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Prebiotic chemical reactivity in solution with quantum accuracy and microsecond sampling using neural network

Zakarya Benayad^1,2, Rolf David^1,2, Guillaume Stirnemann^1,2

¹CNRS Laboratoire de Biochimie Théorique, Institut de Biologie Physico-Chimique, Paris Sciences et Lettres University, Université Paris-Cité, 75005 Paris, France.

Proceedings of the National Academy of Sciences of the United States of America

|May 29, 2024

Summary

The abiotic synthesis of RNA oligonucleotides is challenging. Our study reveals a concerted, dissociative mechanism for phosphoester bond formation in water, explaining experimental results and guiding catalyst design.

Keywords:

explicit solvent neural network potentials origins of life reaction mechanism transition path sampling

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Area of Science:

Origin of Life Studies
Computational Chemistry
Biochemistry

Background:

RNA is a candidate for early autocatalytic systems, but its non-enzymatic synthesis is slow and mechanistically debated.
Experimental studies provide limited insight into the uncatalyzed RNA synthesis mechanism due to reaction slowness.

Purpose of the Study:

To elucidate the mechanism of phosphoester bond formation in RNA synthesis.
To investigate the role of water solvent in abiotic RNA formation.
To provide insights for designing efficient abiotic catalysts.

Main Methods:

Development and application of neural network potentials (NNPs) for complex chemical reactions.
Enhanced sampling simulations with quantum accuracy in explicit water.
Analysis of reaction pathways and transition states for phosphoester bond formation.

Main Results:

The preferred pathway involves a concerted, dissociative mechanism with a metaphosphate transition state.
Water molecules directly participate in proton exchange via nonbridging phosphate oxygens.
Diprotonated phosphate is less reactive than monoprotonated phosphate under typical conditions.

Conclusions:

The findings rationalize experimental observations and temperature dependence of RNA synthesis rates.
The study clarifies the role of solvent and protonation states in abiotic RNA formation.
This work provides a foundation for designing improved abiotic catalysts for RNA synthesis.