generating archaea drive the final step in anaerobic organic compound mineralization and dictate the carbon flow of Earth’s diverse anoxic ecosystems in the absence of inorganic electron acceptors. Although such Archaea were presumed to be restricted to life on simple compounds like hydrogen (H2), acetate or methanol, an archaeon, Methermicoccus shengliensis, was recently found to convert methoxylated aromatic compounds to methane. Methoxylated aromatic compounds are important components of lignin and coal, and are present in most subsurface sediments. Despite the novelty of such a methoxydotrophic archaeon its metabolism has not yet been explored. In this study, transcriptomics and proteomics reveal that under methoxydotrophic growth M. shengliensis expresses an O-demethylation/methyltransferase system related to the one used by acetogenic bacteria. Enzymatic assays provide evidence for a two step-mechanisms in which the methyl-group from the methoxy compound is (1) transferred on cobalamin and (2) further transferred on the C1-carrier tetrahydromethanopterin, a mechanism distinct from conventional methanogenic methyl-transfer systems which use coenzyme M as final acceptor. We further hypothesize that this likely leads to an atypical use of the methanogenesis pathway that derives cellular energy from methyl transfer (Mtr) rather than electron transfer (F420H2 re-oxidation) as found for methylotrophic methanogenesis.

Linking transcriptional dynamics of CH4-cycling grassland soil microbiomes to seasonal gas fluxes

“…The contribution of methanogenesis from methylated compounds to terrestrial CH 4 emissions is considered to be small [ 9 ]. However, recent research suggests it to be more important [ 10 , 13 , 81 , 82 ]. For instance, the methylotrophic Methanomassiliicoccales were the second most abundant methanogenic group in Zoige peatlands [ 83 ] and also highly abundant in wetlands in northeast Germany [ 84 ].…”

“…Acetoclastic methanogens utilize acetate, hydrogenotrophic methanogens utilize H 2 /CO 2 and formate, and methylotrophic methanogens utilize methanol/methylamines to form CH 4 [ 9 ]. Recently, methoxydotrophic methanogens that utilize methoxylated aromatic compounds were proposed as a novel methanogenic group [ 10 , 11 ]. In soils, acetoclastic and hydrogenotrophic methanogens are considered the predominant sources of CH 4 [ 9 , 12 ].…”

Expanding the phylogenetic distribution of cytochrome b-containing methanogenic archaea sheds light on the evolution of methanogenesis

“…It is likely that the "Ca. Methylarchaeales" MtrH may be involved in methyl transfer directly to H 4 MPT, as previously shown in M. shengliensis for utilization of methoxylated aromatic compounds [24]. The absence of a complete gene operon for Mtr complex suggests that the "Ca.…”

“…Methylarchaeales" were identified by searching against arCOGs and nr database using BLASTP. Reference sequences were derived from a previous study [24]. For group 4 [NiFe] hydrogenases, catalytic subunit of group 4 [NiFe] hydrogenases homologs from the "Ca.…”

Overview of Diverse Methyl/Alkyl-Coenzyme M Reductases and Considerations for Their Potential Heterologous Expression

“…Methylotrophic methanogenesis involves the activation of methylated compounds, such as methanol and trimethylamine via substrate-specific corrinoid proteins, which then transfer the methyl group into methanogenesis via CH 3 -S-CoM. The more recently discovered methoxydotrophic pathway involves methanogenesis from methoxylated aromatic compounds ( Mayumi et al, 2016 ), where the methyl group is transferred to tetrahydromethanopterin instead of coenzyme M (HS-CoM; Kurth et al, 2021a ). Finally, acetoclastic methanogenesis utilizes acetate as a methanogenesis substrate, where the carboxyl group is oxidized to CO 2 and the methyl group is reduced to CH 4 .…”