Thermodynamic Constraints on the Citric Acid Cycle and Related Reactions in Ocean World Interiors

Abstract

Icy ocean worlds in our solar system have attracted significant interest for their astrobiological and biogeochemical potential due to the predicted presence of global subsurface liquid water oceans, the presence of organics in Enceladus and Titan, and plausible sources of chemical energy available for life therein. A difficulty in placing quantitative constraints on the occurrence and effectiveness of biogeochemical reactions favorable for life and metabolism in ocean worlds is the paucity of thermodynamic data for the relevant reactions for pressure, temperature and compositional conditions pertaining to ocean worlds, in addition to uncertainties in the estimation of such conditions. Here, we quantify the thermodynamic viability and energetics of various reactions of interest to metabolism at pressures and temperatures relevant to ocean worlds Enceladus, Europa, Titan and Ganymede, and conditions relevant to the Lost City Hydrothermal Field for comparison. Specifically, we examine the tricarboxylic acid cycle (also known as TCA, Krebs cycle, or citric acid cycle) and a plausible precursor prebiotic network of reactions leading to the TCA cycle. We use DEWPython, a program based on the deep earth water (DEW) model (which is a high pressure and high temperature extension of the Helgeson─Kirkham─Flowers equation of state used to calculate thermodynamic properties of ions and complexes in aqueous solutions), to compute the equilibrium constants and the Gibbs free energy changes for given reactions, as a function of pressure and temperature. Using instantaneous concentrations of inorganics and organics from terrestrial microbial experiments and those derived from the Cassini mission for Enceladus, we calculate chemical affinities of reactions in the network. We carry out similar calculations using the SUPCRT model for lower pressures and temperatures. Together, the two models span temperatures between 0 and 1200 °C and pressures between 1 bar and 60 kbar. We found that across the majority of oceanic pressure─temperature profiles, certain TCA cycle species, such as citrate and succinate, accumulate, while others, including fumarate and oxaloacetate, exhibit a diminishing trend. This observation suggests that the internal conditions of ocean worlds may not thermodynamically favor a unidirectional TCA cycle, thereby implying an additional source of energy (e.g., metabolites) to overcome energy bottlenecks. Notably, we find similar bottlenecks at the Lost City Hydrothermal Field, which is undoubtedly inhabited by organisms. In the prebiotic network, we found that pyruvate and acetate exhibit remarkable stability and accumulate in substantial quantities, thereby feeding the TCA cycle through the production of citrate. In this case the oxaloacetate bottleneck within the TCA cycle is bypassed via the prebiotic pathway. We also found that the formation of all TCA cycle species from inorganic compounds (CO₂ + H₂) is highly favored throughout the geotherms of ocean worlds. Although based on largely uncertain concentrations of chemical species in ocean worlds, our nonequilibrium thermodynamic predictions are rather insensitive to changes in the activities, and may aid in the interpretation of data gathered by future missions, as compositional data will become available. Specifically, spacecraft measurements of TCA cycle species in aqueous environments that align with or deviate strongly from our estimations would have a critical impact on the search for life in ocean worlds.