Abstract
Multienzyme complexes catalyze important metabolic reactions in many organisms, but little is known about the complexes involved in biological methane production (methanogenesis). A crosslinking-mass spectrometry (XL-MS) strategy was employed to identify proteins associated with coenzyme M-coenzyme B heterodisulfide reductase (Hdr), an essential enzyme in all methane-producing archaea (methanogens). In Methanosarcina acetivorans, Hdr forms a multienzyme complex with acetyl-CoA decarbonylase synthase (ACDS), and F420-dependent methylene-H4MPT reductase (Mer). ACDS is essential for production of acetyl-CoA during growth on methanol, or for methanogenesis from acetate, whereas Mer is essential for methanogenesis from all substrates. Existence of a Hdr:ACDS:Mer complex is consistent with growth phenotypes of ACDS and Mer mutant strains in which the complex samples the redox status of electron carriers and directs carbon flux to acetyl-CoA or methanogenesis. We propose the Hdr:ACDS:Mer complex comprises a special class of multienzyme redox complex which functions as a “biological router” that physically links methanogenesis and acetyl-CoA biosynthesis pathways.
Highlights
Multienzyme complexes catalyze important reactions in central metabolic processes such as photosynthesis, respiration, and amino acid synthesis
The HdrD1 protein was chosen for XL-MS experiments because it contains the CoM-S-S-CoB heterodisulfide reductase active site and the gene has been shown to be essential for growth on trimethylamine, methanol, methanol + acetate, and acetate [11]
We propose that the Hdr:acetyl-CoA decarbonylase synthase (ACDS):methylene-H4MPT reductase (Mer) complex is a multienzyme ‘‘router’’ that directs substrates and electrons through either the acetyl-CoA or methanogenesis pathways by connecting the CoMS-S-CoB, acetyl-CoA, and CH3-H4MPT metabolic nodes (Figure 3c)
Summary
Multienzyme complexes catalyze important reactions in central metabolic processes such as photosynthesis, respiration, and amino acid synthesis. We wanted to determine whether multienzyme complexes are involved in the central metabolic process of biological methane production (methanogenesis) in methaneproducing archaea (methanogens). Methanogens are obligately anaerobic archaea that derive all their energy for growth by reducing carbon sources such as acetate, formate, CO2, methanol, methylamines and methyl-sulfides to methane gas. Metabolic engineering of methanogens is an attractive prospect for increasing the yield and rate of renewable methane production from biomass in anaerobic digesters. Successful metabolic engineering requires an in-depth understanding of methanogen physiology, and a knowledge of which reactions are physically linked by multienzyme complexes. A detailed, three-dimensional spatial model of methanogenesis proteins would be useful in these efforts
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