Chemolithoautotrophic bacteria flourish at dark water-ice interfaces of an emerged Arctic cold seep

Below their ice shells, icy moons may offer a source of chemical energy that could support microbial life in the absence of light. In the Arctic, past and present glacial retreat leads to isostatic uplift of sediments through which cold and methane-saturated groundwater travels. This fluid reaches the surface and freezes as hill-shaped icings during winter, producing dark ice-water interfaces above water ponds containing chemical energy sources. In one such system characterized by elevated methane concentrations - the Lagoon Pingo in Adventdalen, Svalbard, Norway (~10 mg/L CH4, <0.3 mg/L O2, -0.25°C, pH 7.9), we studied amplicons of the bacterial and archaeal (microbial) 16S rRNA gene and transcripts in the water pond and overlaying ice. We found that active chemolithoautotrophic sulfur-oxidizing microorganisms (Sulfurimonas, Thiomicrorhabdus) dominate a niche at the bottom of the ice that is in contact with the anoxic water reservoir. There, the growing ice offers surfaces that interface with water and hosts favorable physico-chemical conditions for sulfide oxidation. The detection of anaerobic methanotrophs further suggests that throughout the winter, a steady-state dark and cold methane sink occurs under the ice in two steps: first, methane is oxidized to carbon dioxide and sulfates are concomitantly reduced to sulfides by the activity of anaerobic methanotrophs (ANME) ANME-1a and sulfate-reducing bacteria (SRB) SEEP-SRB1 consortia; and second, energy from sulfides is used by sulfur-oxidizing microorganisms to fix carbon dioxide into organic carbon. Our results underscore that ice-covered and dark ecosystems are hitherto overlooked oases of microbial life and emphasize the need to study microbial communities in icy habitats.