Research ArticlePHYSICS

Oriented chiral water wires in artificial transmembrane channels

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Science Advances  23 Mar 2018:
Vol. 4, no. 3, eaao5603
DOI: 10.1126/sciadv.aao5603
  • Fig. 1 I-quartet artificial water channels and their chiral isomers packing.

    Top views in stick representation (N, blue; C, gray; O, red; H, white) of the water-confined I-quartet x-ray single-crystal structures of (A) octylureido-ethylimidazole HC8, (B) S-octylureido-ethylimidazole S-HC8, and (C) R-octylureido-ethylimidazole R-HC8 (14). (D) Side view in stick representation of planar arrays of the urea H-bonded ribbons of HC8 showing that oriented water wires form along a 2.6 Å diameter pore of the channel. (E) Tetrameric H-bonded water I-quartet architectures confining dipolar oriented water. (F) Achiral centrosymmetric HC8 I-quartets confining water wires of the opposite dipolar orientations, filling successive channels separated by water-free I-quartets and (G) chiral noncentrosymmetric S-HC8 I-quartets confining oriented water wires with a unique dipolar orientation for total water-filled I-quartet channels.

  • Fig. 2 Incorporation of HC8 I-quartets in 4:1 = PC/PS SLB.

    Experimental QCM-D frequency, ΔF (hertz) and dissipation coefficient, ΔD (−) shifts associated with the SLB formation on silica QCM-D sensors via fusion of SUVs of mixtures of lipids: (A) PC/PS, 4:1 mol/mol, and (B) PC/PS, 4:1 mol/mol + HC8. The two arrows for each panel indicate (i) SUV injection at 4 min and (ii) the washing step with 10 mM phosphate buffer (pH 6.4) after 12 min. Data of the fifth, seventh, and ninth overtones are shown for ΔF (F5, F7, and F9) and ΔD (D5, D7, and D9). SUV concentration was 0.2 mg/ml. Flow rate was kept constant at 100 μl/min.

  • Fig. 3 SFG vibrational spectroscopy.

    SFG spectra of 4:1 = PC/PS SLB (reference), HC8, and S-HC8 I-quartets in 4:1 = PC/PS SLB determined for pure achiral (A) ppp and (B) ssp, as well as pure chiral (C) psp and (D) spp polarization combinations. (E) Highlighted regions describe (a) imidazole groups of the channel perpendicular to the lipid bilayer, (b) water orientated by the headgroup charges, (c) hydrogen bond chain-like channel water molecules, (d) weakly hydrogen-bonded water molecules interacting with the ester carbonyl groups of the lipids or less likely the imidazole carbonyls, and (e) non–hydrogen-bonded OH groups of water in the channel environment.

  • Fig. 4 Molecular dynamics.

    MD simulations of the I-quartets feature well-structured central water wires through these artificial channels depicted in (A). The region considered for analysis is highlighted by a cyan transparent rectangle. (B) Electrostatic potential field across the membrane and water channel region for HC8, S-HC8, and R-HC8 systems. (C) Hydrogen bond energy depicting the stabilization of the two central water channels as compared to bulk water averaged over the 450- to 500-ns time frames. The x axis is the direction perpendicular to the membrane plane. Hydrogen bonds were calculated for the colored water molecules with their surroundings (gray atoms). (D) Distribution of O-H orientation angles (as defined in fig. S9A) for the water molecules within the transmembrane region of HC8, S-HC8, and R-HC8 systems. Only the smallest of both orientation angles is reported. (E) Order parameters for water molecules within the membrane region calculated in the direction normal to the membrane plane.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/4/3/eaao5603/DC1

    fig. S1. Atomic displacement ellipsoid plot of the structure.

    fig. S2. Incorporation of HC8 I-quartets in lipid bilayers determined by QCM-D experiments.

    fig. S3. Formation of a hydration layer between an SLB and a silica substrate.

    fig. S4. Surface area occupied by the single lipid molecule as a function of the hydration layer thickness.

    fig. S5. Top views of water-confining I-quartet channels.

    fig. S6. Difference interference SFG spectra in two polarization combinations.

    fig. S7. FTIR ATR spectrum of dry HC8 powder.

    fig. S8. Number of water molecules and hydrogen bonds formed by water in the membrane region.

    fig. S9. Schematic representation of the O-H orientation angles that were calculated.

    table S1. X-ray data collection and refinement details.

    table S2. Estimate of lipid, HC8, and H2O amounts.

    table S3. Estimate of the area that the single lipid molecule occupies on the available QCM-D sensor surface.

    table S4. Statistics of water molecules within the lipid bilayer region.

    table S5. Statistics of central channel water molecules within the lipid bilayer region.

    note S1. Characterization of SLB by QCM-D.

  • Supplementary Materials

    This PDF file includes:

    • fig. S1. Atomic displacement ellipsoid plot of the structure.
    • fig. S2. Incorporation of HC8 I-quartets in lipid bilayers determined by QCM-D experiments.
    • fig. S3. Formation of a hydration layer between an SLB and a silica substrate.
    • fig. S4. Surface area occupied by the single lipid molecule as a function of the hydration layer thickness.
    • fig. S5. Top views of water-confining I-quartet channels.
    • fig. S6. Difference interference SFG spectra in two polarization combinations.
    • fig. S7. FTIR ATR spectrum of dry HC8 powder.
    • fig. S8. Number of water molecules and hydrogen bonds formed by water in the membrane region.
    • fig. S9. Schematic representation of the O-H orientation angles that were calculated.
    • table S1. X-ray data collection and refinement details.
    • table S2. Estimate of lipid, HC8, and H2O amount.
    • table S3. Estimate of the area that the single lipid molecule occupies on the available QCM-D sensor surface.
    • table S4. Statistics of water molecules within the lipid bilayer region.
    • table S5. Statistics of central channel water molecules within the lipid bilayer region.
    • note S1. Characterization of SLB by QCM-D.

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