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Abstract Cell membranes are composed of both bilayer-supporting and non-bilayer phospholipids, with the latter’s negative intrinsic curvature aiding in membrane trafficking and the dynamics of membrane proteins. Phospholipid metabolism has long been recognized to maintain membrane fluidity, but whether it also acts to maintain the function of high-curvature lipids is not resolved. Here, we find that cells grown under hydrostatic pressure – used to artificially reduce lipid curvature – maintain lipidome curvature through metabolic acclimation. We first observed that manipulation of the lipidome curvature via the phosphatidylethanolamine (PE) to phosphatidylcholine (PC) ratio affects high-pressure growth and viability of yeast independently of membrane fluidity. In wild-type cells, X-ray scattering measurements revealed an increased propensity for lipid extracts to form non-lamellar phases after extended pressure incubations. Unexpectedly, this change in phase behavior was not due to increased levels of PE, but of phosphatidylinositol (PI), the only major phospholipid class whose curvature had not been previously characterized. We found that PI is a non-bilayer lipid, with a negative curvature intermediate to that of PE and PC. Accounting for PI, mean lipidome curvature was defended in response to pressure by two distantly related yeasts. Lipidome curvature also responded to pressure in a human cancer cell line through ether phospholipid metabolism and chain remodeling, but not in bacterial cells. These findings indicate that eukaryotic phospholipid metabolism uses diverse mechanisms to maintain curvature frustration in cell membranes. 

Hydrostatic pressure increases with depth in the ocean, but little is known about the molecular bases of biological pressure tolerance. We describe a mode of pressure adaptation in comb jellies (ctenophores) that also constrains these animals’ depth range. Structural analysis of deep-sea ctenophore lipids shows that they form a nonbilayer phase at pressures under which the phase is not typically stable. Lipidomics and all-atom simulations identified phospholipids with strong negative spontaneous curvature, including plasmalogens, as a hallmark of deep-adapted membranes that causes this phase behavior. Synthesis of plasmalogens enhanced pressure tolerance inEscherichia coli, whereas low-curvature lipids had the opposite effect. Imaging of ctenophore tissues indicated that the disintegration of deep-sea animals when decompressed could be driven by a phase transition in their phospholipid membranes. 

ABSTRACT Animals are known to regulate the composition of their cell membranes to maintain key biophysical properties in response to changes in temperature. For deep-sea marine organisms, high hydrostatic pressure represents an additional, yet much more poorly understood, perturbant of cell membrane structure. Previous studies in fish and marine microbes have reported correlations with temperature and depth of membrane-fluidizing lipid components, such as polyunsaturated fatty acids. Because little has been done to isolate the separate effects of temperature and pressure on the lipid pool, it is still not understood whether these two environmental factors elicit independent or overlapping biochemical adaptive responses. Here, we use the taxonomic and habitat diversity of the phylum Ctenophora to test whether distinct low-temperature and high-pressure signatures can be detected in fatty acid profiles. We measured the fatty acid composition of 105 individual ctenophores, representing 21 species, from deep and shallow Arctic, temperate, and tropical sampling locales (sea surface temperature, −2° to 28°C). In tropical and temperate regions, remotely operated submersibles (ROVs) enabled sampling down to 4000 m. We found that among specimens with body temperatures 7.5°C or colder, depth predicted fatty acid unsaturation levels. In contrast, in the upper 200 m of the water column, temperature predicted fatty acid chain lengths. Taken together, our findings suggest that lipid metabolism may be specialized with respect to multiple physical variables in diverse marine environments. Largely distinct modes of adaptation to depth and cold imply that polar marine invertebrates may not find a ready refugium from climate change in the deep.