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The response of biomembranes to aqueous-phase separation and to the resulting water-in-water droplets has been recently studied on the micrometer scale using optical microscopy and elasticity theory. When such a droplet adheres to the membrane, it forms a contact area that is bounded by a contact line. For a micrometer-sized droplet, the line tension associated with this contact line can usually be ignored compared with the surface tensions. However, for a small nanoscopic droplet, this line tension is expected to affect the membrane-droplet morphology. Here, we use molecular simulations to study nanodroplets at membranes and to gain insight into these line tension effects. The latter effects are shown to depend strongly on another key parameter, the mechanical tension experienced by the membrane. For a large membrane tension, a droplet adhering to the membrane is only partially engulfed by the membrane, and the membrane-droplet system exhibits an axisymmetric morphology. A reduction of the membrane tension leads to an increase in the contact area and a decrease in the interfacial area of the droplet, initially retaining its axisymmetric shape, which implies a circular contact line and a circular membrane neck. However, when the tension falls below a certain threshold value, the system undergoes a morphological transition toward a non-axisymmetric morphology with a non-circular membrane neck. This morphology persists until the nanodroplet is completely engulfed by the membrane and the membrane neck has closed into a tight-lipped shape. The latter morphology is caused by a negative line tension, which is shown to be a robust feature of membrane-droplet systems. A closed membrane neck with a tight-lipped shape suppresses both thermally activated and protein-induced scission of the neck, implying a reduction in the cellular uptake of nanodroplets by pinocytosis and fluid-phase endocytosis. Furthermore, based on our results, we can also draw important conclusions about the time-dependent processes corresponding to the surface nucleation and growth of nanodroplets at membranes.

Nanodroplets at Membranes Create Tight-Lipped Membrane Necks via Negative Line Tension