Ancient metagenomics reveals subglacial microbiomes driven by oxygen availability

Beneath Earths glaciers and ice sheets lies an aquatic realm where ice, water, rock, and microbial life interact, driving chemical reactions that can collectively influence the global carbon cycle, polar oceans, and climate. Efforts to describe subglacial microbiomes have been limited by the challenge of cleanly drilling through hundreds of meters of ice, such that only a few sites have ever been directly sampled. Here we use ancient metagenomics to present the first spatiotemporal characterization of subglacial bacteria and archaea. We extracted DNA from 25 subglacial precipitate samples, sedimentary accumulations of minerals that form in subglacial waters prior to exposure on the surface. The precipitates studied here formed between 16,000 and 570,000 years ago beneath the Antarctic and Laurentide Ice Sheets. We show that postmortem DNA damage patterns can reliably distinguish between ancient subglacial and modern surface taxa, and that this approach can enable reconstruction of subglacial microbiomes across poles and ice ages. Our analysis suggests that subglacial microbiomes are dominated by chemolithoautotrophs, ultra-small microbes, and taxa closely related to those found in deep subsurface or extreme cold and hypersaline environments. These microbiomes split into two distinct clusters distinguished by oxygen availability and redox conditions, irrespective of geography or age. Geochemical measurements of subglacial redox state, measured either indirectly via precipitate calcite Fe and Mn concentrations or directly via water reduction potential, reproduce these same two clusters exactly. Our findings describe how subglacial water redox states are held in balance by microbes, hydrology, and oxygen input from fresh subglacial meltwater, that we interpret to be controlled by the ice sheet response to past climate variations.