Signatures of glassy dynamics in highly ordered lipid bilayers with emergence of soft dynamic channels

Abstract

Over the last few decades, extensive investigations on spatial and dynamic heterogeneity have been performed on carefully reconstituted biological lipid membranes. Characterizing the molecular features in heterogeneous membranes is extremely challenging due to the experimentally inaccessible time- and length-scales of these emergent systems. In this context, simulations can provide important insights into molecular-level interactions leading to membrane heterogeneity and associated functions. To that end, we use the non-affine displacement (NAD) framework (a concept borrowed from the physics of granular materials) to faithfully capture molecular-scale local membrane order in simulated heterogeneous bilayers. In our latest application of NAD, we investigate the temperature-dependent spatial and temporal organization on microsecond trajectories of liquid-ordered bilayer systems at all-atom resolution (DPPC/DOPC/CHOL: 0.55:0.15:0.30; 40 × 40 nm2 with a total of 5600 lipids and 2 × 106 atoms). Lateral organization in these large bilayer patches shows noticeable dynamic heterogeneity despite their liquid-ordered nature. Moreover, our NAD analyses reveal soft fluid channels within the tightly packed membrane reminiscent of the classical two-component Kob–Andersen glass-forming binary mixture. Hence, we characterized these systems using classical glass physics markers for dynamic heterogeneities such as overlap, four-point susceptibility, Van Hove, and intermediate scattering functions to quantify the multiple time scales underlying the lipid dynamics. Our analyses reveal that highly ordered membrane systems can have glass-like dynamics with distinct soft fluid channels inside them. Biologically, these dynamic channels could act as conduits for facilitating molecular encounters for biological functions even in highly ordered phases such as lipid nanodomains and rafts.