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Ferruginous conditions prevailed through Earth’s early oceans history, yet our understanding of biogeochemical cycles in anoxic iron-rich, sulfate-poor sediments remains elusive in terms of redox processes and organic matter remineralization. Using comprehensive geochemistry, cell counts and metagenomic data, we investigated the taxonomic and functional distribution of the microbial subsurface biosphere in Lake Towuti, a stratified ferruginous analogue. Below the zone in which pore water becomes depleted in electron acceptors, cell densities exponentially decreased while microbial assemblages shifted from iron- and sulfate-reducing bacterial populations to fermentative anaerobes and methanogens, mostly selecting Bathyarchaeia below the sulfate reduction zone. Bathyarchaeia encode metabolic machinery to cycle and assimilate polysulfides via sulfhydrogenase, sulfide dehydrogenase and heterodisulfide reductase, using dissimilatory sulfite reductase subunit E and rubredoxin as carriers. Their metagenome-assembled genomes showed that carbon fixation could proceed through the complete methyl-branch Wood-Ljungdahl pathway, conducting (homo)acetogenesis in the absence of methyl coenzyme M reductase. Further, their partial carbonyl-branch, assumed to act in tetrahydrofolate interconversions of C1 and C2 compounds, could support close interactions with methylotrophic methanogens in the fermentation zone. Thus, Bathyarchaeia appeared capable of coupling sulfur-redox reactions with fermentative processes, using electron bifurcation in a redox-conserving (homo)acetogenic Wood-Ljungdahl pathway, and revealing geochemical ferruginous conditions at the transition between the sulfate reduction and fermentation zone as their preferential niche.
