Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Energy consumption in chemical fuel-driven self-assembly

Abstract

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Self-assembly at equilibrium and out of equilibrium.
Fig. 2: Self-assembly under dissipative conditions.
Fig. 3: Dissipative self-assembly.
Fig. 4: Simulations of dissipative self-assembly processes.
Fig. 5: Dissipative self-assembly in nature.
Fig. 6: Dissipative adaptation.

References

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leonard J. Prins.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Information

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ragazzon, G., Prins, L.J. Energy consumption in chemical fuel-driven self-assembly. Nature Nanotech 13, 882–889 (2018). https://doi.org/10.1038/s41565-018-0250-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41565-018-0250-8

This article is cited by

Search

Quick links

Find nanotechnology articles, nanomaterial data and patents all in one place. Visit Nano by Nature Research