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Highly mechanosensitive ion channels from graphene-embedded crown ethers

Nature Materials volume 18, pages 76–81 (2019)Cite this article

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Abstract

The ability to tune ionic permeation across nanoscale pores profoundly impacts diverse fields from nanofluidic computing to drug delivery. Here, we take advantage of complex formation between crown ethers and dissolved metal ions to demonstrate graphene-based ion channels highly sensitive to externally applied lattice strain. We perform extensive room-temperature molecular dynamics simulations of the effects of tensile lattice strain on ion permeation across graphene-embedded crown ether pores. Our findings suggest the first instance of solid-state ion channels with an exponential permeation sensitivity to strain, yielding an order of magnitude ion current increase for 2% of isotropic lattice strain. Significant permeation tuning is also shown to be achievable with anisotropic strains. Finally, we demonstrate strain-controllable ion sieving in salt mixtures. The observed high mechanosensitivity is shown to arise from strain-induced control over the competition between ion–crown and ion–solvent interactions, mediated by the atomic thinness of graphene.

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Fig. 1: Examples of crown ethers and schematic of the simulated system.
Fig. 2: Potential of mean force curves as a function of the distance of the K+ ions from the pore-containing membrane.
Fig. 3: Single-pore K+ currents as a function of transmembrane field Ez.
Fig. 4: Ion interaction energies and water density profile.
Fig. 5: Cation currents from an NaCl solution and KCl + NaCl mixtures.

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Data availability

The data sets generated and analysed in this study are available from the corresponding author upon reasonable request.

References

  1. Nam, S.-W. et al. Ionic field effect transistors with sub-10 nm multiple nanopores. Nano Lett. 9, 2044–2048 (2009).

    Article  CAS  Google Scholar 

  2. Joshi, P. et al. Field effect modulation of ionic conductance of cylindrical silicon-on-insulator nanopore array. J. Appl. Phys. 107, 054701 (2010).

    Article  Google Scholar 

  3. Humplik, T. et al. Nanostructured materials for water desalination. Nanotechnology. 22, 292001 (2011).

    Article  CAS  Google Scholar 

  4. Höltzel, A. & Tallarek, U. Ionic conductance of nanopores in microscale analysis systems: where microfluidics meets nanofluidics. J. Sep. Sci. 30, 1398–1419 (2007).

    Article  Google Scholar 

  5. Schoch, R. B., Han, J. & Renaud, P. Transport phenomena in nanofluidics. Rev. Mod. Phys. 80, 839–883 (2008).

    Article  CAS  Google Scholar 

  6. Duan, R., Xia, F. & Jiang, L. Constructing tunable nanopores and their application in drug delivery. ACS Nano 7, 8344–8349 (2013).

    Article  CAS  Google Scholar 

  7. Catterall, W. A. Structure and function of voltage-gated ion channels. Annu. Rev. Biochem. 64, 493–531 (1995).

    Article  CAS  Google Scholar 

  8. Tasneem, A. et al. Identification of the prokaryotic ligand-gated ion channels and their implications for the mechanisms and origins of animal Cys-loop ion channels. Genome Biol. 6, R4–R4 (2005).

    Article  Google Scholar 

  9. Chowdhury, S., Jarecki, B. W. & Chanda, B. A molecular framework for temperature-dependent gating of ion channels. Cell 158, 1148–1158 (2014).

    Article  CAS  Google Scholar 

  10. Martinac, B. Mechanosensitive ion channels: molecules of mechanotransduction. J. Cell Sci. 117, 2449–2460 (2004).

    Article  CAS  Google Scholar 

  11. Kasianowicz, J. J. et al. Characterization of individual polynucleotide molecules using a membrane channel. Proc. Natl Acad. Sci. USA 93, 13770–13773 (1996).

    Article  CAS  Google Scholar 

  12. Dekker, C. Solid-state nanopores. Nat. Nanotech. 2, 209–215 (2007).

    Article  CAS  Google Scholar 

  13. Wang, L. et al. Fundamental transport mechanisms, fabrication and potential applications of nanoporous atomically thin membranes. Nat. Nanotech. 12, 509–522 (2017).

