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Autonomous fuelled directional rotation about a covalent single bond

Nature volume 604, pages 80–85 (2022)Cite this article

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Abstract

Biology operates through autonomous chemically fuelled molecular machinery1, including rotary motors such as adenosine triphosphate synthase2 and the bacterial flagellar motor3. Chemists have long sought to create analogous molecular structures with chemically powered, directionally rotating, components4,5,6,7,8,9,10,11,12,13,14,15,16,17. However, synthetic motor molecules capable of autonomous 360° directional rotation about a single bond have proved elusive, with previous designs lacking either autonomous fuelling7,10,12 or directionality6. Here we show that 1-phenylpyrrole 2,2′-dicarboxylic acid18,19 (1a) is a catalysis-driven20,21 motor that can continuously transduce energy from a chemical fuel9,20,21,22,23,24,25,26,27 to induce repetitive 360° directional rotation of the two aromatic rings around the covalent N–C bond that connects them. On treatment of 1a with a carbodiimide21,25,26,27, intramolecular anhydride formation between the rings and the anhydride’s hydrolysis both occur incessantly. Both reactions are kinetically gated28,29,30 causing directional bias. Accordingly, catalysis of carbodiimide hydration by the motor molecule continuously drives net directional rotation around the N–C bond. The directionality is determined by the handedness of both an additive that accelerates anhydride hydrolysis and that of the fuel, and is easily reversed additive31. More than 97% of fuel molecules are consumed through the chemical engine cycle24 with a directional bias of up to 71:29 with a chirality-matched fuel and additive. In other words, the motor makes a ‘mistake’ in direction every three to four turns. The 26-atom motor molecule’s simplicity augurs well for its structural optimization and the development of derivatives that can be interfaced with other components for the performance of work and tasks32,33,34,35,36.

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Fig. 1: Chemical engine cycle of an autonomous, continuously operating, chemically fuelled single bond rotary motor.
Fig. 2: Mechanical gating of 1-arylpyrrole 2,2′-dicarboxylic acids (1).
Fig. 3: Chemical transformations of 1-arylpyrrole 2,2′-dicarboxylic acids (1).
Fig. 4: Autonomous chemically fuelled operation of 1-arylpyrrole 2,2′-dicarboxylic acids (1).

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Data availability

The data that support the findings of this study are available within the paper and its Supplementary Information, or are available from the Mendeley data repository (https://data.mendeley.com/) at http://doi.org/10.17632/2zvst4kg2w.1.

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Acknowledgements

We thank the Engineering and Physical Sciences Research Council (EPSRC; grant number EP/P027067/1), the European Research Council (ERC; Advanced Grant number 786630) and the German Research Foundation (DFG; Individual Postdoctoral Fellowship to E.K.) for funding, the University of Manchester’s Department of Chemistry Services for mass spectrometry, I. J. Vitorica-Yrezabal for X-ray crystallography used to assign atropisomer handedness, S. Amano and J. M. Gallagher for useful discussions, and S. Jantzen of Biocinematics for the rotary motor animation. D.A.L. is a Royal Society Research Professor.

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Author notes

  1. These authors contributed equally: Stefan Borsley, Elisabeth Kreidt, Benjamin M. W. Roberts

Authors and Affiliations

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

    Stefan Borsley, Elisabeth Kreidt, David A. Leigh & Benjamin M. W. Roberts

  2. School of Chemistry and Molecular Engineering, East China Normal University, Shanghai, China

    David A. Leigh

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Contributions

S.B., E.K. and B.M.W.R. designed and carried out the experiments. D.A.L. 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.

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Supplementary Information

Supplementary sections 1–7 and Appendix

Supplementary Video 1

Animation of the design and autonomous chemically fuelled rotation of motor molecule 1a. Credit: Stuart Jantzen, Biocinematics.

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Borsley, S., Kreidt, E., Leigh, D.A. et al. Autonomous fuelled directional rotation about a covalent single bond. Nature 604, 80–85 (2022). https://doi.org/10.1038/s41586-022-04450-5

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