Cracking donuts and sorting lipids: Geometry controls archaeal membrane stability and lipid organization

TL;DR

This study uses molecular dynamics simulations to explore how the unique lipid compositions of archaeal membranes influence their stability and organization under various curvatures, revealing curvature-dependent lipid behaviors.

Contribution

It systematically investigates the physical principles of archaeal membrane stability and lipid organization across different curvatures using coarse-grained simulations.

Findings

Soft bilayer membranes can sustain all induced curvatures.

Rigid bolalipid monolayers may rupture or change shape under certain curvatures.

U-shaped bolalipids and bilayer lipids accumulate in high mean curvature regions.

Abstract

Cells are defined by lipid membranes that differ in their structure across the tree of life. While the membranes of most bacteria and eukaryotes consist of single-headed bilayer lipids, the membranes of archaea are composed of mixtures of single-headed bilayer lipids and double-headed bolalipids. Archaeal bolalipids can adopt straight or u-shaped conformations, enabling them - together with bilayer lipids - to control whether membranes form bilayer or monolayer structures. Yet, the physical principles governing archaeal membranes remain largely unexplored, especially how membrane structure couples to externally imposed curvature during membrane remodeling. Here, we perform coarse-grained molecular dynamics simulations of toroidal vesicles to systematically probe the effects of all relevant combinations of mean and Gaussian curvatures on shape stability and lipid organization. We find that soft bilayer membranes can sustain all curvatures induced, whereas rigid bolalipid monolayer membranes either transition to different vesicle shapes or rupture. Bilayer-mimicking u-shaped bolalipids and bilayer lipids are spatially accumulated in regions of high mean membrane curvature independent of Gaussian curvature. Our work identifies curvature-composition coupling as a physical signature of archaeal membrane remodeling.