Polymerization and replication of primordial RNA explained by clay-water interface dynamics

RNA is the only known biopolymer that combines genotype and phenotype in a single molecular entity. This has suggested that the flow of genetic information DNA-RNA-proteins already operating in LUCA could have been preceded by a primordial era when RNA was the genetic and catalytic macromolecule. However, understanding how RNA could have polymerized and subsequently replicated in early Earth remains challenging. We present a theoretical and computational framework to model the non-enzymatic polymerization of ribonucleotides and the template-dependent replication of primordial RNA molecules, at the interfaces between the aqueous solution and a clay mineral supplied by its interlayers and channels. Our results demonstrate that efficient polymerization and accurate replication of single-stranded RNA polymers, sufficiently long to fold and acquire basic functions ($>15$ nt), were possible at clay-water interfaces in early Earth, provided the physico-chemical environment exhibited an oscillatory pattern of large amplitude and a period compatible with spring tide dynamics. Interestingly, the theoretical analysis presents rigorous evidence that RNA replication efficiency increases in oscillating environments compared to constant ones. Moreover, the versatility of our framework enables comparisons between different genetic alphabets, showing that a four-letter alphabet -- particularly when allowing non-canonical base pairs, as in current RNA -- represents an optimal balance of replication speed and sequence diversity in the pathway to life.
Comment: This file contains the main manuscript (6 figures) and the Supplementary Information (4 sections and 7 Supplementary figures)