Thermodynamics and Kinetics of the Early Steps of Solid-State Nucleation in the Fluid Lipid Bilayer

Abstract

Temperature-scanning (10−70 °C) calorimetric, densitometric, and acoustic measurements have been performed in aqueous dispersions of dipalmitoylphosphatidylcholine multilamellar vesicles. In the biologically relevant liquid-crystalline state close to the chain freezing point (within 42−50 °C, in our case), the measured quantities display anomalous deviations from the “ideal” shape of their temperature dependence curves. The deviations indicate the early steps of gel-state nucleation within the stable liquid-crystalline state (Frenkel's heterophase fluctuations). An earlier proposed kinetic model of nucleation (Kharakoz et al. J. Phys. Chem. 1993, 97, 9844−9851) has been refined to achieve more clear physical substantiation. When the deviations are analyzed through the refined model, both the thermodynamic and kinetic characteristics of nucleation are determined. The fluid−solid interface line tension energy is about 0.7 kT per boundary lipid molecule. The tension is strong enough for the phase transition to be first-order and, at the same time, weak enough to allow extensive heterophase fluctuations. The speed of new-phase-front propagation near the transition temperature is virtually proportional to the difference between the current temperature and transition temperature, the proportionality coefficient being 0.2 cm s-1 K-1 (estimated from ultrasonic relaxation data). The experimental data and the nucleation model are consistent with literature data on the anomalous “critical-like” behavior of lipid membranes near the main transition (bending rigidity drop, anomalous swelling, slowing relaxation processes, etc.). Thus, we show that most of the anomalies can be rationalized in terms of the weak first-order transition mechanism without a hypothesis on the proximity of bilayer to a critical state.