Research on geologic carbon sequestration raises questions about potential impacts of subsurface microbiota on carbon cycling and biogeochemistry. Subsurface, high-CO₂ systems are poorly biologically characterized, partly due to difficulty accessing high-volume, uncontaminated samples. CO₂–driven Crystal Geyser (Utah, USA), an established geologic carbon sequestration analog, provides high volumes of deep (∼200-500 m) subsurface fluids. We explored microbial diversity and metabolic potential in this high-CO₂ environment by assembly and analysis of metagenomes recovered from geyser water filtrate. The system is dominated by neutrophilic, iron-oxidizing bacteria, including “marine” Mariprofundus (Zetaproteobacteria) and “freshwater” Gallionellales, sulfur-oxidizing Thiomicrospira crunogena, and Thiobacillus-like Hydrogenophilales. Near-complete genomes were reconstructed for these bacteria. Crystal Geyser is notably populated by a wide diversity of bacteria and archaea from phyla lacking isolated representatives (Candidate Phyla, CP) and from as-yet undefined lineages. Many bacteria affiliate with OD1, OP3, OP9, PER, ACD58, WWE3, BD1-5, OP11, TM7, and ZB2. The recovery of nearly 100 genes encoding RuBisCO subunit proteins of the Calvin Cycle and AMP salvage pathways suggests a strong biological role in high-CO₂ subsurface carbon cycling. Overall, we predict microbial impacts on subsurface biogeochemistry via iron, sulfur, and complex carbon oxidation, carbon and nitrogen fixation, fermentation, hydrogen metabolism, and aerobic and anaerobic respiration.