Several ways one goal-methanogenesis from unconventional substrates

Abstract

Methane is the second most important greenhouse gas on earth. It is produced by methanogenic archaea, which play an important role in the global carbon cycle. Three main methanogenesis pathways are known: in the hydrogenotrophic pathway H₂ and carbon dioxide are used for methane production, whereas in the methylotrophic pathway small methylated carbon compounds like methanol and methylated amines are used. In the aceticlastic pathway, acetate is disproportionated to methane and carbon dioxide. However, next to these conventional substrates, further methanogenic substrates and pathways have been discovered. Several phylogenetically distinct methanogenic lineages (Methanosphaera, Methanimicrococcus, Methanomassiliicoccus, Methanonatronarchaeum) have evolved hydrogen-dependent methylotrophic methanogenesis without the ability to perform either hydrogenotrophic or methylotrophic methanogenesis. Genome analysis of the deep branching Methanonatronarchaeum revealed an interesting membrane-bound hydrogenase complex affiliated with the hardly described class 4 g of multisubunit hydrogenases possibly providing reducing equivalents for anabolism. Furthermore, methylated sulfur compounds such as methanethiol, dimethyl sulfide, and methylmercaptopropionate were described to be converted into adapted methylotrophic methanogenesis pathways of Methanosarcinales strains. Moreover, recently it has been shown that the methanogen Methermicoccus shengliensis can use methoxylated aromatic compounds in methanogenesis. Also, tertiary amines like choline (N,N,N-trimethylethanolamine) or betaine (N,N,N-trimethylglycine) have been described as substrates for methane production in Methanococcoides and Methanolobus strains. This review article will provide in-depth information on genome-guided metabolic reconstructions, physiology, and biochemistry of these unusual methanogenesis pathways. KEY POINTS: • Newly discovered methanogenic substrates and pathways are reviewed for the first time. • The review provides an in-depth analysis of unusual methanogenesis pathways. • The hydrogenase complex of the deep branching Methanonatronarchaeum is analyzed.

Keywords: Archaea; Extended substrate range; Methane production; Novel pathways.

Fig. 1

Hydrogenotrophic (a), methylotrophic (b) and aceticlastic (c) methanogenesis pathways. The ferredoxin electron carrier is a two-electron carrier. Some methanogens use a H₄MPT derivative called tetrahydrosarcinopterin (H₄SPT). The Na⁺/H⁺ translocation stoichiometry is not represented in the figure. FwdA-F/FmdA-F: formylmethanofuran dehydrogenase, Ftr: formylmethanofuran-tetrahydromethanopterin formyl-transferase, Mch: methenyl-tetrahydromethanopterin cyclohydrolase, Mtd: methylenetetrahydromethanopterin dehydrogenase, Mer: 5,10-methylenetetrahydromethanopterin reductase, MtrA-H: tetrahydromethanopterin S-methyl-transferase, McrABCDG methyl-coenzyme M reductase, FrhABG: coenzyme F₄₂₀-reducing hydrogenase, HdrABC: soluble heterodisulfide reductase, MvhAGD: F₄₂₀-non-reducing hydrogenase, FdhAB: formate dehydrogenase, FpoA-O: F₄₂₀H₂ dehydrogenase, HdrDE: membrane-bound heterodisulfide reductase, Ech-H₂ase: energy-converting hydrogenase, Rnf: Na⁺-translocating ferredoxin:NAD⁺ oxidoreductase complex, ATPase: ATP synthase, CODH-ACS: Acetyl-CoA decarbonylase/synthase, MTI and MTII: methyltransferase, CoB: coenzyme B, CoM: coenzyme M, H₄MPT: tetrahydromethanopterin, MFR: methanofuran, Fd: ferredoxin, F₄₂₀H₂: reduced coenzyme F₄₂₀, MP: methanophenazine, CO(III): cobalamin binding protein

