Genomic expansion of archaeal lineages resolved from deep Costa Rica sediments

Numerous archaeal lineages are known to inhabit marine subsurface sediments, although their distributions, metabolic capacities and interspecies interactions are still not well understood. Abundant and diverse archaea were recently reported in Costa Rica (CR) margin subseafloor sediments recovered during IODP Expedition 334. Here, we recover metagenome-assembled genomes (MAGs) of archaea from the CR-margin and compare them to their relatives from shallower settings. We describe 31 MAGs of 6 different archaeal lineages (Lokiarchaeota, Thorarchaeota, Heimdallarchaeota, Bathyarcheota, Thermoplasmatales and Hadesarchaea) and thoroughly analyze representative MAGs from the phyla Lokiarchaeota and Bathyarchaeota. Our analysis suggests the potential capabilities of Lokiarchaeota members to anaerobically degrade aliphatic and aromatic hydrocarbons. We show it is genetically possible and energetically feasible for Lokiarchaeota to degrade benzoate if they associate with organisms using nitrate, nitrite and sulfite as electron acceptors, which suggests a possibility of syntrophic relationships between Lokiarchaeota and nitrite and sulfite reducers. The novel Bathyarchaeota lineage possesses an incomplete methanogenesis pathway lacking the methyl co-enzyme M reductase complex and encodes a non-canonical acetogenic pathway potentially coupling methylotrophy to acetogenesis via the methyl branch of Wood-Ljundahl pathway. These novel metabolic characteristics suggest the potential of this Bathyarchaeota lineage to be a transition between methanogenic and acetogenic Bathyarchaeota lineages. This work substantially expands our knowledge about the metabolic function repertoire of marine benthic archaea.