Perspective | Published:

Energy consumption in chemical fuel-driven self-assembly

Nature Nanotechnologyvolume 13pages882889 (2018) | Download Citation


Nature extensively exploits high-energy transient self-assembly structures that are able to perform work through a dissipative process. Often, self-assembly relies on the use of molecules as fuel that is consumed to drive thermodynamically unfavourable reactions away from equilibrium. Implementing this kind of non-equilibrium self-assembly process in synthetic systems is bound to profoundly impact the fields of chemistry, materials science and synthetic biology, leading to innovative dissipative structures able to convert and store chemical energy. Yet, despite increasing efforts, the basic principles underlying chemical fuel-driven dissipative self-assembly are often overlooked, generating confusion around the meaning and definition of scientific terms, which does not favour progress in the field. The scope of this Perspective is to bring closer together current experimental approaches and conceptual frameworks. From our analysis it also emerges that chemically fuelled dissipative processes may have played a crucial role in evolutionary processes.

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  1. 1.

    Grzybowski, B. A. & Huck, W. T. S. The nanotechnology of life-inspired systems. Nat. Nanotech. 11, 585–592 (2016).

  2. 2.

    Kassem, S. et al. Artificial molecular motors. Chem. Soc. Rev. 46, 2592–2621 (2017).

  3. 3.

    Koumura, N., Zijlstra, R. W. J., van Delden, R. A., Harada, N. & Feringa, B. L. Light-driven monodirectional molecular rotor. Nature 401, 152–155 (1999).

  4. 4.

    Ragazzon, G., Baroncini, M., Silvi, S., Venturi, M. & Credi, A. Light-powered autonomous and directional motion of a dissipative self-assembling system. Nat. Nanotech. 10, 70–75 (2015).

  5. 5.

    Cheng, C. et al. An artificial molecular pump. Nat. Nanotech. 10, 547–553 (2015).

  6. 6.

    Wilson, M. R. et al. An autonomous chemically fuelled small-molecule motor. Nature 534, 235–240 (2016).

  7. 7.

    Erbas-Cakmak, S. et al. Rotary and linear molecular motors driven by pulses of a chemical fuel. Science 358, 340–343 (2017).

  8. 8.

    Merindol, R. & Walther, A. Materials learning from life: concepts for active, adaptive and autonomous molecular systems. Chem. Soc. Rev. 46, 5588–5619 (2017).

  9. 9.

    van Rossum, S. A. P., Tena-Solsona, M., van Esch, J. H., Eelkema, R. & Boekhoven, J. Dissipative out-of-equilibrium assembly of man-made supramolecular materials. Chem. Soc. Rev. 46, 5519–5535 (2017).

  10. 10.

    Li, Q. et al. Macroscopic contraction of a gel induced by the integrated motion of light-driven molecular motors. Nat. Nanotech. 10, 161–165 (2015).

  11. 11.

    Boekhoven, J., Hendriksen, W., Koper, G., Eelkema, R. & van Esch, J. Transient assembly of active materials fueled by a chemical reaction. Science 349, 1075–1079 (2015).

  12. 12.

    Ikegami, T., Kageyama, Y., Obara, K. & Takeda, S. Dissipative and autonomous square-wave self-oscillation of a macroscopic hybrid self-assembly under continuous light irradiation. Angew. Chem. Int. Ed. 55, 8239–8243 (2016).

  13. 13.

    Foy, J. T. et al. Dual-light control of nanomachines that integrate motor and modulator subunits. Nat. Nanotech. 12, 540–545 (2017).

  14. 14.

    Fialkowski, M. et al. Principles and implementations of dissipative (dynamic) self-assembly. J. Phys. Chem. B. 110, 2482–2496 (2006).

  15. 15.

    Grzybowski, B. A., Stone, H. A. & Whitesides, G. M. Dynamic self-assembly of magnetized, millimetre-sized objects rotating at a liquid-air interface. Nature 405, 1033–1036 (2000).

  16. 16.

    Krabbenborg, S. O., Veerbeek, J. & Huskens, J. Spatially controlled out-of-equilibrium host–guest system under electrochemical control. Chem. Eur. J. 21, 9638–9644 (2015).

  17. 17.

