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Thermodynamic Basis for the Emergence of Genomes during Prebiotic Evolution
The RNA world hypothesis views modern organisms as descendants of RNA molecules. The earliest RNA molecules must have been random sequences, from which the first genomes that coded for polymerase ribozymes emerged. The quasispecies theory by Eigen predicts the existence of an error threshold limitin...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Public Library of Science
2012
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3364946/ https://www.ncbi.nlm.nih.gov/pubmed/22693440 http://dx.doi.org/10.1371/journal.pcbi.1002534 |
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author | Woo, Hyung-June Vijaya Satya, Ravi Reifman, Jaques |
author_facet | Woo, Hyung-June Vijaya Satya, Ravi Reifman, Jaques |
author_sort | Woo, Hyung-June |
collection | PubMed |
description | The RNA world hypothesis views modern organisms as descendants of RNA molecules. The earliest RNA molecules must have been random sequences, from which the first genomes that coded for polymerase ribozymes emerged. The quasispecies theory by Eigen predicts the existence of an error threshold limiting genomic stability during such transitions, but does not address the spontaneity of changes. Following a recent theoretical approach, we applied the quasispecies theory combined with kinetic/thermodynamic descriptions of RNA replication to analyze the collective behavior of RNA replicators based on known experimental kinetics data. We find that, with increasing fidelity (relative rate of base-extension for Watson-Crick versus mismatched base pairs), replications without enzymes, with ribozymes, and with protein-based polymerases are above, near, and below a critical point, respectively. The prebiotic evolution therefore must have crossed this critical region. Over large regions of the phase diagram, fitness increases with increasing fidelity, biasing random drifts in sequence space toward ‘crystallization.’ This region encloses the experimental nonenzymatic fidelity value, favoring evolutions toward polymerase sequences with ever higher fidelity, despite error rates above the error catastrophe threshold. Our work shows that experimentally characterized kinetics and thermodynamics of RNA replication allow us to determine the physicochemical conditions required for the spontaneous crystallization of biological information. Our findings also suggest that among many potential oligomers capable of templated replication, RNAs may have evolved to form prebiotic genomes due to the value of their nonenzymatic fidelity. |
format | Online Article Text |
id | pubmed-3364946 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2012 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-33649462012-06-12 Thermodynamic Basis for the Emergence of Genomes during Prebiotic Evolution Woo, Hyung-June Vijaya Satya, Ravi Reifman, Jaques PLoS Comput Biol Research Article The RNA world hypothesis views modern organisms as descendants of RNA molecules. The earliest RNA molecules must have been random sequences, from which the first genomes that coded for polymerase ribozymes emerged. The quasispecies theory by Eigen predicts the existence of an error threshold limiting genomic stability during such transitions, but does not address the spontaneity of changes. Following a recent theoretical approach, we applied the quasispecies theory combined with kinetic/thermodynamic descriptions of RNA replication to analyze the collective behavior of RNA replicators based on known experimental kinetics data. We find that, with increasing fidelity (relative rate of base-extension for Watson-Crick versus mismatched base pairs), replications without enzymes, with ribozymes, and with protein-based polymerases are above, near, and below a critical point, respectively. The prebiotic evolution therefore must have crossed this critical region. Over large regions of the phase diagram, fitness increases with increasing fidelity, biasing random drifts in sequence space toward ‘crystallization.’ This region encloses the experimental nonenzymatic fidelity value, favoring evolutions toward polymerase sequences with ever higher fidelity, despite error rates above the error catastrophe threshold. Our work shows that experimentally characterized kinetics and thermodynamics of RNA replication allow us to determine the physicochemical conditions required for the spontaneous crystallization of biological information. Our findings also suggest that among many potential oligomers capable of templated replication, RNAs may have evolved to form prebiotic genomes due to the value of their nonenzymatic fidelity. Public Library of Science 2012-05-31 /pmc/articles/PMC3364946/ /pubmed/22693440 http://dx.doi.org/10.1371/journal.pcbi.1002534 Text en This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. https://creativecommons.org/publicdomain/zero/1.0/ This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. |
spellingShingle | Research Article Woo, Hyung-June Vijaya Satya, Ravi Reifman, Jaques Thermodynamic Basis for the Emergence of Genomes during Prebiotic Evolution |
title | Thermodynamic Basis for the Emergence of Genomes during Prebiotic Evolution |
title_full | Thermodynamic Basis for the Emergence of Genomes during Prebiotic Evolution |
title_fullStr | Thermodynamic Basis for the Emergence of Genomes during Prebiotic Evolution |
title_full_unstemmed | Thermodynamic Basis for the Emergence of Genomes during Prebiotic Evolution |
title_short | Thermodynamic Basis for the Emergence of Genomes during Prebiotic Evolution |
title_sort | thermodynamic basis for the emergence of genomes during prebiotic evolution |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3364946/ https://www.ncbi.nlm.nih.gov/pubmed/22693440 http://dx.doi.org/10.1371/journal.pcbi.1002534 |
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