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The 'dsRNA first' hypothesis
- Modelling evolution on design-by-contract predicts an origin of Life through an abiotic double-stranded RNA world

An independent evolution of both informational and catalytic functionalities of RNA would provide the necessary flexibility for the evolution of the genome. The potential for system evolvability is met in software development by using the design-by-contract methodology that views a system as a set of communicating modules whose interaction is based on precisely defined interfaces. As long as existing interfaces stay intact, independent evolution of the individual modules is possible. In case of the genome, we can discern two separate functional modules: the ability to store genetic information on one hand, and the ability to function as a catalyst on the other hand. In all organisms, the informational and catalytic entities in the genome are well-separated into respectively dsDNA and ssRNA, and can therefore be seen as the mechanistic implementation of these functional modules. Their relation or interface is strictly defined and conserved throughout the Tree of Life: one part of the double-stranded DNA represents the template for the transcription of ssRNA. Thus, the separation of the informational and catalytic characteristics of RNA by a defined interface allows in principle an independent evolution of both functions as long as this interface stays intact.

Design-by-contract predicts a scenario where once established interfaces remain intact during evolution and thus enforces functional continuity [14,15]. Since a double-stranded RNA provides the template and thus the functional interface for the derivation of single-stranded catalytic RNA, a straightforward explanation for the origin of catalytic RNA is when double-stranded RNA would also have preceded the catalytic single-stranded RNA in evolution. In this way, double-stranded RNA carried the informational function consistently from the start, while ssRNA always harboured the later-derived catalytic function (Fig. 1). This scenario keeps information flow through evolution intact and does not require a substantial change of interfaces during evolution. For instance, the dsRNA template could be changed later in evolution to a dsDNA interface without conceptually affecting transcription of ssRNA. Also, mRNA could be added as the template for protein translation without needing a substantial change in the existing carriers of genetic information. In the same way, the replacement of dsRNA with dsDNA would leave existing interfaces (the generation of catalytic RNA and mRNA) intact. Thus, based on a simple engineering paradigm, it is proposed that dsRNA as the informational molecule was the first molecule to have evolved, and that catalytic ssRNA as the first ribozymes would be derived later in evolution.

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