Abstract
Recent studies indicate that environmentally abundant quaternary amines (QAs) are a primary source for methanogenesis, yet the catabolic enzymes are unknown. We hypothesized that the methanogenic archaeon Methanolobus vulcani B1d metabolizes glycine betaine (GB) through a corrinoid-dependent GB:coenzyme M (CoM) methyl transfer pathway. The draft genome sequence of M. vulcani B1d revealed a gene encoding a predicted non-pyrrolysine MttB homolog (MV8460) with high sequence similarity to the GB methyltransferase encoded by Desulfitobacterium hafniense Y51. MV8460 catalyzes GB-dependent methylation of free cob(I)alamin indicating it is an authentic MtgB enzyme. Proteomic analysis revealed that MV8460 and a corrinoid binding protein (MV8465) were highly abundant when M. vulcani B1d was grown on GB relative to growth on trimethylamine. The abundance of a corrinoid reductive activation enzyme (MV10335) and a methylcorrinoid:CoM methyltransferase (MV10360) were significantly higher in GB-grown B1d lysates compared to other homologs. The GB:CoM pathway was fully reconstituted in vitro using recombinant MV8460, MV8465, MV10335, and MV10360. Demonstration of the complete GB:CoM pathway expands the knowledge of direct QA-dependent methylotrophy and establishes a model to identify additional ecologically relevant anaerobic quaternary amine pathways.
Highlights
Methane is a greenhouse gas with approximately 28 times greater potency than carbon dioxide (CO2) and is an important common fuel source (Auffret et al, 2017)
We recently showed that one non-Pyl MttB homolog from Desulfitobacterium hafniense Y51 (DhMtgB) is a glycine betaine (GB) methyltransferase, suggesting a role of this family in breaking down higher order methylated ammonium compounds (Ticak et al, 2014)
GB-grown B1d compared to methanolor TMA-grown B1d showed significant increases in MV8460 (Figure 1 and Supplementary Figure S1), a putative Pyl-lacking homolog of MttB from the COG5598 superfamily
Summary
Methane is a greenhouse gas with approximately 28 times greater potency than carbon dioxide (CO2) and is an important common fuel source (Auffret et al, 2017). The atmospheric concentration of methane is increasing (Yvon-Durocher et al, 2014) and this increase triggers feedback loops by releasing carbon from the permafrost in polar regions leading to increased methanogenesis (Olefeldt et al, 2013; Deng et al, 2017). Methanogenesis increases in response to elevated temperature, and methanogens demonstrate a larger temperature dependent. Glycine Betaine-Dependent Methanogenesis Pathway flux than photosynthetic and other CO2 respiring organisms (Yvon-Durocher et al, 2014). Methane represents a larger percentage of increased atmospheric carbon emissions in response to warming (Yvon-Durocher et al, 2014). Our ability to predict future increases in methane relies upon expanding our knowledge of methanogenesis mechanisms, including those from higher order methylated ammonium compounds which are environmentally abundant (Mausz and Chen, 2019)
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