Methanogenesis and the Wood-Ljungdahl Pathway: An Ancient, Versatile, and Fragile Association

Abstract

Methanogenesis coupled to the Wood-Ljungdahl pathway is one of the most ancient metabolisms for energy generation and carbon fixation in the Archaea. Recent results are sensibly changing our view on the diversity of methane-cycling capabilities in this Domain of Life. The availability of genomic sequences from uncharted branches of the archaeal tree has highlighted the existence of novel methanogenic lineages phylogenetically distant to previously known ones, such as the Methanomassiliicoccales. At the same time, phylogenomic analyses have suggested a methanogenic ancestor for all Archaea, implying multiple independent losses of this metabolism during archaeal diversification. This prediction has been strengthened by the report of genes involved in methane cycling in members of the Bathyarchaeota (a lineage belonging to the TACK clade), representing the first indication of the presence of methanogenesis outside of the Euryarchaeota. In light of these new data, we discuss how the association between methanogenesis and the Wood-Ljungdahl pathway appears to be much more flexible than previously thought, and might provide information on the processes that led to loss of this metabolism in many archaeal lineages. The combination of environmental microbiology, experimental characterization and phylogenomics opens up exciting avenues of research to unravel the diversity and evolutionary history of fundamental metabolic pathways.

Keywords: Archaea; Wood–Ljungdahl pathway; archaeal ancestor; methanogenesis; pathway loss.

Fig. 1.—

Schematic views of the archaeal phylogeny including complete genomes available before 2012 (A) and currently (B), based on the literature (see text for details). Fast evolving DPANN lineages are not included as their position is unclear. Red arrows indicate the inferred origin of methanogenesis, with further divergence leading to lineages that retained this metabolism based on experimental characterization or the presence of MCR homologues (in red). Colored circles indicate the type of known and predicted pathways in representatives of the lineages according to the descriptive panel.

Fig. 2.—

Different configurations for the associated or independent functioning of the archaeal version of the Wood-Ljungdahl (WL) pathway and methanogenesis. Missing enzymatic complexes and related reactions are shaded in gray. (A) CO₂-reducing methanogenesis as present in Class I and Class II methanogens without cytochromes. (B) Methanogenesis by reduction of methyl-compounds using H₂ as present in Methanomassiliicoccales. (C) Methanogenesis by reduction of methyl-compounds using H₂ as inferred in Bathyarchaeota BA1, and potential link with the WL pathway in absence of MTR. (D) Carbon fixation using the archaeal WL pathway in absence of methanogenesis, and proposal of a mechanism to generate low potential ferredoxin (Fd_red²⁻) during sulphate reduction in the case of Archaeoglobales. Carbon fluxes originating from CO₂ or methyl-compounds are shown by red arrows, and carbon fluxes from other sources by blue arrows. Green arrows indicate electron transfers associated with ferredoxins reduction or oxidation. The dotted green arrows in (B) and (C) integrate the electron bifurcation process leading to the generation of an Fd_red²⁻ by the Hdr/Mvh complex as described in (A). The reduction of heterodisulfide by Fd_red²⁻ in (B) and the reduction of 2H⁺ by Fd_red²⁻ in (C) that are coupled to proton translocation across the membrane are not shown. Abbreviations are as follows: MBWL, methyl-branch of the WL pathway; CBWL, carbonyl-branch of the WL pathway; MTR, N⁵-methyltetrahydromethanopterin: coenzyme M methyltransferase complex; MCR, methyl-coenzyme M reductase complex; Hdr, cytoplasmic heterodisulfide reductase complex; Mvh, F420-non-reducing hydrogenase complex; Hdl, cytoplasmic heterodisulfide reductase-like complex; Ech, Energy converting hydrogenase complex; Fpo, truncated F₄₂₀H₂ hydrogenase; H₄MPT, tetrahydromethanopterin; CoM–S–H, coenzyme M; CoB–S–H, coenzyme B; CoM–S–S–CoB, heterodisulfide; Fd/Fd_red²⁻, oxidized/reduced low potential ferredoxin; R-CH₃, methylated compound such as methanol or methylamines; DsrC>S, DsrC trisulfide.