Genetic isolation and metabolic complexity of an Antarctic subglacial microbiome

Abstract Microbes inhabiting and evolving in aquatic ecosystems at the base of polar ice sheets subsist under energy-limited conditions while in relative isolation from surface gene pools and their common ancestral populations of origin. Samples recently obtained from the base of West Antarctic Ice Sheet (WAIS) allowed us to examine evolutionary relationships of and identify metabolic pathways in microbial genomes recovered from the Mercer Subglacial Lake (SLM) ecosystem. We obtained 1,374 single-cell amplified genomes from individual bacterial and archaeal cells that were isolated from samples of SLM’s water column and sediments. Genome-based taxonomic classification coherently identified nearly all of the subglacial microorganisms as new species or novel taxonomic groups, and phylogenomic analyses showed evidence for genetically isolation of the microbial populations from marine and surface biomes. Comparative genomic analysis revealed a lake ecosystem exhibiting a range of metabolisms to oxidize various organic and inorganic compounds via aerobic or anerobic respiration. Network construction identified two distinct organotrophic and chemolithotrophic metabolic guilds that may operate alternatively depending on oxygen availability. Our SAG data imply substantial metabolic flexibility in the microbial assemblage characterized, reveal key energy generating strategies in the subglacial ecosystem, and provide a framework to assess microbial evolution beneath WAIS.