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.

  • Article
  • Published:

An artificial molecular pump

Nature Nanotechnology volume 10, pages 547–553 (2015)Cite this article

Subjects

Abstract

Carrier proteins consume fuel in order to pump ions or molecules across cell membranes, creating concentration gradients. Their control over diffusion pathways, effected entirely through noncovalent bonding interactions, has inspired chemists to devise artificial systems that mimic their function. Here, we report a wholly artificial compound that acts on small molecules to create a gradient in their local concentration. It does so by using redox energy and precisely organized noncovalent bonding interactions to pump positively charged rings from solution and ensnare them around an oligomethylene chain, as part of a kinetically trapped entanglement. A redox-active viologen unit at the heart of a dumbbell-shaped molecular pump plays a dual role, first attracting and then repelling the rings during redox cycling, thereby enacting a flashing energy ratchet mechanism with a minimalistic design. Our artificial molecular pump performs work repetitively for two cycles of operation and drives rings away from equilibrium toward a higher local concentration.

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

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

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

Figure 1: A blueprint for an artificial molecular pump that acts to compartmentalize rings in a high-energy state on a polymethylene chain.
Figure 2: Components of the artificial molecular pump.
Figure 3: Graphical representations of the pumping mechanism, which operates in response to redox cycling, with simplified illustrations of the corresponding energy profiles.
Figure 4: 1H NMR spectroscopic evidence in support of the stepwise pumping of rings onto DB3+ over two cycles of reduction and oxidation.
Figure 5: 1H NOESY and DOSY spectroscopic evidence confirms that the ring(s) encircle the ring-collecting oligomethylene chain.

Similar content being viewed by others

References

  1. Vinothkumar, K. R. & Henderson, R. Structures of membrane proteins. Quart. Rev. Biophys. 43, 65–158 (2010).

    Article  CAS  Google Scholar 

  2. Boyer, P. D. Energy, life, and ATP (Nobel lecture). Angew. Chem. Int. Ed. 37, 2296–2307 (1998).

    Article  Google Scholar 

  3. Walker, J. E. ATP synthesis by rotary catalysis (Nobel lecture). Angew. Chem. Int. Ed. 37, 2308–2319 (1998).

    Article  CAS  Google Scholar 

  4. Skou, J. C. The identification of the sodium–potassium pump (Nobel lecture). Angew. Chem. Int. Ed. 37, 2320–2328 (1998).

    Article  CAS  Google Scholar 

  5. Shi, Y. G. Common folds and transport mechanisms of secondary active transporters. Annu. Rev. Biophys. 42, 51–72 (2013).

    Article  Google Scholar 

  6. Gai, F., Hasson, K. C., McDonald, J. C. & Anfinrud, P. A. Chemical dynamics in proteins: the photoisomerization of retinal in bacteriorhodopsin. Science 279, 1886–1891 (1998).

    Article  CAS  Google Scholar 

  7. Brandt, U. Energy converting NADH: quinone oxidoreductase (complex I). Annu. Rev. Biochem. 75, 69–92 (2006).

    Article  CAS  Google Scholar 

  8. Sazanoz, L. A. The mechanism of coupling between electron transfer and proton translocation in respiratory complex I. J. Bioenerg. Biomembr. 46, 247–253 (2014).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  10. Kinbara, K. & Aida, T. Toward intelligent molecular machines: directed motions of biological and artificial molecules and assemblies. Chem. Rev. 105, 1377–1400 (2005).

    Article  CAS  Google Scholar 

  11. Kay, E. R., Leigh, D. A. & Zerbetto, F. Synthetic molecular motors and mechanical machines. Angew. Chem. Int. Ed. 46, 72–191 (2007).

    Article  CAS  Google Scholar 

  12. Krishnan, Y. & Simmel, F. C. Nucleic acid based molecular devices. Angew. Chem. Int. Ed. 50, 3124–3156 (2011).

    Article  CAS  Google Scholar 

  13. Coskun, A., Banaszak, M., Astumian, R. D., Stoddart, J. F. & Grzybowski, B. A. Great expectations: can artificial molecular machines deliver on their promise? Chem. Soc. Rev. 41, 19–30 (2012).

