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Insights from an information thermodynamics analysis of a synthetic molecular motor

Nature Chemistry volume 14, pages 530–537 (2022)Cite this article

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Abstract

Information is physical, a realization that has transformed the physics of measurement and communication. However, the flow between information, energy and mechanics in chemical systems remains largely unexplored. Here we analyse a minimalist autonomous chemically driven molecular motor in terms of information thermodynamics, a framework that quantitatively relates information to other thermodynamic parameters. The treatment reveals how directional motion is generated by free energy transfer from chemical to mechanical (conformational and/or co-conformational) processes by ‘energy flow’ and ‘information flow’. It provides a thermodynamic level of understanding of molecular motors that is general, complements previous analyses based on kinetics and has practical implications for machine design. In line with kinetic analysis, we find that power strokes do not affect the directionality of chemically driven machines. However, we find that power strokes can modulate motor velocity, the efficiency of free energy transfer and the number of fuel molecules consumed per cycle. This may help explain the role of such (co-)conformational changes in biomachines and illustrates the interplay between energy and information in chemical systems.

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Fig. 1: A Rosetta Stone for chemical (reactions and co-conformational dynamics) and information thermodynamics descriptions of a molecular motor: two distinct but complementary accounts of the processes involved in a minimalist, autonomous, chemically fuelled, molecular rotary motor.
Fig. 2: Rotary motor as an open and bipartite chemical reaction network.
Fig. 3: Numerical simulations of different molecular motor design modifications.
Fig. 4: Potential ways of achieving different molecular motor design modifications.

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Data availability

All data needed to reproduce the numerical results are reported in the Supplementary Information.

Code availability

The code that generated the plots is available at the following link: gitlab.com/emanuele.penocchio/infothermorotmot

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Acknowledgements

We acknowledge support from the European Research Council (ERC Consolidator grant no. 681456 to M.E. and funding to E.P.; ERC Advanced grant no. 786630 to D.A.L.), the FQXi Foundation, project ‘Information as a fuel in colloids and superconducting quantum circuits’ (grant no. FQXi-IAF19-05 to M.E.), the Engineering and Physical Sciences Research Council (EPSRC; grant no. EP/P027067/1 to D.A.L.), the Deutsche Forschungsgemeinschaft (a postdoctoral fellowship to E.K.) and the University of Manchester and EPSRC for PhD studentships to S.A. and B.M.W.R. D.A.L. is a Royal Society Research Professor. We thank R. D. Astumian for valuable discussions regarding the science in this study as well as robust debate regarding the use of the term ‘local detailed balance’ within the stochastic thermodynamics community.

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Authors and Affiliations

  1. Department of Chemistry, University of Manchester, Manchester, UK

    Shuntaro Amano, Elisabeth Kreidt, David A. Leigh & Benjamin M. W. Roberts

  2. Department of Physics and Materials Science, University of Luxembourg, Luxembourg City, Luxembourg

    Massimiliano Esposito & Emanuele Penocchio

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  1. Shuntaro Amano
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Contributions

S.A., B.M.W.R. and E.K. proposed the collaboration. E.P. developed the theoretical model. S.A., B.M.W.R., E.P. and E.K. carried out the theoretical analysis and simulations. D.A.L. and M.E. directed the research. All authors contributed to the analysis of the results and the writing of the manuscript.

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Correspondence to David A. Leigh or Emanuele Penocchio.

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Supplementary Sections I–VI, Figs. 1–6, equations 1–70 and Table I.

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Amano, S., Esposito, M., Kreidt, E. et al. Insights from an information thermodynamics analysis of a synthetic molecular motor. Nat. Chem. 14, 530–537 (2022). https://doi.org/10.1038/s41557-022-00899-z

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