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.
Highlights
While known methanogens transfer methyl compounds using coenzyme M (CoM) as a C1 carrier [14], we suggest that the M. shengliensis ArOCH3 methyltransferase rather uses tetrahydromethanopterin (H4MPT) as final C1 carrier
An archaeal O-demethylase/methyltransferase system for methoxylated aromatic compounds has not been described previously, some genes identified in this study and mentioned above show homology with counterparts in the bacterial Mtv O-demethylation system present in the homoacetogenic bacterium Moorella thermoacetica (Pierce et al [60]; Fig. 1a, b; Supplementary Table S1)
We analysed the growth of the demethoxylating methanogen M. shengliensis on methoxylated aromatic compounds and showed that this archaeon uses a demethoxylation system (Mto) similar to those found in acetogenic bacteria
Summary
Methanogens are known to produce methane from one- to two-carbon substrates (i.e., carbon dioxide [CO2], acetate, and methylated compounds), often using (in)organic compounds as electron donors (e.g., hydrogen [H2] and formate). The environmental abundance of methoxylated aromatics indicates that methoxydotrophic archaea might play a so far unrecognized and underestimated role in methane formation and carbon cycling of coal, lignin, and other humic substances, especially in the subsurface [8]. The discovery of the methoxydotrophic ability of M. shengliensis revealed that the capacity to degrade methoxylated aromatic compounds is not confined to bacteria as previously thought, yet how M. shengliensis (and archaea) accomplish methoxydotrophic methanogenesis remains unknown. Isotope-based investigation showed that methoxydotrophic methanogenesis unprecedentedly entails both methyl disproportionation and CO2 reduction to CH4 [6], suggesting the involvement of a novel methanogenic pathway. The different entry point into methanogenesis (i.e., as CH3H4MPT rather than CH3-CoM) putatively prompts changes in energetics, thermodynamics, and kinetics that might involve an idiosyncratic C1 catabolism cycling between oxidation and reduction
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