Artificial water channels enable fast and selective water permeation through water-wire networks

Abstract

Artificial water channels are synthetic molecules that aim to mimic the structural and functional features of biological water channels (aquaporins). Here we report on a cluster-forming organic nanoarchitecture, peptide-appended hybrid[4]arene (PAH[4]), as a new class of artificial water channels. Fluorescence experiments and simulations demonstrated that PAH[4]s can form, through lateral diffusion, clusters in lipid membranes that provide synergistic membrane-spanning paths for a rapid and selective water permeation through water-wire networks. Quantitative transport studies revealed that PAH[4]s can transport >109 water molecules per second per molecule, which is comparable to aquaporin water channels. The performance of these channels exceeds the upper bound limit of current desalination membranes by a factor of ~104, as illustrated by the water/NaCl permeability–selectivity trade-off curve. PAH[4]’s unique properties of a high water/solute permselectivity via cooperative water-wire formation could usher in an alternative design paradigm for permeable membrane materials in separations, energy production and barrier applications.

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Fig. 1: Cluster-forming PAH[4] channels.
Fig. 2: Measurements of water and ion conduction rates through PAH[4]s.
Fig. 3: Intrinsic water/NaCl selectivity (Pw/Ps) versus Pw of PAH[4]-, CNTP- and RsAqpZ-based biomimetic membranes.
Fig. 4: MD simulations of a 22-mer cluster of PAH[4] channels and of an AQP1 tetramer embedded in a lipid bilayer membrane.

Data availability

The datasets that support the finding of this study are available in ScholarSphere repository with the identifier(s) (https://doi.org/10.26207/ykbm-r806).

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Acknowledgements

The authors acknowledge financial support from the National Science Foundation (NSF) CAREER grant (CBET-1552571) to M.K. for this work. A.A. and H.J. acknowledge support from the National Science Foundation under grant DMR-1827346 and the National Institutes of Health under grant P41-GM104601. Additional support was provided by NSF grant CBET-1804836 to M.K. Supercomputer time was provided through XSEDE Allocation Grant no. MCA05S028 and the Blue Waters petascale supercomputer system at the University of Illinois at Urbana−Champaign. H.J. acknowledges the Government of India for the DST-Overseas Visiting Fellowship in Nano Science and Technology.

Author information

W.S., H.J., A.A. and M.K. conceived and designed the research. W.S. and Y.-x.S. performed the experiments with the assistance of J.S.N., C.L., C.B.H., Y.-M.T., M.F., M.E.P. and J.-l.H. in specialized analytical tools. H.J. and R.C. performed the computer simulations. W.S., H.J., R.C., C.D.M., P.S.C., R.J.H., S.A.S., J.-l.H., A.A. and M.K. analysed the data. W.S., H.J., R.C., A.A. and M.K. co-wrote the paper.

Correspondence to Manish Kumar.

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The authors declare no competing interests.

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Peer review information Nature Nanotechnology thanks Andreas Horner, Meni Wanunu and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary methods and discussions, Figs. 1–30 and Video captions 1–5.

Supplementary Video 1

Molecular Model of PAH[4] channels. The central constriction of the hybrid[4]arene macromolecules and the nearest phenylalanine moieties are coloured in green. The remaining phenylalanine moieties are coloured in purple.

Supplementary Video 2

Top and cross-sectional views of a MD system featuring a 22-mer cluster (green and purple) of PAH[4] channels embedded in a POPC lipid bilayer membrane (turquoise). For visual clarity, water and ions are not shown.

Supplementary Video 3

A 100 ns long MD simulation trajectory of 22-mer PAH[4] cluster with the ±1 V externally applied bias across the simulation box. In these applied electric field MD simulations, the cluster was harmonically restrained to its equilibrium configuration obtained at the end of a 400 ns-long MD simulation. Lipid bilayer membrane is shown in turquoise, whereas the PAH[4] units are shown in purple and green. Na+ and Cl ions are shown in yellow and blue colour with vdW representation. Water is not shown for clarity.

Supplementary Video 4

MD system featuring a 22-mer cluster (green and purple) of PAH[4] channels embedded in a POPC lipid bilayer membrane (turquoise), showing cooperative water wire network formation spanning the membrane. Water, Na+, and Cl atoms are shown in red and white, magenta, and yellow, respectively.

Supplementary Video 5

Cut-away view of a simulation system illustrating the cooperative water permeation through a water wire network. The 22-mer PAH[4] cluster, POPC lipid membrane, and water molecules are shown in green and purple, turquoise, and red and white, respectively.

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Song, W., Joshi, H., Chowdhury, R. et al. Artificial water channels enable fast and selective water permeation through water-wire networks. Nat. Nanotechnol. 15, 73–79 (2020) doi:10.1038/s41565-019-0586-8

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