Genomic Expansion of Archaeal Lineages Resolved from Deep Costa Rica Sediments

The marine subsurface is a reservoir of numerous exotic archaeal lineages, although their distributions, full metabolic capacities and interspecies interactions are still not well understood. Abundant and diverse archaea were recently reported in Costa Rica (CR) Margin subseafloor sediments . Here we recover metagenome-assembled genomes (MAGs) of archaea from CR-Margin and compare them to their relatives from shallower settings. We describe 32 MAGs of 7 different archaeal lineages (Lokiarchaeota, Thorarchaeota, Helarchaeota, Heimdallarchaeota, Bathyarcheota, Thermoplasmatales and Hadesarchaea) and thoroughly analyze representative MAGs from the phyla Lokiarchaeota, Helarchaeota and Bathyarchaeota. Our analysis suggests the unprecedented potential capabilities of Helarchaeota and Lokiarchaeota members to anaerobically degrade aliphatic and aromatic hydrocarbons. We show that Lokiarchaeota could potentially degrade benzoate when coupled with nitrite and sulfite as electron acceptors, suggesting syntrophic relationships between these metabolic groups. Also, we reveal a metabolically novel Bathyarchaeota lineage, which lacks methyl co-enzyme M reductase complex and possesses a non-canonical acetogenic pathway coupling methylotrophy to acetogenesis via the methyl branch of Wood-Ljundahl pathway. These novel metabolic characteristics promote this CR-Batharchaeota to be the potential common descent between methanogenic and acetogenic Bathyarchaeota lineages. This work substantially expands our knowledge about the repertoire of metabolic functions that potentially encoded by benthic marine archaea.