    Göstl, R., Senf, A. & Hecht, S. Remote-controlling chemical reactions by light: towards chemistry with high spatio-temporal resolution. Chem. Soc. Rev. 43, 1982–1996 (2014).

  18. 18.

    Göstl, R. & Hecht, S. Controlling covalent connection and disconnection with light. Angew. Chem. Int. Ed. 53, 8784–8787 (2014).

  19. 19.

    Kathan, M. & Hecht, S. Photoswitchable molecules as key ingredients to drive systems away from the global thermodynamic minimum. Chem. Soc. Rev. 46, 5536–5550 (2017).

  20. 20.

    Walsh, C. T., Tu, B. P. & Tang, Y. Eight kinetically stable but thermodynamically activated molecules that power cell metabolism. Chem. Rev. 118, 1460–1494 (2018).

  21. 21.

    Pezzato, C. & Prins, L. J. Transient signal generation in a self-assembled nanosystem fueled by ATP. Nat. Commun. 6, 7790 (2015).

  22. 22.

    Maiti, S., Fortunati, I., Ferrante, C., Scrimin, P. & Prins, L. J. Dissipative self-assembly of vesicular nanoreactors. Nat. Chem. 8, 725–731 (2016).

  23. 23.

    Dhiman, S., Jain, A. & George, S. J. Transient helicity: fuel-driven temporal control over conformational switching in a supramolecular polymer. Angew. Chem. Int. Ed. 56, 1329–1333 (2017).

  24. 24.

    Dhiman, S., Jain, A., Kumar, M. & George, S. J. Adenosine-phosphate-fueled, temporally programmed supramolecular polymers with multiple transient states. J. Am. Chem. Soc. 139, 16568–16575 (2017).

  25. 25.

    Hao, X., Sang, W., Hu, J. & Yan, Q. Pulsating polymer micelles via ATP-fueled dissipative self-assembly. ACS Macro Lett. 6, 1151–1155 (2017).

  26. 26.

    Boekhoven, J. et al. Dissipative self-assembly of a molecular gelator by using a chemical fuel. Angew. Chem. Int. Ed. 49, 4825–4828 (2010).

  27. 27.

    Dambenieks, A. K., Vu, P. H. Q. & Fyles, T. M. Dissipative assembly of a membrane transport system. Chem. Sci. 5, 3396–3403 (2014).

  28. 28.

    Fanlo-Virgós, H., Alba, A. R., Hamieh, S., Colomb-Delsuc, M. & Otto, S. Transient substrate-induced catalyst formation in a dynamic molecular network. Angew. Chem. Int. Ed. 53, 11346–11350 (2014).

  29. 29.

    Wood, C. S., Browne, C., Wood, D. M. & Nitschke, J. R. Fuel-controlled reassembly of metal−organic architectures. ACS Cent. Sci. 1, 504–509 (2015).

  30. 30.

    Tena-Solsona, M. et al. Non-equilibrium dissipative supramolecular materials with a tunable lifetime. Nat. Commun. 8, 15895 (2017).

  31. 31.

    Kariyawasam, L. S. & Hartley, C. S. Dissipative assembly of aqueous carboxylic acid anhydrides fueled by carbodiimides. J. Am. Chem. Soc. 139, 11949–11955 (2017).

  32. 32.

    Sawczyk, M. & Klajn, R. Out-of-equilibrium aggregates and coatings during seeded growth of metallic nanoparticles. J. Am. Chem. Soc. 139, 17973–17978 (2017).

  33. 33.

    Sorrenti, A., Leira-Iglesias, J., Sato, A. & Hermans, T. M. Non-equilibrium steady-states in supramolecular polymerization. Nat. Commun. 8, 15899 (2017).

  34. 34.

    van Ravensteijn, B. G. P., Hendriksen, W. E., Eelkema, R., van Esch, J. H. & Kegel, W. K. Fuel-mediated transient clustering of colloidal building blocks. J. Am. Chem. Soc. 139, 9763–9766 (2017).

  35. 35.

    Mishra, A. et al. Biomimetic tempolar self-assembly via fuel-driven controlled supramolecular polymerization. Nat. Commun. 9, 1295 (2018).

  36. 36.

