Does Sucrose Change Its Mechanism of Stabilization of Lipid Bilayers during Desiccation? Influences of Hydration and Concentration.

Sugar-membrane interactions are believed to be responsible for cell preservation during desiccation and freezing, but the molecular mechanism by which they achieve this is still not well understood. The associated decrease of the main phase transition temperature of phospholipid bilayers is explained by two opposing views on the matter: the direct sugar-phospholipid interaction at the bilayer interface (water replacement hypothesis) and an entropy-driven phase transition with sugar molecules concentrating away from the lipid interface (hydration forces explanation). Both mechanisms are supported by experiments but molecular dynamics (MD) simulations have overwhelmingly shown the occurrence of direct sugar-phospholipid interactions. We have performed MD simulations of 1,2-dioleoyl-sn-glycero-3-phosphocholine (DOPC) bilayers at different water and sucrose contents. The behavior of sucrose was found to depend on both the sucrose and water contents: at high sucrose concentration and at low hydration, it is best described by the hydration forces explanation model, whereas at low sucrose concentration, it is consistent with the water replacement hypothesis model. These simulations reveal that at low concentration, sucrose molecules preferentially interact directly with the membrane interface while at high concentration, they preferentially accumulate in the intermembrane solution. The transition between the two modes of interaction is revealed for the first time as being governed by the saturation of the lipid bilayer interface with sucrose molecules, and this occurs more rapidly as the level of hydration decreases.