Thermodynamics of accuracy in kinetic proofreading: Dissipation and efficiency trade-offs

TL;DR

This paper provides a thermodynamic analysis of kinetic proofreading, exploring the trade-offs between accuracy, dissipation, and efficiency in enzyme-assisted processes, and introduces models accounting for correlations between steps.

Contribution

It offers a consistent thermodynamic framework and efficiency measure for proofreading models, including correlated step analysis, highlighting energetic and kinetic discrimination regimes.

Findings

Proofreading efficiency is constrained by dissipation and error trade-offs.

Correlations between assembly steps influence accuracy and energetics.

Distinct regimes of energetic and kinetic discrimination affect process performance.

Abstract

The high accuracy exhibited by biological information transcription processes is due to kinetic proofreading, i.e., by a mechanism which reduces the error rate of the information-handling process by driving it out of equilibrium. We provide a consistent thermodynamic description of enzyme-assisted assembly processes involving competing substrates, in a Master Equation framework. We introduce and evaluate a measure of the efficiency based on rigorous non-equilibrium inequalities. The performance of several proofreading models are thus analyzed and the related time, dissipation and efficiency vs. error trade-offs exhibited for different discrimination regimes. We finally introduce and analyze in the same framework a simple model which takes into account correlations between consecutive enzyme-assisted assembly steps. This work highlights the relevance of the distinction between energetic and kinetic discrimination regimes in enzyme-substrate interactions.