Sulfur Reduction Coupled with Anaerobic Ammonium Oxidation Drove Prebiotic Proto-Anabolic Networks

The geochemical energy that drove the transition from geochemistry to biochemistry on early Earth remains unknown. Here, we show that the reduction of sulfurous species, such as thiosulfate, sulfite, elemental sulfur, and sulfate, coupled with anaerobic ammonium oxidation (Sammox), could have provided the primordial redox equivalents and proton potential for prebiotic proto-anabolic networks consisting of the reductive acetyl-CoA pathway combined with the incomplete reductive tricarboxylic acid (rTCA) cycle under mild hydrothermal conditions. Sammox-driven prebiotic proto-anabolic networks (SPPN) include CO2 reduction, esterification, reductive amination, pyrrole synthesis, and peptides synthesis, in one geochemical setting. Iron-sulfur (FeS) minerals, as the proto-catalysts, enhanced the efficiency of SPPN. Thiols/thioesters were used as the energy currency in non-enzymatic phosphate-independent metabolism and accelerated SPPN. Peptides that consisted of 15 proteinogenic amino acids were the end products of SPPN with bicarbonate as the only source of carbon. Most peptides shared high similarity with the truly minimal protein content (TMPC) of the last universal common ancestor (LUCA). The peptides and/or proteinogenic amino acids might have endowed SPPN with autocatalysis and homochirality. Thus, Sammox drove the coupling transformation of carbon, hydrogen, oxygen, nitrogen, sulfur, and/or iron simultaneously in the far-from-equilibrium environment, thereby initiating the emergence of biochemistry. The existing Sammox microorganisms might belong to the phylum of Planctomycetes, and might be transitional forms between the three domains of life.