Abstract

Catalysis by nucleic acids is indispensable for extant cellular life, and it is widely accepted that nucleic acid enzymes were crucial for the emergence of primitive life 3.5‐4 billion years ago. However, geochemical conditions on early Earth must have differed greatly from the constant internal milieus of today's cells. In order to explore plausible scenarios for early molecular evolution, it is therefore essential to understand how different physicochemical parameters, such as temperature, pH, and ionic composition, influence nucleic acid catalysis and to explore to what extent nucleic acid enzymes can adapt to non‐physiological conditions. In this article, we give an overview of the research on catalysis of nucleic acids, in particular catalytic RNAs (ribozymes) and DNAs (deoxyribozymes), under extreme and/or unusual conditions that may relate to prebiotic environments.

Highlights

  • Catalysis by nucleic acids is indispensable for extant cellular life, and it is widely accepted that nucleic acid enzymes were crucial for the emergence of primitive life 3.54 billion years ago

  • We give an overview of the research on catalysis of nucleic acids, in particular catalytic RNAs and DNAs, under extreme and/or unusual conditions that may relate to prebiotic environments

  • We will explore the range of conditions under which nucleic acid catalysis is possible, highlighting how nucleic acids can adapt to extreme conditions, and how these conditions can both support and potentiate function

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Summary

Introduction

The discovery of the catalytic properties of nucleic acids by Cech and Altman in 1982-83 both redefined biological catalysis and provided compelling support for origin of life hypotheses centered around nucleic acid-based information storage and catalysis, in particular the “RNA world” hypothesis first suggested by Alexander Rich, in which self-replicating RNA emerged prior to the evolution of DNA and proteins.[1,2,3] Despite the prevalence of the RNA World hypothesis and related conjectures, such as different “pre-RNA” worlds[4] and mixed chimeric systems including, for example, both RNA and DNA,[5] a key unanswered question is: under which environmental conditions did functional nucleic acids emerge and sustain themselves? Constraining the parameter space of a habitable early Earth is crucial to understanding the emergence of life. ‘warm little ponds’ on land would be subject to temperature, composition and concentration fluctuations due to evaporation and condensation driven by day–night cycles,[61] eutectic phases in frozen environments lead to strong solute up-concentration and significant pH shifts,[62] and hydrothermal vents provide extreme temperature and pH gradients.[51] Any of these environments might provide shelter from adverse conditions such as UV radiation, the surface intensity of which was several orders of magnitude higher than today.[63] In this focus review, we will explore the range of conditions under which nucleic acid catalysis is possible, highlighting how nucleic acids can adapt to extreme conditions, and how these conditions can both support and potentiate function. Reaction conditions may deviate strongly from in vivo or typical in vitro environments

Folding of nucleic acids
Modes of metal ion—nucleic acid interaction
Impact of metal ions on nucleic acid catalysis
Metal ion induced hydrolysis
Potential pH values in prebiotic settings
Heat tolerance of nucleic acid catalysis
Prebiotic temperatures and thermophilic RNAs
In vitro selection of thermophilic nucleic acid enzymes
Pressure as a modulator of nucleic acid catalysis
Freezing and dehydration induced ribozyme catalysis
Ultraviolet light
Findings
Conclusion and perspectives
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