Survival of the best heads: The physical merits of lipid headgroup adaptation in anhydrobiosis


Survival of the best heads: The physical merits of lipid headgroup adaptation in anhydrobiosis

Abu Sharkh, S.; Erkut, C.; Kurzchalia, T.; Fahmy, K.

Anhydrobiotic organisms down-regulate their metabolism and preserve their cellular architecture at strongly reduced water potential to resume life after periods of desiccation. We have studied the dauer larva of the nematode Caenorhabditis elegans which represents an anhydrobiotic state of this genetically fully described organism. After preconditioning, an adaptational 4 days period of reduced humidity, survival of harsh desiccation occurs and depends on the synthesis of the disaccharide trehalose [1]. Using the temperature-sensitive strain daf-2(e1370), which arrests in the dauer state when grown at 25 °C, we show by thin layer chromatography that the phospholipid composition is altered from high to low PC/PE content during preconditioning. Time-resolved FTIR spectroscopy of lyotropic phase transitions induced within seconds in extracted C.elegans phospholipids by short hydration pulses, reveals that the decreased PC content allows a larger coupling of headgroup hydration to acyl chain packing as compared to the PE-rich state. The compressibility modulus was derived from CH-stretching frequency changes and the effect of trehalose studied. The data suggest a dynamic interaction of trehalose with the lipids during fast hydration at low humidity (75-85 % relative humidity) such that hydration water is transiently directed to the sub-headgroup carbonyl region, rather than being stably entrapped by trehalose. In combination with film balance experiments we show that the headgroup remodelling during preconditioning specifically increases the interaction of trehalose with the phospholipids, leading to a "softer" PC-depleted membrane which responds with larger lateral expansion during fast hydration transients. We explain the advantage of a reduced PC/PE ratio for anydrobiosis by the different intrinsic hydration properties of the two headgroups [2-3] which allows a more flexible water-mediated H-bond-network to form in the presence of trehalose. As a consequence, phase transitions on the seconds time-scale can proceed under close to equilibrium conditions in membranes of preconditioned worms. These molecular processes result in the relief of osmotic strain during membrane rehydration, thereby preventing membrane rupture during the critical phase of typically instantaneous rehydration of the desiccated anhydrobiotic organism before resuming its normal metabolism.

Keywords: Fourier transform infrared; time-resolved; membrane; hydration

  • Contribution to proceedings
    International Workshop "Molecular Membrane Biophysics", 03.-05.03.2014, Hünfeld, Germany

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Publ.-Id: 19987