Abstract

In RNA-World scenarios for the origin of life, replication is catalyzed by polymerase ribozymes. Replicating RNA systems are subject to invasion by non-functional parasitic strands. It is well-known that there are two ways to avoid the destruction of the system by parasites: spatial clustering in models with limited diffusion, or group selection in protocells. Here, we compare computational models of replication in spatial models and protocells as closely as possible in order to determine the relative importance of these mechanisms in the RNA World. For the survival of the polymerases, the replication rate must be greater than a minimum threshold value, kmin, and the mutation rate in replication must be less than a maximum value, Mmax, which is known as the error threshold. For the protocell models, we find that kmin is substantially lower and Mmax is substantially higher than for the equivalent spatial models; thus, the survival of polymerases is much easier in protocells than on surfaces. The results depend on the maximum number of strands permitted in one protocell or one lattice site in the spatial model, and on whether replication is limited by the supply of monomers or the population size of protocells. The substantial advantages that are seen in the protocell models relative to the spatial models are robust to changing these details. Thus, cooperative polymerases with limited accuracy would have found it much easier to operate inside lipid compartments, and this suggests that protocells may have been a very early step in the development of life. We consider cases where parasites have an equal replication rate to polymerases, and cases where parasites multiply twice as fast as polymerases. The advantage of protocell models over spatial models is increased when the parasites multiply faster.

Highlights

  • The most widely studied theory for the origin of life—the transition from a mixture of prebiotic chemical components to a living system that is sustained by autocatalytic replication—is the RNA World theory [1,2,3,4,5,6,7]

  • Note that Mmax = 0 for S0 > 20 reduced when the parasites multiply faster, but the SLD model is reduced more, meaning that the for SLD2X, because faster parasites kill the polymerases in the spatial model. k = 25 and h = 0.4

  • The mechanisms by which compartments and spatial clustering promote the survival of polymerases have been understood for some time, there has not been much quantitative comparison of the two

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Summary

Introduction

The most widely studied theory for the origin of life—the transition from a mixture of prebiotic chemical components to a living system that is sustained by autocatalytic replication—is the RNA World theory [1,2,3,4,5,6,7]. Most versions of the RNA World propose the existence of RNA polymerase ribozymes that use a second strand as a template to synthesize the complementary strand to the template. RNA polymerase ribozymes have been experimentally developed while using in vitro evolution with maximum template lengths of 200 nucleotides and per-base error rates of a few percent [8,9,10]. Replicating systems containing polymerase ribozymes are subject to invasion by non-functional sequences that act as parasites. Parasite strands are likely to frequently arise, either as a result of chemical synthesis of new random sequences, or as a result of errors in the replication of functional strands

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