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

Nature Nanotechnology volume 15, pages 73–79 (2020)Cite this article

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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

Author notes

  1. Woochul Song & Yu-Ming Tu

    Present address: Department of Chemical Engineering, The University of Texas at Austin, Austin, TX, USA

  2. Joseph S. Najem

    Present address: Department of Mechanical Engineering, The Pennsylvania State University, UniversityPark, PA, USA

  3. Manish Kumar

    Present address: Department of Civil, Architectural and Environmental Engineering, The University of Texas at Austin, Austin, TX, USA

Authors and Affiliations

  1. Department of Chemical Engineering, The Pennsylvania State University, University Park, PA, USA

    Woochul Song, Ratul Chowdhury, Chao Lang, Yu-Ming Tu, Megan Farell, Costas D. Maranas & Manish Kumar

  2. Department of Physics, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    Himanshu Joshi & Aleksei Aksimentiev

  3. Department of Mechanical, Aerospace, and Biomedical Engineering, The University of Tennessee, Knoxville, TN, USA

    Joseph S. Najem, Megan E. Pitz & Stephen A. Sarles

  4. Department of Civil, Environmental, & Construction Engineering, Texas Tech University, Lubbock, TX, USA

    Yue-xiao Shen

  5. Department of Chemistry, The Pennsylvania State University, University Park, PA, USA

    Codey B. Henderson & Paul S. Cremer

  6. Department of Materials Science and Engineering, The Pennsylvania State University, University Park, PA, USA

    Robert J. Hickey

  7. Department of Chemistry, Fudan University, Shanghai, China

    Jun-li Hou

  8. Department of Biomedical Engineering, The Pennsylvania State University, University Park, PA, USA

    Manish Kumar

  9. Department of Civil and Environmental Engineering, The Pennsylvania State University, University Park, PA, USA

    Manish Kumar

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Contributions

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.

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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). https://doi.org/10.1038/s41565-019-0586-8

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