    Della Sala, F., Maiti, S., Bonanni, A., Scrimin, P. & Prins, L. Fuel-selective transient activation of nanosystems for signal generation. Angew. Chem. Int. Ed. 130, 1611–1615 (2018).

  37. 37.

    Astumian, R. D. Stochastic conformational pumping: a mechanism for free-energy transduction by molecules. Annu. Rev. Biophys. 40, 289–313 (2011).

  38. 38.

    Astumian, R. D. Stochastic pumping of non-equilibrium steady-states: how molecules adapt to a fluctuating environment. Chem. Commun. 54, 427–444 (2018).

  39. 39.

    Astumian, R. D. Design principles for Brownian molecular machines: how to swim in molasses and walk in a hurricane. Phys. Chem. Chem. Phys. 9, 5067–5083 (2007).

  40. 40.

    Alvarez-Pérez, M., Goldup, S. M., Leigh, D. A. & Slawin, A. M. Z. A chemically-driven molecular information ratchet. J. Am. Chem. Soc. 130, 1836–1838 (2008).

  41. 41.

    Astumian, R. D. Microscopic reversibility as the organizing principle of molecular machines. Nat. Nanotech. 7, 684–688 (2012).

  42. 42.

    Rao, R. & Esposito, M. Nonequilibrium thermodynamics of chemical reaction networks: wisdom from stochastic thermodynamics. Phys. Rev. X 6, 041064 (2016).

  43. 43.

    Kondepudi, D. & Prigogine, I. Modern Thermodynamics: From Heat Engines to Dissipative Structures (Wiley, Hoboken, 1998).

  44. 44.

    Hess, H. & Ross, J. L. Nonequilibrium assembly of microtubules: from molecules to autonomous chemical robots. Chem. Soc. Rev. 46, 5570–5587 (2017).

  45. 45.

    David-Pfeuty, T., Erickson, H. P. & Pantaloni, D. Guanosinetriphosphatase activity of tubulin associated with microtubule assembly. Proc. Natl Acad. Sci. USA 74, 5372–5376 (1977).

  46. 46.

    Caplow, M. & Shanks, J. Mechanism of the microtubule GTPase reaction. J. Biol. Chem. 265, 8935–8941 (1990).

  47. 47.

    Bowne-Anderson, H., Zanic, M., Kauer, M. & Howard, J. Microtubule dynamic instability: a new model with coupled GTP hydrolysis and multistep catastrophe. Bioessays 35, 452–461 (2013).

  48. 48.

    Desai, A. & Mitchison, T. J. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83–117 (1997).

  49. 49.

    Epstein, I. R. & Xu, B. Reaction-diffusion processes at the nano- and microscales. Nat. Nanotech. 11, 312–319 (2016).

  50. 50.

    England, J. L. Dissipative adaptation in driven self-assembly. Nat. Nanotech. 10, 919–923 (2015).

  51. 51.

    Perunov, N., Marsland, R. A. & England, J. L. Statistical physics of adaptation. Phys. Rev. X 6, 021036 (2016).

  52. 52.

    Del Grosso, E., Amodio, A., Ragazzon, G., Prins, L. & Ricci, F. Dissipative synthetic DNA-based receptors for the transient load and release of molecular cargo. Angew. Chem. Int. Ed. 57, 10489–10493 (2018).

  53. 53.

    Hoffmann, P. M. Life’s Ratchet: How Molecular Machines Extract Order from Chaos (Basic Books, New York, 2012).

  54. 54.

    Branscomb, E., Biancalani, T., Goldenfeld, N. & Russell, M. Escapement mechanisms and the conversion of disequilibria; the engines of creation. Phys. Rep. 677, 1–60 (2017).

  55. 55.

    Erbas-Cakmak, S., Leigh, D. A., McTernan, C. T. & Nussbaumer, A. L. Artificial molecular machines. Chem. Rev. 115, 10081–10206 (2015).

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The authors would like to acknowledge E. Penocchio and D. Frezzato for insightful discussions. The authors are grateful to D. Astumian for his help improving the clarity of the manuscript.

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  1. Department of Chemical Sciences, University of Padova, Padova, Italy

    • Giulio Ragazzon
    •  & Leonard J. Prins


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Correspondence to Leonard J. Prins.

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