    Article  CAS  Google Scholar 

  14. Pedersen, C. J. Cyclic polyethers and their complexes with metal salts. J. Am. Chem. Soc. 89, 2495–2496 (1967).

    Article  CAS  Google Scholar 

  15. Glendening, E. D., Feller, D. & Thompson, M. A. An ab initio investigation of the structure and alkali metal cation selectivity of 18-crown-6. J. Am. Chem. Soc. 116, 10657–10669 (1994).

    Article  CAS  Google Scholar 

  16. Izatt, R. M. et al. Calorimetric titration study of the interaction of several uni- and bivalent cations with 15-crown-5, 18-crown-6, and two isomers of dicyclohexo-18-crown-6 in aqueous solution at 25 °C and μ = 0.1. J. Am. Chem. Soc. 98, 7620–7626 (1976).

    Article  CAS  Google Scholar 

  17. Inokuchi, Y. et al. Ion selectivity of crown ethers investigated by UV and IR spectroscopy in a cold ion trap. J. Phys. Chem. A 116, 4057–4068 (2012).

    Article  CAS  Google Scholar 

  18. Gokel, G. W., Leevy, W. M. & Weber, M. E. Crown ethers: sensors for ions and molecular scaffolds for materials and biological models. Chem. Rev. 104, 2723–2750 (2004).

    Article  CAS  Google Scholar 

  19. Guo, J. et al. Crown ethers in graphene. Nat. Commun. 5, 5389 (2014).

    Article  CAS  Google Scholar 

  20. Gaikwad, A. G., Noguchi, H. & Yoshio, M. Stability constants of crown ether complexes with aqueous hydronium ion. Anal. Sci. 3, 217–220 (1987).

    Article  CAS  Google Scholar 

  21. Smolyanitsky, A., Paulechka, E. & Kroenlein, K. Aqueous ion trapping and transport in graphene-embedded 18-crown-6 ether pores. ACS Nano 12, 6677–6684 (2018).

    Article  CAS  Google Scholar 

  22. Fasolino, A., Los, J. H. & Katsnelson, M. I. Intrinsic ripples in graphene. Nat. Mater. 6, 858–861 (2007).

    Article  CAS  Google Scholar 

  23. Gordillo, M. C. & Martí, J. Structure of water adsorbed on a single graphene sheet. Phys. Rev. B 78, 075432 (2008).

    Article  Google Scholar 

  24. Nelson, P. H. A permeation theory for single-file ion channels: one- and two-step models. J. Chem. Phys. 134, 165102 (2011).

    Article  Google Scholar 

  25. Rawicz, W. et al. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys. J. 79, 328–339 (2000).

    Article  CAS  Google Scholar 

  26. Androulidakis, C. et al. Experimentally derived axial stress–strain relations for two-dimensional materials such as monolayer graphene. Carbon 81, 322–328 (2015).

    Article  CAS  Google Scholar 

  27. Horn, H. W. et al. Development of an improved four-site water model for biomolecular simulations: TIP4P-Ew. J. Chem. Phys. 120, 9665–9678 (2004).

    Article  CAS  Google Scholar 

  28. Noskov, S. Y., Bernèche, S. & Roux, B. Control of ion selectivity in potassium channels by electrostatic and dynamic properties of carbonyl ligands. Nature 431, 830 (2004).

    Article  CAS  Google Scholar 

  29. Moreno, C. et al. Bottom-up synthesis of multifunctional nanoporous graphene. Science 360, 199–203 (2018).

    Article  CAS  Google Scholar 

  30. Goldsche, M. et al. Tailoring mechanically tunable strain fields in graphene. Nano Lett. 18, 1707–1713 (2018).

    Article  CAS  Google Scholar 

  31. Cretu, O. et al. Structure and local chemical properties of boron-terminated tetravacancies in hexagonal boron nitride. Phys. Rev. Lett. 114, 075502 (2015).

