Oxidation processes diversify the metabolic menu on Enceladus

The Cassini mission to the Saturn system discovered a plume of ice grains and water vapor erupting from cracks on the icy surface of the satellite Enceladus. This moon has a global ocean in contact with a rocky core beneath its icy exterior, making it a promising location to search for evidence of extraterrestrial life in the solar system. The previous detection of molecular hydrogen (H2) in the plume indicates that there is free energy available for methanogenesis, the metabolic reaction of H2 with CO2 to form methane and water. Additional metabolic pathways could also provide sources of energy in Enceladus’ ocean, but they require the use of other oxidants that have not been detected in the plume. Here, we perform chemical modeling to determine how the production of radiolytic O2 and H2O2, and abiotic redox chemistry in the ocean and rocky core, contribute to chemical disequilibria that could support metabolic processes in Enceladus’ ocean. We consider three possible cases for ocean redox chemistry: Case I in which reductants are not present in appreciable amounts and O2 and H2O2 accumulate over time, and Cases II and III in which aqueous reductants or seafloor minerals, respectively, convert O2 and H2O2 in the ocean to SO42− and ferric oxyhydroxides. We calculate the upper limits on the concentrations of oxidants and on the chemical energy available for metabolic reactions in all three cases, neglecting any additional abiotic reactions which could further affect energy availability. For all three cases, we find that many aerobic and anaerobic metabolic reactions used by microbes on Earth could meet the minimum free energy threshold, ΔGmin, required for terrestrial life to convert ADP to ATP. We show that aerobic metabolisms could sustain up to ∼1 cell cm−3 within a 20 m depth across Enceladus’ seafloor, even in our second case where O2 and H2O2 are scarce. Additionally, anaerobic metabolisms could sustain up to ∼1 cell for every two cm−3 within this volume in our latter two cases. In contrast, methanogenesis could support up to 6×102 cells cm−3 throughout this depth, due to the potential for a high hydrogen production rate at the seafloor as indicated by H2 measurements from Enceladus’ plume. While methanogenesis is the only metabolism that predicts cell density values close to those reported in Earth’s oceans and Antarctic subglacial lakes at this depth, our reported values depend on the area considered to be inhabited, which could be smaller than the entire Enceladus seafloor. Overall, the capacity for aerobic and anaerobic metabolisms to meet or exceed ΔGmin as well as sustain positive cell density values indicate that oxidant production and oxidation chemistry could contribute to supporting possible life and a metabolically diverse microbial community on Enceladus.