Abstract
Symbiotic digestion of lignocellulose in the hindgut of higher termites is mediated by a diverse assemblage of bacteria and archaea. During a large-scale metagenomic study, we reconstructed 15 metagenome-assembled genomes of Bathyarchaeia that represent two distinct lineages in subgroup 6 (formerly MCG-6) unique to termite guts. One lineage (TB2; Candidatus Termitimicrobium) encodes all enzymes required for reductive acetogenesis from CO2 via an archaeal variant of the Wood–Ljungdahl pathway, involving tetrahydromethanopterin as C1 carrier and an (ADP-forming) acetyl-CoA synthase. This includes a novel 11-subunit hydrogenase, which possesses the genomic architecture of the respiratory Fpo-complex of other archaea but whose catalytic subunit is phylogenetically related to and shares the conserved [NiFe] cofactor-binding motif with [NiFe] hydrogenases of subgroup 4 g. We propose that this novel Fpo-like hydrogenase provides part of the reduced ferredoxin required for CO2 reduction and is driven by the electrochemical membrane potential generated from the ATP conserved by substrate-level phosphorylation; the other part may require the oxidation of organic electron donors, which would make members of TB2 mixotrophic acetogens. Members of the other lineage (TB1; Candidatus Termiticorpusculum) are definitely organotrophic because they consistently lack hydrogenases and/or methylene-tetrahydromethanopterin reductase, a key enzyme of the archaeal Wood–Ljungdahl pathway. Both lineages have the genomic capacity to reduce ferredoxin by oxidizing amino acids and might conduct methylotrophic acetogenesis using unidentified methylated compound(s). Our results indicate that Bathyarchaeia of subgroup 6 contribute to acetate formation in the guts of higher termites and substantiate the genomic evidence for reductive acetogenesis from organic substrates, possibly including methylated compounds, in other uncultured representatives of the phylum.
Highlights
Bathyarchaeia are widespread in anoxic environments, their physiology is only poorly understood
Based on average nucleotide identity (ANI), the metagenome-assembled genomes (MAGs) were assigned to nine phylotypes (Table 1)
MAGs of the same phylotype were always derived from different gut compartments of the same host species, indicating that they most likely represent bathyarchaeal populations distributed along the entire hindgut
Summary
Bathyarchaeia are widespread in anoxic environments, their physiology is only poorly understood. Other studies detected key enzymes of the pathway in bathyarchaeal genomes of several subgroups and proposed that these lineages are involved in reductive acetogenesis from CO2 (He et al, 2016; Lazar et al, 2016). Considering the putative roles of Bathyarchaeia in methanogenesis and reductive acetogenesis and the evidence for the utilization of lignin-derived methoxy groups (Yu T. et al, 2018), the presence of this group in termite guts is intriguing. A study based on the formyltetrahydrofolate synthetase (FTHFS) gene, a key enzyme of the Wood–Ljungdahl pathway that has been used as a marker for reductive acetogenesis, indicated that the community of potential acetogens shifts from spirochetes in lower termites to clostridia in higher termites (Ottesen and Leadbetter, 2011). We conducted detailed phylogenomic analyses of these MAGs and investigated their potential capacity for methanogenesis and reductive acetogenesis using a genome-centric approach
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