On the Origin of DNA Genomes: Evolution of the Division of Labor between Template and Catalyst in Model Replicator Systems

Abstract

The division of labor between template and catalyst is a fundamental property of all living systems: DNA stores genetic information whereas proteins function as catalysts. The RNA world hypothesis, however, posits that, at the earlier stages of evolution, RNA acted as both template and catalyst. Why would such division of labor evolve in the RNA world? We investigated the evolution of DNA-like molecules, i.e. molecules that can function only as template, in minimal computational models of RNA replicator systems. In the models, RNA can function as both template-directed polymerase and template, whereas DNA can function only as template. Two classes of models were explored. In the surface models, replicators are attached to surfaces with finite diffusion. In the compartment models, replicators are compartmentalized by vesicle-like boundaries. Both models displayed the evolution of DNA and the ensuing division of labor between templates and catalysts. In the surface model, DNA provides the advantage of greater resistance against parasitic templates. However, this advantage is at least partially offset by the disadvantage of slower multiplication due to the increased complexity of the replication cycle. In the compartment model, DNA can significantly delay the intra-compartment evolution of RNA towards catalytic deterioration. These results are explained in terms of the trade-off between template and catalyst that is inherent in RNA-only replication cycles: DNA releases RNA from this trade-off by making it unnecessary for RNA to serve as template and so rendering the system more resistant against evolving parasitism. Our analysis of these simple models suggests that the lack of catalytic activity in DNA by itself can generate a sufficient selective advantage for RNA replicator systems to produce DNA. Given the widespread notion that DNA evolved owing to its superior chemical properties as a template, this study offers a novel insight into the evolutionary origin of DNA.

Virus World as an Evolutionary Network of Viruses and Capsidless Selfish Elements

“…Genetic parasites, i.e., viruses and virus-like selfish elements, seem to be truly ubiquitous: some such elements apparently are associated with all cellular life forms. Mathematical models of the evolution of replicator systems aimed at the reconstruction of the first stages in the history of life invariably reveal partitioning into hosts and parasites (180)(181)(182)(183). This fundamental separation emerges as soon as the evolving systems reach a minimum complexity whereby dedicated replication devices, such as polymerases, evolve and thus can be hijacked by "cheaters," the first parasites (184).…”

Are viruses alive? The replicator paradigm sheds decisive light on an old but misguided question

“…Indeed, emergence of selfish, parasitic elements is inevitable in even the simplest replicator systems (Konnyu, Czaran, & Szathmary, 2008; Szathmary & Maynard Smith, 1997; Takeuchi & Hogeweg, 2007, 2012; Takeuchi, Hogeweg, & Koonin, 2011). Probably, a more accurate statement is that the entire history of life is a story of host-parasite coevolution.…”

“…Mathematical models of coevolution convincingly show that, in well-mixed populations of hosts, parasites cause collapse of the entire host-parasite system. Stable coevolution is possible only in structured populations (Takeuchi and Hogeweg 2012, 2007; Takeuchi, Hogeweg and Koonin 2011). Thus, selfish replicators promote evolution of complexity of the entire replicator ecosystem.…”

“…Thus, selfish replicators promote evolution of complexity of the entire replicator ecosystem. More specifically, such major evolutionary transitions as the advent of DNA as a dedicated information storage device (Takeuchi, Hogeweg and Koonin 2011) and the origin of multicellular life forms could have been promoted by the parasite-host arms race, in particular, through the evolution of programmed cell death as a defense (Iranzo et al 2014). …”

Crucial steps to life: From chemical reactions to code using agents

“…The emergence of DNA and protein-based cellular life created a new biosphere with real cell-based organisms (Takeuchi et al, 2011). Their own identity group building, evolution and development from an RNA-only perspective opened up a completely new dimension of genome-bearing entities as appropriate resources for infectious/cooperative RNA settlements.…”