Metal-catalyzed phosphorylation by phosphite at the origin of bioenergetics

How did phosphate become the universal energetic currency of life? Traditional approaches to phosphorylation in early evolution studies entail oven drying, non-aqueous solvents, dangerously reactive forms of phosphorus, or other non-physiological conditions. With microbial physiology as a vade mecum , we have recently found that phosphite, HPO ₃ ^2– , which is enzymatically oxidized by many microbes and which naturally occurs in serpentinizing hydrothermal vents, will readily phosphorylate ribose, glucose, glycerol, serine, AMP, creatine and acetate to generate phosphoester, phosphoanhydride and acylphosphate bonds in hours to days at 25-100°C in pure alkaline water. These reactions are thermodynamically favourable because anoxic phosphite oxidation to phosphate and H ₂ is highly exergonic, but they do not proceed without catalysts. The most effective catalyst yet identified is a nanoparticular form of a shiny metal: zero-valent (native, or elemental) palladium (Pd ⁰ ). Native palladium, like phosphite, also naturally occurs in serpentinizing hydrothermal vents, as do other native platinum group elements (PGE), including Pt, Rh, Ru and Ir. Here we test those PGE as catalysts of phosphite oxidation and phosphorylation. Though all metals tested readily oxidize phosphite, only Pd ⁰ efficiently catalyzes phosphorylation, generating phosphorylated products at concentrations often equal to their physiological concentrations in growing Escherichia coli cells. Metaphosphate is a possible reaction intermediate. In phosphorylation reactions via phosphite oxidation (D G ₀ ′= –46 kJ·mol ⁻¹ ), a portion of the energy released is conserved in phosphorylated products, as in biological energy conservation. A natural environment and energy-conserving thermodynamics implicate these facile aqueous phosphorylating reactions in the origin of bioenergetics.