Comparison of the Roles of Nucleotide Synthesis, Polymerization, and Recombination in the Origin of Autocatalytic Sets of RNAs
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abstract
Ribozymes that act as polymerases and nucleotide synthases are known experimentally, even though no fully self-replicating system has yet been found. If the RNA World hypothesis is true, ribozymes must have arisen initially from within a random abiotic polymerization system. To investigate the origin of the RNA world, we studied a mathematical model of a chemical reaction system describing RNA polymerization. It is supposed that, in absence of ribozymes, polymerization occurs at a small spontaneous rate, and that in the presence of polymerase ribozymes, polymerization occurs at a faster rate that is proportional to the ribozyme concentration. Chains must be longer than a minimum threshold length in order to have the possibility of acting as ribozymes. The reaction system has two stable states that we term dead and living. The dead state is controlled by the small spontaneous rate and has negligible concentration of ribozymes. The living state has high concentration of ribozymes, and the reaction rates are determined by the ribozymes; thus, the system is autocatalytic. Concentration fluctuations in a finite volume can cause a transition to occur from the dead to the living state, that is, an origin of life occurs within this model. We also consider ribozymes that catalyze nucleotide synthesis. We show that living and dead states arise in the presence of synthase ribozymes in the same way as for polymerases. It has been proposed that recombination reactions are a way of generating long RNA chains in the early stages of life. We show that if the possibility of random reversible recombination reactions is added to our model, this does not lead to an increase in long polymer concentration. Thus, if recombination is fully reversible, there is no autocatalytic state controlled by recombination. Nevertheless, recombination can play an important role in ribozyme synthesis if there is an additional process that keeps the recombination reactions out of equilibrium. We modeled a case studied experimentally in which building block strands of moderate length associate due to RNA secondary structure formation. A recombination reaction then occurs between these strands to form a longer sequence that catalyzes its own formation via the recombination reaction. This system has an autocatalytic state, and it is possible for it to arise within our random polymerization system. If complexes formed by associations of shorter strands can act as catalysts without the requirement that the strands be covalently linked, this would alleviate the need for synthesis of very long strands; hence, it makes the emergence of an autocatalytic system from an abiotic random polymerization system much more likely.
