Artificial Water Channels Enable Fast and Selective Water Permeation Through Water-wire Networks

Woochul Song, Himanshu Joshi, Ratul Chowdhury, Joseph S. Najem, Yue-xiao Shen, Chao Lang, Codey B. Henderson, Yu-Ming Tu, Megan Farell, Megan E. Pitz, Costas D. Maranas, Paul S. Cremer, Robert J. Hickey, Stephen A. Sarles, Jun-li Hou, Aleksei Aksimentiev, and Manish Kumar
Nature Nanotechnology. 15, 73-79 (2020)
DOI:https://doi.org/10.1038/s41565-019-0586-8  BibTex

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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. 

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 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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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.

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.

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.

(Left) 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. (Right) a close-up view of the  transmembrane water diffusion in the cetral constriction region. Water, Na+, and Cl− atoms are shown in red and white, magenta, and yellow, respectively.