Primitive purine biosynthesis connects ancient geochemistry to modern metabolism

Abstract

A major unresolved question in the origin and evolution of life is whether a continuous path from geochemical precursors to the majority of molecules in the biosphere can be reconstructed from modern day biochemistry. Here we simulated the emergence of ancient metabolic networks and identified a feasible path from simple geochemically plausible precursors (e.g., phosphate, sulfide, ammonia, simple carboxylic acids, and metals) using only known biochemical reactions and models of primitive coenzymes. We find that purine synthesis constitutes a bottleneck for metabolic expansion, and that non-autocatalytic phosphoryl coupling agents are necessary to enable expansion from geochemistry to modern metabolic networks. Our model predicts punctuated phases of metabolic evolution characterized by the emergence of small molecule coenzymes (e.g., ATP, NAD+, FAD). Early phases in the resulting expansion are associated with enzymes that are metal dependent and structurally symmetric, supporting models of early biochemical evolution. This expansion trajectory produces distinct hypotheses regarding the timing and mode of metabolic pathway evolution, including a late appearance of methane metabolisms and oxygenic photosynthesis consistent with the geochemical record. The concordance between biological and geological analysis suggests that this trajectory provides a plausible evolutionary history for the vast majority of core biochemistry.