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Ribozyme Mutagenic Evolution: Mechanisms of Survival

Origins of Life and Evolution of Biospheres volume 51, pages 321–339 (2021)Cite this article

Abstract

Primeval populations replicating at high error rates required a mechanism to overcome the accumulation of mutations and information deterioration. Known strategies to overcome mutation pressures include RNA processivity, epistasis, selection, and quasispecies. We investigated the mechanism by which small molecular ribozyme populations can survive under high error rates by propagating several lineages under different mutagen concentrations. We found that every population that evolved without mutagen went extinct, while those subjected to mutagenic evolution survived. To understand how they survived, we characterized the evolved genotypic diversity, the formation of genotype-genotype interaction networks, the fitness of the most common mutants for each enzymatic step, and changes in population size along the course of evolution. We found that the elevated mutation rate was necessary for the populations to survive in the novel environment, in which all the steps of the metabolism worked to promote the survival of even less catalytically efficient ligases. Besides, an increase in population size and the mutational coupling of genotypes in close-knit networks, which helped maintain or recover lost genotypes making their disappearance transient, prevented Muller's ratchet and extinction.

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Data Availability

Ribozyme data can be made available.

Code Availability

Scripts can be made available.

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Acknowledgements

This work was supported by the Nucleic Acid Chemistry and Engineering, the Ecology and Evolution, and the Physics and Biology Units of the Okinawa Institute of Science and Technology Graduate University (OIST); the Japanese Society for the Promotion of Science KAKENHI Grant-in-Aid for Challenging Exploratory Research (grant number 16K14790) awarded to CDA; the Engineering and Physical Sciences Research Council, and the Medical Research Council (grant number EP/L016044/1) awarded to AA. We thank Robert Sinclair; and Jotun Hein (University of Oxford) for helpful discussions.

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Authors and Affiliations

  1. Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa Prefecture, Japan

    Carolina Diaz Arenas, Jonathan Miller, Alexander S. Mikheyev & Yohei Yokobayashi

  2. Wolfson Centre for Mathematical Biology, Mathematical Institute, University of Oxford, Oxford, UK

    Aleksandra Ardaševa

  3. Evolutionary Genomics Lab, Research School of Biology, Australian National University, Canberra, Australia

    Alexander S. Mikheyev

  4. Yale University, New Haven, CT, USA

    Carolina Diaz Arenas

Authors
  1. Carolina Diaz Arenas
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  2. Aleksandra Ardaševa
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  3. Jonathan Miller
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  4. Alexander S. Mikheyev
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  5. Yohei Yokobayashi
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Contributions

CDA, conception and design, performed the experiments, data analysis and discussion, manuscript writing; AA, scripts for data-processing and analysis, discussion, manuscript review; JM, ASM, YY, design, discussion, manuscript review.

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Correspondence to Carolina Diaz Arenas.

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Diaz Arenas, C., Ardaševa, A., Miller, J. et al. Ribozyme Mutagenic Evolution: Mechanisms of Survival. Orig Life Evol Biosph 51, 321–339 (2021). https://doi.org/10.1007/s11084-021-09617-0

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  • DOI: https://doi.org/10.1007/s11084-021-09617-0

Keywords

  • Ribozyme
  • Mutagenic evolution
  • Extinction
  • Genotypic diversity
  • Quasispecies