Metabolic features explaining the prevalence Bathyarchaeia among microbial communities in ferruginous deposits

Although ferruginous conditions prevailed in the oceans through much of Earth's history, past biogeochemical cycling in early seafloor deposits remains poorly constrained in terms of metal redox processes and organic matter remineralization prior to lithification. We investigated the metabolic potential of microbial communities in iron-rich anoxic sediments from Lake Towuti, a modern stratified ferruginous system, and report extensive data combining pore water geochemistry, cell count and metagenomic analyses of taxonomic and functional marker genes during early burial. After pore water depletion in electron acceptors, microbial assemblages shifted from a consortium of iron- and sulfate-reducing bacteria to fermentative anaerobes while cell densities exponentially decreased in the fermentative zone. Abundant populations therein were vertically distributed as Desulfobacterota, Chloroflexota, Euryarchaota, Halobacterota, Hadarchaeota, but primarily as Bathyarchaeia that prevailed below 10 cm sediment depth. Taxonomic assignments of functional marker genes show that metabolic features selecting Bathyarchaeia under ferruginous conditions include cycling of sulfur intermediates via genes encoding sulfhydrogenase and sulfide dehydrogenase with heterodisulfide reductase driving electron bifurcation. Heterotrophic dark carbon fixation can proceed through a partial acetogenic but mostly methanogenic Wood-Ljungdahl pathway combined with hydrogen production, putatively supported by the reductive hexulose-phosphate pathway via RuBisCo genes and formaldehyde-activating enzymes. These metabolic capabilities, which confirm Bathyarchaeia as (homo)acetogens, are consistent with their postulated hydrothermal origin and would have been critical in early ferruginous systems to drive redox reactions involved in the Wood-Ljungdahl pathway, yet the most ancient metabolism for energy generation and carbon fixation in Archaea.