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Mixed Anhydrides at the Intersection Between Peptide and RNA Autocatalytic Sets: Evolution of Biological Coding

We present a scenario for the origin of biological coding. In this context, coding is a semiotic relationship between chemical information stored in one location that links to chemical information stored in a separate location. Coding originated by the cooperative interaction of two, originally separate collectively autocatalytic sets, one for nucleic acids and one for peptides. When these two sets interacted, a series of RNA-folding-directed processes led to their joint cooperativity. The amino acyl adenylate, today amino acid-AMP, was the first covalent association made by these two collectively autocatalytic sets and solidified their interdependence. This molecule is a palimpsest of this era, and is a relic of the original semiotic, and thus coding, relationship between RNA and proteins. More defined coding was driven by selection pressure to eliminate waste in the collective autocatalytic sets. Eventually a 1:1 relationship between single amino acids and short RNA pieces (e.g., three nucleotides) was established, leading to what is today known as the genetic code. Transfer RNA aminoacylating enzymes, or aaRSs, arose concomitantly with the advent of specific coding. The two classes of aaRS enzymes are remnants of the duality of complementary information in two nucleic acid strands, as originally postulated by Rodin and Ohno. Every stage in the evolution of coding was driven by the downward selection on the components of a system to satisfy the Kantian whole. Coding was ultimately forced because there were at least two chemically distinct classes of polymers needed for open-ended evolution; systems with only one polymer cannot exhibit this characteristic. Coding is thus synonymous with life as we know it, and can be thought of as a phase transition in the history of the universe.