    Article  CAS  Google Scholar 

  14. Michl, J. & Sykes, E. C. H. Molecular rotors and motors: recent advances and future challenges. ACS Nano 3, 1042–1048 (2009).

    Article  CAS  Google Scholar 

  15. Vogelsberg, C. S. & Garcia-Garibay, M. A. Crystalline molecular machines: function, phase order, dimensionality, and composition. Chem. Soc. Rev. 41, 1892–1910 (2012).

    Article  CAS  Google Scholar 

  16. Steinburgh-Yfrach, G. et al. Conversion of light energy to proton potential in liposomes by artificial photosynthetic reaction centres. Nature 385, 239–241 (1997).

    Article  Google Scholar 

  17. Bhosale, S. et al. Photoproduction of proton gradients with π-stacked fluorophore scaffolds in lipid bilayers. Science 313, 84–86 (2006).

    Article  CAS  Google Scholar 

  18. Xie, X., Crespo, G. A., Mistlberger, G. & Bakker, E. Photocurrent generation based on a light-driven proton pump in an artificial liquid membrane. Nature Chem. 6, 202–207 (2014).

    Article  CAS  Google Scholar 

  19. Bennett, I. M. et al. Active transport of Ca2+ by an artificial photosynthetic membrane. Nature 420, 398–401 (2002).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  21. Bruns, C. & Stoddart, J. F. Rotaxane-based molecular muscles. Acc. Chem. Res. 47, 2186–2199 (2014).

    Article  CAS  Google Scholar 

  22. Muraoka, T., Kinbara, K. & Aida, T. Mechanical twisting of a guest by a photoresponsive host. Nature 440, 512–515 (2006).

    Article  CAS  Google Scholar 

  23. Brown, R. A., Diemer, V., Webb, S. J. & Clayden, J. End-to-end conformational communication through a synthetic purinergic receptor by ligand-induced helicity switching. Nature Chem. 5, 853–860 (2013).

    Article  CAS  Google Scholar 

  24. Leigh, D. A., Lewandowska, U., Lewandowski, B. & Wilson, M. R. Synthetic molecular walkers. Top. Curr. Chem. 354, 111–138 (2014).

    Article  CAS  Google Scholar 

  25. Fletcher, S. P., Dumur, F., Pollard, M. M. & Feringa, B. L. A reversible, unidirectional molecular rotary motor driven by chemical energy. Science 310, 80–82 (2005).

    Article  CAS  Google Scholar 

  26. Lu, C.-H., Cecconello, A., Elbaz, J., Credi, A. & Willner, I. A three-station DNA catenane rotary motor with controlled directionality. Nano Lett. 13, 2303–2308 (2013).

    Article  CAS  Google Scholar 

  27. Greb, L. & Lehn, J-M. Light-driven molecular motors: imines as four-step or two-step unidirectional rotors. J. Am. Chem. Soc. 136, 13114–13117 (2014).

    Article  CAS  Google Scholar 

  28. Chatterjee, M. N., Kay, E. R. & Leigh, D. A. Beyond switches: ratcheting a particle energetically uphill with a compartmentalized molecular machine. J. Am. Chem. Soc. 128, 4058–4073 (2006).

    Article  CAS  Google Scholar 

  29. Serreli, V., Lee, C-F., Kay, E. R. & Leigh, D. A. A molecular information ratchet. Nature 445, 523–527 (2007).

    Article  CAS  Google Scholar 

  30. Van Dongen, S. F. M., Elemans, J. A. A. W., Rowan, A. E. & Nolte, R. J. M. Processive catalysis. Angew. Chem. Int. Ed. 53, 11420–11428 (2014).

    Article  CAS  Google Scholar 

  31. Lewandowski, B. et al. Sequence-specific peptide synthesis by an artificial small-molecule machine. Science 339, 189–193 (2013).

    Article  CAS  Google Scholar 

  32. Yoon, H. J., Kuwabara, J., Kim, J-H. & Mirkin, C. A. Allosteric supramolecular triple-layer catalysts. Science 330, 66–69 (2010).

    Article  CAS  Google Scholar 

  33. Wang, J. & Feringa, B. L. Dynamic control of chiral space in a catalytic asymmetric reaction using a molecular motor. Science 331, 1429–1432 (2011).

