Biophysical adaptations of cell membranes to hydrostatic pressure: From deep-sea marine invertebrates to model microorganisms.

Abstract

Life in the deep ocean and continental subsurface is estimated to make up more than half of all biomass on the planet, and must withstand the crushing pressures up to 1000 times that at the surface. Lipid membranes encapsulating cells and organelles are sensitive to their physical environments, especially pressure. To understand the mechanisms by which membrane structure adapts to high pressure environments, we have employed lipidomic and structural analyses of extracted membranes from pressure-adapted deep-sea invertebrates (ctenophores), allowing us to identify key chemical and physical signatures of depth adaptation. To validate these findings, we employed yeast and bacterial model organisms, engineered with tuned lipid biosynthesis pathways, and grown under varying pressures in the lab. This multi-scale, comparative approach has revealed lipid properties such as headgroup stoichiometry, ether vs. ester chain linkages, chain unsaturation, and chain length length provide biophysical advantages to buffer against physiologically-incompatible membrane states and preserve membrane plasticity at high pressure. Understanding lipid adaptations to pressure could allow for the identification of the mechanisms by which cells sense the global membrane environment and thereby facilitate homeoviscous, homeophasic, and homeocurvature responses.