Oriented chiral water wires in artificial transmembrane channels
Open Access
- 2 March 2018
- journal article
- research article
- Published by American Association for the Advancement of Science (AAAS) in Science Advances
- Vol. 4 (3), eaao5603
- https://doi.org/10.1126/sciadv.aao5603
Abstract
Aquaporins (AQPs) feature highly selective water transport through cell membranes, where the dipolar orientation of structured water wires spanning the AQP pore is of considerable importance for the selective translocation of water over ions. We recently discovered that water permeability through artificial water channels formed by stacked imidazole I-quartet superstructures increases when the channel water molecules are highly organized. Correlating water structure with molecular transport is essential for understanding the underlying mechanisms of (fast) water translocation and channel selectivity. Chirality adds another factor enabling unique dipolar oriented water structures. We show that water molecules exhibit a dipolar oriented wire structure within chiral I-quartet water channels both in the solid state and embedded in supported lipid bilayer membranes (SLBs). X-ray single-crystal structures show that crystallographic water wires exhibit dipolar orientation, which is unique for chiral I-quartets. The integration of I-quartets into SLBs was monitored with a quartz crystal microbalance with dissipation, quantizing the amount of channel water molecules. Nonlinear sum-frequency generation vibrational spectroscopy demonstrates the first experimental observation of dipolar oriented water structures within artificial water channels inserted in bilayer membranes. Confirmation of the ordered confined water is obtained via molecular simulations, which provide quantitative measures of hydrogen bond strength, connectivity, and the stability of their dipolar alignment in a membrane environment. Together, uncovering the interplay between the dipolar aligned water structure and water transport through the self-assembled I-quartets is critical to understanding the behavior of natural membrane channels and will accelerate the systematic discovery for developing artificial water channels for water desalting.Keywords
Funding Information
- National Science Foundation (CHE-1151079, DMR-1120296 and ECCS-0335765)
- U.S. Department of Energy (DE-FG02- 09ER16005)
- Agence Nationale de la Recherche (ANR-15-CE29-0009 DYNAFUN)
- Agence Nationale de la Recherche (ANR-10-LABX-05-01)
- Agence Nationale de la Recherche (ANR-11-LABX-0011-01 and ANR-11-EQPX-0008)
- GENCI-CINES (2016-072292)
This publication has 48 references indexed in Scilit:
- Artificial Water ChannelsAngewandte Chemie-International Edition, 2012
- Imidazole‐Quartet Water and Proton Dipolar ChannelsAngewandte Chemie-International Edition, 2011
- Insight into the Mechanism of the Influenza A Proton Channel from a Structure in a Lipid BilayerScience, 2010
- Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid TypesThe Journal of Physical Chemistry B, 2010
- CHARMM general force field: A force field for drug‐like molecules compatible with the CHARMM all‐atom additive biological force fieldsJournal of Computational Chemistry, 2009
- Dynamic hybrid materials for constitutional self-instructed membranesProceedings of the National Academy of Sciences of the United States of America, 2009
- Ion‐Conduction Pathways in Self‐Organised Ureidoarene–Heteropolysiloxane Hybrid MembranesChemistry – A European Journal, 2008
- GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular SimulationJournal of Chemical Theory and Computation, 2008
- Comparison of simple potential functions for simulating liquid waterThe Journal of Chemical Physics, 1983
- Verwendung von Schwingquarzen zur Wägung dünner Schichten und zur MikrowägungThe European Physical Journal A, 1959