On the origin of DNA genomes: evolution of the division of labor between template and catalyst in model replicator systems

The division of labor between template and catalyst is a fundamental property ofall living systems: DNA stores genetic information whereas proteins function ascatalysts. The RNA world hypothesis, however, posits that, at the earlier stagesof evolution, RNA acted as both template and catalyst. Why would such divisionof labor evolve in the RNA world? We investigated the evolution of DNA-likemolecules, i.e. molecules that can function only as template, in minimalcomputational models of RNA replicator systems. In the models, RNA can functionas both template-directed polymerase and template, whereas DNA can function onlyas template. Two classes of models were explored. In the surface models,replicators are attached to surfaces with finite diffusion. In the compartmentmodels, replicators are compartmentalized by vesicle-like boundaries. Bothmodels displayed the evolution of DNA and the ensuing division of labor betweentemplates and catalysts. In the surface model, DNA provides the advantage ofgreater resistance against parasitic templates. However, this advantage is atleast partially offset by the disadvantage of slower multiplication due to theincreased complexity of the replication cycle. In the compartment model, DNA cansignificantly delay the intra-compartment evolution of RNA towards catalyticdeterioration. These results are explained in terms of the trade-off betweentemplate and catalyst that is inherent in RNA-only replication cycles: DNAreleases RNA from this trade-off by making it unnecessary for RNA to serve astemplate and so rendering the system more resistant against evolving parasitism.Our analysis of these simple models suggests that the lack of catalytic activityin DNA by itself can generate a sufficient selective advantage for RNAreplicator systems to produce DNA. Given the widespread notion that DNA evolvedowing to its superior chemical properties as a template, this study offers anovel insight into the evolutionary origin of DNA.