Non-enzymatic glycolysis and pentose phosphate pathway-like reactions in a plausible Archean ocean

Synopsis image Modern cells possess a sophisticated metabolic network, but its origins remain largely unknown. Reconstructing scenarios of the Archean ocean, we observe chemical reactions reminiscent of modern metabolic sequences, indicating that metabolism could be of prebiotic origin. Metabolites of glycolysis and the pentose phosphate undergo non-enzymatic interconversion reactions. Metal ions abundantly found in sediments of the prebiotic Archean ocean, predominantly Fe(II), catalyse additional sugar phosphate interconversion reactions. Reactions catalysed by the Archean ocean metals resemble enzyme-catalysed reactions found in the modern glycolytic and pentose phosphate pathways. The observed reactions are accelerated and gain specificity in conditions simulating the Archean ocean. Abstract The reaction sequences of central metabolism, glycolysis and the pentose phosphate pathway provide essential precursors for nucleic acids, amino acids and lipids. However, their evolutionary origins are not yet understood. Here, we provide evidence that their structure could have been fundamentally shaped by the general chemical environments in earth's earliest oceans. We reconstructed potential scenarios for oceans of the prebiotic Archean based on the composition of early sediments. We report that the resultant reaction milieu catalyses the interconversion of metabolites that in modern organisms constitute glycolysis and the pentose phosphate pathway. The 29 observed reactions include the formation and/or interconversion of glucose, pyruvate, the nucleic acid precursor ribose-5-phosphate and the amino acid precursor erythrose-4-phosphate, antedating reactions sequences similar to that used by the metabolic pathways. Moreover, the Archean ocean mimetic increased the stability of the phosphorylated intermediates and accelerated the rate of intermediate reactions and pyruvate production. The catalytic capacity of the reconstructed ocean milieu was attributable to its metal content. The reactions were particularly sensitive to ferrous iron Fe(II), which is understood to have had high concentrations in the Archean oceans. These observations reveal that reaction sequences that constitute central carbon metabolism could have been constrained by the iron-rich oceanic environment of the early Archean. The origin of metabolism could thus date back to the prebiotic world. Modern cells possess a sophisticated metabolic network, but its origins remain largely unknown. Reconstructing scenarios of the Archean ocean, we observe chemical reactions reminiscent of modern metabolic sequences, indicating that metabolism could be of prebiotic origin.image