Long-term memory in lipid assemblies: Rate-independent hysteresis in the ripple-to-liquid-disordered transition of sphingomyelin bilayers

Sphingomyelin (SM) is the most abundant sphingolipid in mammalian cells. It contains a phosphorylcholine headgroup, which makes SM an analog of the (glycerol-containing) phosphatidylcholines. Palmitoyl (C16:0) SM bilayers in excess water exhibit a thermotropic transition from the ripple to the fluid phase centered at ≈41 °C. In phosphatidylcholines, as in most phospholipids, the ripple-to-fluid transition is fully reversible and virtually free of hysteresis. In this paper, however, the corresponding transition was assessed in aqueous SM by infrared (IR) spectroscopy, a technique detecting molecular vibrations. Vibrational spectra as a function of temperature revealed thermotropic phase transitions. When the samples were successively heated up and cooled down, a clear hysteresis was detected. The cooling transition started at the same temperature as the heating one, but the end-point, in terms of IR band position, was clearly different. Hysteresis was particularly visible in the shift of the IR Amide I band, associated with the lipid polar headgroup, and it was rate-independent, within a wide range of heating/cooling rates (from 5.5 °C/min to less than 0.05 °C/min). Atomistic computer simulations of the molecular dynamics provided information consistent with the IR data. In addition, it showed that the in-plane arrangement of SM bilayers displays a significant amount of hexatic order, and that the hexatic order parameter, reflecting primarily polar headgroup ordering, exhibited the same kind of hysteresis described by IR. Rate-independent hysteresis allows the development of durable memories; therefore, the observations in this paper could lead to novel applications of lipid assemblies.