The Biophysical Tight Rope of Cell Membranes: Lessons Learned from Extreme Lipidome Adaptation in The Deep Ocean

Lipid bilayers are the universal structure of all cell membranes and depend on the propensity of specific phospholipid classes to form fluid lamellar phases. However, no biological membranes are composed entirely of bilayer-forming lipids, instead balancing species with low and high intrinsic curvatures. I will describe how this dynamic plays out in organisms that have adapted to hydrostatic pressure, which increases by 1 atmosphere every 10m in the water column. Small angle x-ray scattering of lipid suspensions from deep sea comb jellies (ctenophores) collected at depths up to 4km revealed a remarkable ability to access non-lamellar lipid phases, which are inhibited by pressure. Lipidomic analysis across a wide range of species identified phospholipids with large, negative spontaneous curvature as a depth-specific adaptation across the phylum. High pressure molecular dynamics of lipidome-derived bilayers supports this adaptation. Using engineered bacterial strains, we found that lipid spontaneous curvature can modulate pressure tolerance. Based on these results, we propose a homeocurvature adaptation model for cell membranes, in which the effect of pressure on lipid shape can contribute to both fitness and specialization in the deep oceans.