Nonequilibrium correlations in minimal dynamical models of polymer copying

Jenny M. Poulton, Pieter Rein ten Wolde, and Thomas E. Ouldridge
PNAS February 5, 2019 116 (6) 1946-1951; published ahead of print February 5, 2019 https://doi.org/10.1073/pnas.1808775116

  1. Edited by David J. Schwab, Northwestern University, and accepted by Editorial Board Member Curtis G. Callan Jr. December 11, 2018 (received for review May 24, 2018)

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Significance

The ordering of chemical units within DNA, RNA, and proteins carries information about how living cells operate, and copying these sequences accurately is vital. We have a limited understanding of the fundamental physical underpinnings of these processes, since important mechanistic constraints due to the need to separate daughter sequences from their templates have never been investigated in detail. By considering the simplest models that incorporate these constraints, we highlight their profound consequences in terms of the effort that must be expended to make accurate copies. These insights will help us to understand not only life today but also how early replicators may have functioned in the past, and how we might develop synthetic copiers in the future.

Abstract

Living systems produce “persistent” copies of information-carrying polymers, in which template and copy sequences remain correlated after physically decoupling. We identify a general measure of the thermodynamic efficiency with which these nonequilibrium states are created and analyze the accuracy and efficiency of a family of dynamical models that produce persistent copies. For the weakest chemical driving, when polymer growth occurs in equilibrium, both the copy accuracy and, more surprisingly, the efficiency vanish. At higher driving strengths, accuracy and efficiency both increase, with efficiency showing one or more peaks at moderate driving. Correlations generated within the copy sequence, as well as between template and copy, store additional free energy in the copied polymer and limit the single-site accuracy for a given chemical work input. Our results provide insight into the design of natural self-replicating systems and can aid the design of synthetic replicators.

Footnotes

  • ↵1To whom correspondence should be addressed. Email: t.ouldridge{at}imperial.ac.uk.

  • Author contributions: T.E.O. designed research; J.M.P. performed research; J.M.P., P.R.t.W., and T.E.O. analyzed data; and J.M.P., P.R.t.W., and T.E.O. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. D.J.S. is a guest editor invited by the Editorial Board.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1808775116/-/DCSupplemental.

Published under the PNAS license.

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Nonequilibrium correlations in minimal dynamical models of polymer copying
Jenny M. Poulton, Pieter Rein ten Wolde, Thomas E. Ouldridge
Proceedings of the National Academy of Sciences Feb 2019, 116 (6) 1946-1951; DOI: 10.1073/pnas.1808775116
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