DNA Before Proteins? Recent Discoveries in Nucleic Acid Catalysis Strengthen the Case

Burton, Aaron; Lehman, Niles

doi:10.1089/ast.2008.0240

Cited by 21 publications

(17 citation statements)

References 30 publications

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“…Although the order of appearance of different types of biopolymers during primordial evolution is still debated [44], [45], the universality of the translation machinery in all domains of life suggests that proteins most likely evolved in the RNA world before DNA (e.g., [46]). If RNA molecules functioned predominantly as templates in the RNA-protein world, the division of labor between templates and catalysts was established before the emergence of DNA.…”

Section: Discussionmentioning

confidence: 99%

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

2011

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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.

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Section: Discussionmentioning

confidence: 99%

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

2011

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“…[64] Surprisingly, however, little attention has been given to the possibility of nucleobase refinement during or after this transition. As previously discussed regarding uracil-based DNA, the possibility exists that life in the early DNA world may still have been “settling” on the specific composition of the genetic alphabet.…”

Section: Base Refinement In An Early Dna World?mentioning

confidence: 99%

On the Origin of the Canonical Nucleobases: An Assessment of Selection Pressures across Chemical and Early Biological Evolution

Rios

Tor

2013

Israel Journal of Chemistry

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The native bases of RNA and DNA are prominent examples of the narrow selection of organic molecules upon which life is based. How did nature “decide” upon these specific heterocycles? Evidence suggests that many types of heterocycles could have been present on the early Earth. It is therefore likely that the contemporary composition of nucleobases is a result of multiple selection pressures that operated during early chemical and biological evolution. The persistence of the fittest heterocycles in the prebiotic environment towards, for example, hydrolytic and photochemical assaults, may have given some nucleobases a selective advantage for incorporation into the first informational polymers. The prebiotic formation of polymeric nucleic acids employing the native bases remains, however, a challenging problem to reconcile. Hypotheses have proposed that the emerging RNA world may have included many types of nucleobases. This is supported by the extensive utilization of non-canonical nucleobases in extant RNA and the resemblance of many of the modified bases to heterocycles generated in simulated prebiotic chemistry experiments. Selection pressures in the RNA world could have therefore narrowed the composition of the nucleic acid bases. Two such selection pressures may have been related to genetic fidelity and duplex stability. Considering these possible selection criteria, the native bases along with other related heterocycles seem to exhibit a certain level of fitness. We end by discussing the strength of the N-glycosidic bond as a potential fitness parameter in the early DNA world, which may have played a part in the refinement of the alphabetic bases.

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“…In other words, RNA, not DNA, was still the genetic medium at the time of the origin of the genetic code. This is supported by the fact that the key molecules of the translation system are shared by all forms of life, whereas the key molecules of DNA replication are not the same in all domains (Lazcano et al 1988;Burton and Lehman 2009). It should be borne in mind that the genomes of ancient and modern organisms would be qualitatively different.…”

Section: Introduction: Two Distinct Phases Of Code Evolutionmentioning

confidence: 99%

Pathways of Genetic Code Evolution in Ancient and Modern Organisms

Sengupta

Higgs

2015

J Mol Evol

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There have been two distinct phases of evolution of the genetic code: an ancient phase--prior to the divergence of the three domains of life, during which the standard genetic code was established--and a modern phase, in which many alternative codes have arisen in specific groups of genomes that differ only slightly from the standard code. Here we discuss the factors that are most important in these two phases, and we argue that these are substantially different. In the modern phase, changes are driven by chance events such as tRNA gene deletions and codon disappearance events. Selection acts as a barrier to prevent changes in the code. In contrast, in the ancient phase, selection for increased diversity of amino acids in the code can be a driving force for addition of new amino acids. The pathway of code evolution is constrained by avoiding disruption of genes that are already encoded by earlier versions of the code. The current arrangement of the standard code suggests that it evolved from a four-column code in which Gly, Ala, Asp, and Val were the earliest encoded amino acids.

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DNA Before Proteins? Recent Discoveries in Nucleic Acid Catalysis Strengthen the Case

Cited by 21 publications

References 30 publications

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

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

On the Origin of the Canonical Nucleobases: An Assessment of Selection Pressures across Chemical and Early Biological Evolution

Pathways of Genetic Code Evolution in Ancient and Modern Organisms

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