Prebiotic Metabolism: Production by Mineral Photoelectrochemistry of α-Ketocarboxylic Acids in the Reductive Tricarboxylic Acid Cycle

Abstract

A reductive tricarboxylic acid (rTCA) cycle could have fixed carbon dioxide as biochemically useful energystorage molecules on early Earth. Nonenzymatic chemical pathways for some steps of the rTCA cycle, however, such as the production of the a-ketocarboxylic acids pyruvate and a-ketoglutarate, remain a challenging problem for the viability of the proposed prebiotic cycle. As a class of compounds, a-ketocarboxylic acids have high free energies of formation that disfavor their production. We report herein the production of pyruvate from lactate and of a-ketoglutarate from pyruvate in the millimolar concentration range as promoted by ZnS mineral photoelectrochemistry. Pyruvate is produced from the photooxidation of lactate with 70% yield and a quantum efficiency of 0.009 at 158C across the wavelength range of 200-400 nm. The produced pyruvate undergoes photoreductive back reaction to lactate at a 30% yield and with a quantum efficiency of 0.0024. Pyruvate alternatively continues in photooxidative forward reaction to a-ketoglutarate with a 50% yield and a quantum efficiency of 0.0036. The remaining 20% of the carbon follows side reactions that produce isocitrate, glutarate, and succinate. Small amounts of acetate are also produced. The results of this study suggest that a-ketocarboxylic acids produced by mineral photoelectrochemistry could have participated in a viable enzyme-free cycle for carbon fixation in an environment where light, sulfide minerals, carbon dioxide, and other organic compounds interacted on prebiotic Earth.

Origin of first cells at terrestrial, anoxic geothermal fields

“…Some of the most successful attempts to simulate primitive abiogenic reactions have been conducted under conditions that are compatible with reconstructed conditions at the geothermal fields of the anoxic Earth. These promising experiments include syntheses of biologically relevant compounds in formamide solutions (98)(99)(100)(101)(102)(103)(104)(105)(106)(107)(108)(111)(112)(113)(114)(115), photosynthesis/photoselection of natural nucleotides (120)(121)(122)133), montmorillonite-catalyzed formation of long RNA oligomers (118) and membrane vesicles (134), RNA polymerization in the eutectic phase in water-ice (135), abiotic UV photosynthesis of the tricarboxylic acid cycle intermediates at ZnS (83,84) and TiO 2 crystals (136), as well as UV-triggered recharging of ADP to ATP (137). Further experimental exploration of models that mimic the conditions at anoxic geothermal fields are expected to shed more light on precellular evolution.…”

“…Similar reactions could lead to the ammonia formation (80), which might account for the high ammonia content in the exhalations of geothermal fields [as much as 130 mg/L in the mud pot solutions of Kamchatka (55)]. In addition, diverse organic molecules could be produced by abiotic photosynthesis catalyzed by ZnS and MnS particles (81)(82)(83)(84). Such crystals are semiconductors, which can trap quanta with a λ of less than 320 nm and transiently store their energy in a form of charge-separated states, capable of reducing diverse compounds at the surface (81).…”

“…‡ Particles of ZnS can catalyze photopolymerization reactions (85) and photoreduce carbonaceous compounds to diverse organic molecules, including intermediates of the tricarboxylic acid cycle (83,84); the highest quantum yield of 80% was observed upon reduction of CO 2 to formate (81).…”

Detection and formation scenario of citric acid, pyruvic acid, and other possible metabolism precursors in carbonaceous meteorites

“…For example, high temperature laboratory simulations of prebiotic hydrothermal vents produced small amounts of pyruvic acid using a FeS catalyst (28). Pyruvate and α-ketoglutarate (among other compounds) were also produced by photolysis in the presence of zinc sulfide (29).…”

The Role of Microbial Electron Transfer in the Coevolution of the Biosphere and Geosphere

“…The effective cross sections for the photochemical oxidation of siderite by ultraviolet radiation potentially supplied electrons for life in the Archean oceans at fluxes comparable if not exceeding that from hydrothermal vents (67,121). Significant steps in the reductive tricarboxylic acid cycle (one of the six extant carbon fixation pathways) have been carried out abiotically with photo-driven zinc sulfide catalysis (48,136). These and other photogeochemical reactions involving minerals almost certainly played a significant role in fueling the earliest life-forms on Earth as well as foreshadowing the emergence of photosynthesis (92,118).…”