X-ray scattering reveals molecular tilt is an order parameter for the main phase transition in a model biomembrane

Synchrotron diffuse x-ray scattering data reveal a dramatic softening of the molecular tilt modulus $K_{\theta }$ of the model biomembrane composed of DMPC lipids as the temperature is lowered towards the main phase transition temperature at $T_M={24}^{\circ }\mathrm{C}$. Spontaneous tilt occurs below $T_M$, suggesting that tilt is a symmetry breaking order parameter. Consistent with this hypothesis, it is also found that a different lipid POPS has no spontaneous tilt below its $T_M$ at ${14}^{\circ }\mathrm{C}$ and correspondingly its tilt modulus did not soften as $T_M$ was approached from above. As previously known, the bending modulus $K_C$ of DMPC also softens close to $T_M$, but unlike the tilt modulus, $K_C$ has a maximum $3^{\circ }$ above $T_M$, which also marks the limit of the well-known anomalous swelling regime. Tilt adds a different perspective to our previous understanding of the main phase transition in lipid bilayers.

Figure 1

Tilt modulus $K_{\theta }$ vs temperature for bilayers of DMPC (solid squares) and POPS (open circles) with phase transition temperatures $T_M$ shown in the legend. Results were obtained from analysis of diffuse x-ray scattering data [11, 12].

Figure 2

Grazing incidence background subtracted scattering intensity from oriented bilayers of DMPC at $10{}^{\circ }\mathrm{C}$ (top) and POPS at $5{}^{\circ }\mathrm{C}$ (bottom). The beam is located at 0, lamellar diffraction from the stack of membranes appears along the $q_r=0$ meridian, blocked for DMPC in (a). Wide angle scattering from aligned hydrocarbon chains of POPS is centered at $q_r=1.47{\AA }^{-1}$ and $q_z=0$, with negative $q_z$ intensity cut off by the substrate. The nonzero extent in the $q_z$ direction is due to the finite thickness of the chain region. Lipids with tilted chains such as DMPC exhibit additional wide angle peaks not centered on the $q_z=0$ equator [15, 16].

Figure 3

Bending modulus $K_C$ vs temperature ($T_M={24}^{\circ }\mathrm{C}$) for DMPC bilayers with tilt (solid squares) and without tilt (open circles) included in the analysis of the diffuse x-ray scattering data [12].

Figure 4

Tilt modulus $K_{\theta }$ vs temperature difference $\mathrm{\Delta }T$ between the experimental temperature and the main chain melting transition temperature $T_M$ of each of nine common lipids with the same large PC head group that induces spontaneous tilt in gel phases [13]. See https://avantilipids.com/ for the full chemical names, structures, and $T_M$ of these lipids.