    Article  Google Scholar 

  32. Feng, J. et al. Electrochemical reaction in single layer MoS2: nanopores opened atom by atom. Nano Lett. 15, 3431–3438 (2015).

    Article  CAS  Google Scholar 

  33. Thiruraman, J. P. et al. Angstrom-size defect creation and ionic transport through pores in single-layer MoS2. Nano Lett. 18, 1651–1659 (2018).

    Article  CAS  Google Scholar 

  34. Smolyanitsky, A. Molecular dynamics simulation of thermal ripples in graphene with bond-order-informed harmonic constraints. Nanotechnology 25, 485701 (2014).

    Article  Google Scholar 

  35. Paulechka, E. et al. Nucleobase-functionalized graphene nanoribbons for accurate high-speed DNA sequencing. Nanoscale 8, 1861–1867 (2016).

    Article  CAS  Google Scholar 

  36. Jorgensen, W. L., Maxwell, D. S. & Tirado-Rives, J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118, 11225–11236 (1996).

    Article  CAS  Google Scholar 

  37. Perdew, J. P., Burke, K. & Ernzerhof, M. Generalized gradient approximation made simple. Phys. Rev. Lett. 77, 3865–3868 (1996).

    Article  CAS  Google Scholar 

  38. Hartwigsen, C., Goedecker, S. & Hutter, J. Relativistic separable dual-space Gaussian pseudopotentials from H to Rn. Phys. Rev. B 58, 3641–3662 (1998).

    Article  CAS  Google Scholar 

  39. VandeVondele, J. & Hutter, J. Gaussian basis sets for accurate calculations on molecular systems in gas and condensed phases. J. Chem. Phys. 127, 114105 (2007).

    Article  Google Scholar 

  40. Grimme, S. et al. A consistent and accurate ab initio parametrization of density functional dispersion correction (DFT-D) for the 94 elements H-Pu. J. Chem. Phys. 132, 154104 (2010).

    Article  Google Scholar 

  41. Hutter, J. et al. cp2k: atomistic simulations of condensed matter systems. WIRES Comput. Mol. Sci. 4, 15–25 (2014).

    Article  CAS  Google Scholar 

  42. Van Der Spoel, D. et al. Gromacs: fast, flexible, and free. J. Comput. Chem. 26, 1701–1718 (2005).

    Article  Google Scholar 

  43. Hess, B. et al. Gromacs 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory. Comput. 4, 435–447 (2008).

    Article  CAS  Google Scholar 

  44. Hub, J. S., de Groot, B. L. & van der Spoel, D. g_wham—a free weighted histogram analysis implementation including robust error and autocorrelation estimates. J. Chem. Theory Comput. 6, 3713–3720 (2010).

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank M. Zwolak for suggesting lattice strain as a potential way of controlling permeation, E. Paulechka for enlightening discussions about defects and competitive permeation, and A. Bazyleva for discussions about the chemistry of crown ethers. This research was performed while A. Fang held a National Research Council Postdoctoral Research Associateship at the National Institute of Standards and Technology. The authors acknowledge support from the Materials Genome Initiative.

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Authors and Affiliations

  1. Applied Chemicals and Materials Division, National Institute of Standards and Technology, Boulder, CO, USA

    A. Fang, K. Kroenlein, D. Riccardi & A. Smolyanitsky

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  1. A. Fang
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  2. K. Kroenlein
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  3. D. Riccardi
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Contributions

A.S. designed and performed the simulations, and developed the theory. A.F. and K.K. devised and implemented analysis software. A.F. and D.R. contributed to the theory. All authors discussed the results, wrote the manuscript and contributed to revisions.

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Correspondence to A. Smolyanitsky.

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Supplementary Information

Supplementary Sections 1–4, Supplementary Figures 1–6, Supplementary References 1–6

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Fang, A., Kroenlein, K., Riccardi, D. et al. Highly mechanosensitive ion channels from graphene-embedded crown ethers. Nature Mater 18, 76–81 (2019). https://doi.org/10.1038/s41563-018-0220-4

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