Fig. 2

Evolutionary relationships of methyl-coenzyme M reductase (subunit A) of different methanogens. The evolutionary history was inferred using the Neighbor-Joining method. The optimal tree with the sum of branch length = 3.29201331 is shown. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (500 replicates) are shown next to the branches. The tree is drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree. The evolutionary distances were computed using the Dayhoff matrix-based method and are in the units of the number of amino acid substitutions per site. The analysis involved 29 amino acid sequences. All ambiguous positions were removed for each sequence pair. There were a total of 583 positions in the final dataset. Evolutionary analyses were conducted in MEGA7 (Kumar et al. 2016). MA: methylamines, MS: methylated sulfur compounds, TA: tertiary amines, QA: quaternary amines

Fig. 3

Extended substrate range of methanogens. 2-Methoxybenzoate is only one example for methoxylated aromatic compounds that can be used for methanogenesis (Mayumi et al. 2016)

Fig. 4

Methanogenesis pathway in Methanimicrococcus blatticola (a), Methanosphaera stadtmanae (b), Methanomassiliicoccus luminyensis (c), and Methanonatronarchaeum thermophilum (d) Question marks mark proteins which are encoded in the distinctive genome, but their abundance and function in the cell are yet unclear. The ferredoxin electron carrier is a 2-electron carrier. Some methanogens use a H₄MPT derivative called tetrahydrosarcinopterin (H₄SPT). The Na⁺/H⁺ translocation stoichiometry is not represented in the figure. FwdA-F/FmdA-F: formylmethanofuran dehydrogenase, Ftr: formylmethanofuran-tetrahydromethanopterin formyl-transferase, Mch: methenyl-tetrahydromethanopterin cyclohydrolase, Mtd: methylenetetrahydromethanopterin dehydrogenase, Mer: 5,10-methylenetetrahydromethanopterin reductase, MtrA-H: tetrahydromethanopterin S-methyl-transferase, McrABCDG methyl-coenzyme M reductase, FrhABG: coenzyme F₄₂₀-reducing hydrogenase, HdrABC: soluble heterodisulfide reductase, MvhAGD: F₄₂₀-non-reducing hydrogenase, FdhABI: formate dehydrogenase (FdhI contains a b-type heme), FpoA-O: F₄₂₀H₂ dehydrogenase, HdrDE: membrane bound heterodisulfide reductase, EhbA-Q: energy-conserving hydrogenase, VhtGACD: [NiFe]-hydrogenase, HyaAB: H₂-producing hydrogenase, 4 g Hyd: 4 g-type hydrogenase, ATPase: ATP synthase, MTI and MTII: methyltransferase, CoB: coenzyme B, CoM: coenzyme M, H₄MPT: tetrahydromethanopterin, MFR: methanofuran, Fd: ferredoxin, F₄₂₀H₂: reduced coenzyme F₄₂₀, MP: methanophenazine, CO(III): cobalamin binding protein.

Fig. 5

Methanogenesis from methylated sulfur compounds or tertiary and quaternary amines (a) and from methoxylated aromatic compounds in Methermicoccus shengliensis (b). Panel c shows the proteins that are involved in methyl transfer for diverse substrates. The question mark indicates that there is no biochemical evidence yet if the methyl group is transferred to H₄MPT or CoM during growth on methoxy compounds. For growth on methoxy compounds proteins similar to the O-demethylase MtvB and the methyltransferase MtrH are most likely involved in the methyl transfer. Some methanogens use a H₄MPT derivative called tetrahydrosarcinopterin (H₄SPT). The Na⁺/H⁺ translocation stoichiometry is not represented in the figure. FwdA-F/FmdA-F: formylmethanofuran dehydrogenase, Ftr: formylmethanofuran-tetrahydromethanopterin formyl-transferase, Mch: methenyl-tetrahydromethanopterin cyclohydrolase, Mtd: methylenetetrahydromethanopterin dehydrogenase, Mer: 5,10-methylenetetrahydromethanopterin reductase, MtrA-H: tetrahydromethanopterin S-methyl-transferase, McrABCDG methyl-coenzyme M reductase, MTI, and MTII: methyltransferase, CoB: coenzyme B, CoM: coenzyme M, H₄MPT: tetrahydromethanopterin, MFR: methanofuran, CO(III): cobalamin binding protein, MtrH: tetrahydromethanopterin S-methyltransferase subunit H