Research ArticleBIOPHYSICS

Entropic effects enable life at extreme temperatures

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Science Advances  01 May 2019:
Vol. 5, no. 5, eaaw4783
DOI: 10.1126/sciadv.aaw4783
  • Fig. 1 Correlation between the abundance of tethered lipids and growth temperature in archaea.

    The percentage of tethered lipids in the membranes of three different archaea organisms was found to increase with increasing external growth temperature (1214).

  • Fig. 2 Kinetic analysis of leakage of encapsulated CF from liposomes.

    (A) Structures of monolayer-forming tethered lipids T32 and T36 and bilayer-forming untethered lipid U16. (B to D) Temperature-dependent CF release profile from liposomes prepared from T32 (B), T36 (C), and U16 (D). Data points show replicate results; solid curves are global fits to rate theory across all of the data in each graph simultaneously (see Materials and Methods). (E) Calculated enthalpy (ΔH) and entropy (ΔS) of activation for encapsulated CF leakage from liposomes using Eyring equation (see the “Kinetic analysis” section). Thermodynamic parameters were calculated using replicates from two separate liposome preparations with different diameters (~80 and ~200 nm). (F) Effect of temperature on Gibbs free energy of activation for CF leakage through 80-nm liposomes. Gibbs free energy was calculated at different temperature (22°, 37°, 50°, 60°, and 70°C) using the Gibbs fundamental equation (ΔG = ΔHTΔS). (G) Change in enthalpy (ΔΔH) for T32 (green) and T36 (blue) compared to ΔH obtained for U16. Student’s t test revealed no significant difference in ΔH between the two tethered lipids and between the data from different liposome diameters (and, hence, membrane curvature). (H) Change in entropy (ΔΔS) for T32 (green) and T36 (blue) compared to ΔS obtained for U16.

  • Fig. 3 Computational modeling of bilayer and monolayer membranes.

    (A) Correlation between membrane thickness measured experimentally by atomic force microscopy (AFM) and MD simulations. (B) Lateral diffusion coefficient of lipids in the membrane determined by MD simulation. (C) Correlation between variance in area per lipid determined by MD at different temperatures and experimental CF leakage rates obtained at different temperatures (Pearson r correlation = 0.63, P = 0.07). The dashed lines represent the 95% confidence band of the best-fit line. (D) Correlation between lipid lateral diffusion determined by MD and experimental CF leakage rates at different temperatures (Pearson r correlation = 0.87, P = 0.002). The dashed lines represent the 95% confidence band of the best-fit line. (E) Correlation between lipid self-diffusion determined by MD and experimental CF leakage rates at different temperatures (Pearson r correlation = 0.98, P < 0.0001). The dashed lines represent the 95% confidence band of the best-fit line.

  • Fig. 4 First-order entropy of lipid torsions.

    (A to D) Entropy analysis based on MD simulations with AMBER 14 (34) using GAFF (35) and Lipid14 (36) parameters, with TIP3P water, of membranes with and without CF restrained at a target depth in one leaflet in the presence of 150 mM KCl. (A) Simulation snapshot of CF restrained in the T32 monolayer membrane (100 ns, 300 K, 64 lipids). (B and C) First-order entropy of lipid torsions as a function of torsion position, where torsion 1 is at the top of the membrane and torsion 26 is at the bottom (A). Results are shown here for the unbranched methylene chain (B) and phytanyl chain (C) of each lipid. Red, untethered (U16) lipids; green, tethered (T32) lipids; solid lines, CF present in the membrane; dashed lines, CF absent from the membrane. The first-order entropy reported for each torsion is a per lipid average over all 64 instances of the torsion in the 64 lipid molecules of the tethered membrane simulations or the 128 lipid molecules of the untethered membrane simulations. (D) Effect of the presence of CF in the membrane on the first-order torsional entropy (in cal mol−1 K−1) per lipid of the simulated T32 and U16 lipid membranes, partitioned by lipid chain and bilayer leaflet (top versus bottom).

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/5/5/eaaw4783/DC1

    Fig. S1. Synthesis and characterization of archaea-inspired lipids.

    Fig. S2. Liposome radius distribution.

    Fig. S3. Time dependence of CF leakage at different temperatures for ~80-nm liposomes.

    Fig. S4. Temperature-dependent CF release profile from liposomes ~200 nm in diameter.

    Fig. S5. Cross-sectional views of simulated membranes.

    Fig. S6. Experimental and simulated measurements of membrane thickness.

    Fig. S7. Self-diffusion and lateral diffusion of lipids in simulated membranes.

    Fig. S8. Area per head group in simulated membranes.

    Fig. S9. Correlation plots for the variance in area per lipid.

    Fig. S10. Structures of U16 and T32 lipids including the position of C117 for each lipid.

  • Supplementary Materials

    This PDF file includes:

    • Fig. S1. Synthesis and characterization of archaea-inspired lipids.
    • Fig. S2. Liposome radius distribution.
    • Fig. S3. Time dependence of CF leakage at different temperatures for ~80-nm liposomes.
    • Fig. S4. Temperature-dependent CF release profile from liposomes ~200 nm in diameter.
    • Fig. S5. Cross-sectional views of simulated membranes.
    • Fig. S6. Experimental and simulated measurements of membrane thickness.
    • Fig. S7. Self-diffusion and lateral diffusion of lipids in simulated membranes.
    • Fig. S8. Area per head group in simulated membranes.
    • Fig. S9. Correlation plots for the variance in area per lipid.
    • Fig. S10. Structures of U16 and T32 lipids including the position of C117 for each lipid.

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