Homeocurvature adaptation of phospholipids to pressure in deep-sea invertebrates

Author:

Winnikoff Jacob R.1234ORCID,Milshteyn Daniel1ORCID,Vargas-Urbano Sasiri J.5ORCID,Pedraza-Joya Miguel A.5ORCID,Armando Aaron M.6ORCID,Quehenberger Oswald6ORCID,Sodt Alexander7ORCID,Gillilan Richard E.8ORCID,Dennis Edward A.16ORCID,Lyman Edward5ORCID,Haddock Steven H. D.34ORCID,Budin Itay1ORCID

Affiliation:

1. Department of Chemistry and Biochemistry, University of California San Diego, La Jolla, CA 92093, USA.

2. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.

3. Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039, USA.

4. Department of Ecology and Evolutionary Biology, University of California Santa Cruz, Santa Cruz, CA 95064, USA.

5. Department of Physics and Astronomy, University of Delaware, Newark, DE 19716, USA.

6. Department of Pharmacology, University of California San Diego Health Sciences, La Jolla, CA 92093, USA.

7. Unit on Membrane Chemical Physics, National Institute of Child Health and Human Development, Bethesda, MD 20892, USA.

8. Center for High-Energy X-ray Sciences, Cornell High Energy Synchrotron Source (CHESS), Ithaca, NY 14850, USA.

Abstract

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 in Escherichia 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.

Publisher

American Association for the Advancement of Science (AAAS)

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