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On the emergence of structural complexity in RNA replicators.

ABSTRACT: The RNA world hypothesis relies on the ability of ribonucleic acids to spontaneously acquire complex structures capable of supporting essential biological functions. Multiple sophisticated evolutionary models have been proposed for their emergence, but they often assume specific conditions. In this work, we explore a simple and parsimonious scenario describing the emergence of complex molecular structures at the early stages of life. We show that at specific GC content regimes, an undirected replication model is sufficient to explain the apparition of multibranched RNA secondary structures-a structural signature of many essential ribozymes. We ran a large-scale computational study to map energetically stable structures on complete mutational networks of 50-nt-long RNA sequences. Our results reveal that the sequence landscape with stable structures is enriched with multibranched structures at a length scale coinciding with the appearance of complex structures in RNA databases. A random replication mechanism preserving a 50% GC content may suffice to explain a natural enrichment of stable complex structures in populations of functional RNAs. In contrast, an evolutionary mechanism eliciting the most stable folds at each generation appears to help reaching multibranched structures at highest GC content.

SUBMITTER: Oliver CG

PROVIDER: S-EPMC6859851 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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On the emergence of structural complexity in RNA replicators.

Oliver Carlos G CG Reinharz Vladimir V Waldispühl Jérôme J

RNA (New York, N.Y.) 20190829 12

The RNA world hypothesis relies on the ability of ribonucleic acids to spontaneously acquire complex structures capable of supporting essential biological functions. Multiple sophisticated evolutionary models have been proposed for their emergence, but they often assume specific conditions. In this work, we explore a simple and parsimonious scenario describing the emergence of complex molecular structures at the early stages of life. We show that at specific GC content regimes, an undirected rep ...[more]

PMID: 31467146

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Project description:It is still not clear how prebiotic replicators evolved towards the complexity found in present day organisms. Within the most realistic scenario for prebiotic evolution, known as the RNA world hypothesis, such complexity has arisen from replicators consisting solely of RNA. Within contemporary life, remarkably many RNAs are involved in modifying other RNAs. In hindsight, such RNA-RNA modification might have helped in alleviating the limits of complexity posed by the information threshold for RNA-only replicators. Here we study the possible role of such self-modification in early evolution, by modeling the evolution of protocells as evolving replicators, which have the opportunity to incorporate these mechanisms as a molecular tool. Evolution is studied towards a set of 25 arbitrary 'functional' structures, while avoiding all other (misfolded) structures, which are considered to be toxic and increase the death-rate of a protocell. The modeled protocells contain a genotype of different RNA-sequences while their phenotype is the ensemble of secondary structures they can potentially produce from these RNA-sequences. One of the secondary structures explicitly codes for a simple sequence-modification tool. This 'RNA-adapter' can block certain positions on other RNA-sequences through antisense base-pairing. The altered sequence can produce an alternative secondary structure, which may or may not be functional. We show that the modifying potential of interacting RNA-sequences enables these protocells to evolve high fitness under high mutation rates. Moreover, our model shows that because of toxicity of misfolded molecules, redundant coding impedes the evolution of self-modification machinery, in effect restraining the evolvability of coding structures. Hence, high mutation rates can actually promote the evolution of complex coding structures by reducing redundant coding. Protocells can successfully use RNA-adapters to modify their genotype-phenotype mapping in order to enhance the coding capacity of their genome and fit more information on smaller sized genomes.

Dataset Information

On the emergence of structural complexity in RNA replicators.

Publications

On the emergence of structural complexity in RNA replicators.

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