    Article  CAS  Google Scholar 

  34. He, Y. & Liu, D. Autonomous multistep organic synthesis in a single isothermal solution mediated by a DNA walker. Nature Nanotech. 5, 778–782 (2010).

    Article  CAS  Google Scholar 

  35. McKee, M. L. et al. Programmable one-pot multistep organic synthesis using DNA junctions. J. Am. Chem. Soc. 134, 1446–1449 (2012).

    Article  CAS  Google Scholar 

  36. Gu, H., Chao, J., Xiao, S-J. & Seeman, N. C. A proximity-based programmable DNA nanoscale assembly line. Nature 465, 202–205 (2010).

    Article  CAS  Google Scholar 

  37. Ashton, P. R. et al. A [2]catenane made to order. Angew. Chem. Int. Ed. Engl. 28, 1396–1399 (1989).

    Article  Google Scholar 

  38. Collier, C. P. et al. A [2]catenane-based solid state electronically reconfigurable switch. Science 289, 1172–1175 (2000).

    Article  CAS  Google Scholar 

  39. Odell, B. et al. Cyclobis(paraquat-p-phenylene): a tetracationic multipurpose receptor. Angew. Chem. Int. Ed. Engl. 27, 1547–1550 (1988).

    Article  Google Scholar 

  40. Trabolsi, A. et al. Radically enhanced molecular recognition. Nature Chem. 2, 42–49 (2010).

    Article  CAS  Google Scholar 

  41. Fahrenbach, A. C. et al. Solution-phase mechanistic study and solid-state structure of a tris(bipyridinium radical cation) inclusion complex. J. Am. Chem. Soc. 134, 3061–3072 (2012).

    Article  CAS  Google Scholar 

  42. Cheng, C. et al. Energetically demanding transport in a supramolecular assembly. J. Am. Chem. Soc. 136, 14702–14705 (2014).

    Article  CAS  Google Scholar 

  43. Li, H. et al. Relative unidirectional translation in an artificial molecular assembly fueled by light. J. Am. Chem. Soc. 135, 18609–18620 (2013).

    Article  CAS  Google Scholar 

  44. McGonigal, P. R. et al. Controlling association kinetics in the formation of donor–acceptor pseudorotaxanes. Tetrahedron Lett. http://dx.doi.org/10.1016/j.tetlet.2015.01.169 (2015)

  45. Sevick, E. M. & Williams, D. R. M. A piston-rotaxane with two potential stripes: force transitions and yield stresses. Molecules 18, 13398–13409 (2013).

    Article  CAS  Google Scholar 

  46. Lehn, J-M. Supramolecular Chemistry: Concepts and Perspectives (Wiley-VCH, 1995).

    Book  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This material is based on work supported by the National Science Foundation (NSF; CHE-1308107). The authors acknowledge the Integrated Molecular Structure Education and Research Center at Northwestern University for providing access to equipment for relevant experiments. The authors acknowledge the QUEST High-Performance Computing Cluster at Northwestern University for a research allocation of computer time. S.T.S. thanks the International Institute for Nanotechnology (IIN) at Northwestern University for a postdoctoral fellowship.

Author information

Authors and Affiliations

  1. Department of Chemistry, Northwestern University, 2145 Sheridan Road, Evanston, 60208, Illinois, USA

    Chuyang Cheng, Paul R. McGonigal, Severin T. Schneebeli, Hao Li, Nicolaas A. Vermeulen, Chenfeng Ke & J. Fraser Stoddart

Authors
  1. Chuyang Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul R. McGonigal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Severin T. Schneebeli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nicolaas A. Vermeulen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chenfeng Ke
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. Fraser Stoddart
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

C.C. and N.A.V. conceived the project. C.C. designed, synthesized and tested the compounds. P.R.M., S.T.S. and H.L. performed the barrier searching work. P.R.M. and C.C. wrote the paper. N.A.V. and C.K. helped in evaluating the results and commented on the contents of the manuscript. J.F.S. directed the project.

Corresponding author

Correspondence to J. Fraser Stoddart.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary information (PDF 5711 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheng, C., McGonigal, P., Schneebeli, S. et al. An artificial molecular pump. Nature Nanotech 10, 547–553 (2015). https://doi.org/10.1038/nnano.2015.96

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nnano.2015.96

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing