Energetics of water permeation through fullerene membrane

Abstract

Lipid bilayer membranes are important as fundamental structures in biology and possess characteristic water-permeability, stability, and mechanical properties. Water permeation through a lipid bilayer membrane occurs readily, and more readily at higher temperature, which is largely due to an enthalpy cost of the liquid-to-gas phase transition of water. A fullerene bilayer membrane formed by dissolution of a water-soluble fullerene, Ph(5)C(60)K, has now been shown to possess properties entirely different from those of the lipid membranes. The fullerene membrane is several orders of magnitude less permeable to water than a lipid membrane, and the permeability decreases at higher temperature. Water permeation is burdened by a very large entropy loss and may be favored slightly by an enthalpy gain, which is contrary to the energetics observed for the lipid membrane. We ascribe this energetics to favorable interactions of water molecules to the surface of the fullerene molecules as they pass through the clefts of the rigid fullerene bilayer. The findings provide possibilities of membrane design in science and technology.

Fig. 1.

Water-soluble fullerene Ph₅C₆₀K.

Fig. 2.

Radius of fullerene vesicles examined in the NMR study from 10°C to 80°C. Apparent hydrodynamic radius (R_h) from the dynamic light scattering study of vesicles of 1.75 mM Ph₅C₆₀K in water containing 1.00 mM MnCl₂. The R_h values were used for the calculation of the permeability coefficients at each temperature.

Fig. 3.

Water permeability of the fullerene membrane showing unusual temperature dependence. Experimental data are plotted with error bars showing the SEM of six runs. Analysis with an Eyring plot (Fig. 5) afforded the thermodynamic parameters of ΔH^‡ = 2.88 kJ/mol and ΔS^‡ = −1.65 × 10² J/mol·K (10–30°C; blue) and ΔH^‡ = −37.5 kJ/mol and ΔS^‡ = −2.93 × 10² J/mol·K (50–80°C; red), respectively.

Fig. 4.

Temperature dependence of water permeability. The sample was heated and cooled over 2 h for each direction, and the cycle was performed three times through runs 1–6. Arrows indicate the direction of the temperature change. Raw data are shown in SI Table 1.

Fig. 5.

The Eyring plot [ln(P/T) vs. 1/T] of the permeability coefficients. Average data of warming/cooling cycles are plotted in red with error bars showing the SEM of six runs (Table 1). The lines were obtained by least-squares fitting using Eq. 2. The activation enthalpy (ΔH^‡) and entropy (ΔS^‡) were determined to be 2.88 kJ/mol and −1.65 × 10² J/mol·K for low temperature (10–30°C; shown in blue) and −37.5 kJ/mol and −2.93 × 10² J/mol·K for high temperature (50–80°C; shown in red), respectively.

Fig. 6.

Thermodynamics and schematic views of water permeation through fullerene and lipid bilayers. The light-blue box represents the bilayer as separated from bulk water. (a) Water permeation through the fullerene bilayer at 10–30°C and 50–80°C determined by the NMR method. (b) Water permeation through the phosphatidylcholine bilayer determined by the same method. (c) Schematic view of a Ph₅C₆₀ anion bilayer, with which water molecules (red) interact and through which they permeate. Fullerene is green, and its anionic moiety is blue. (d) Schematic view of lipid bilayer, through which water molecules permeate without much interaction with the hydrocarbon chains. Water molecules pass through the clefts formed by conformational change and by lateral motion of the lipid molecules (2). Lipid is green, and its polar head is blue.