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

Abstract

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.

Membrane–Sugar Interactions Probed by Low-Frequency Raman Spectroscopy: The Monolayer Adsorption Model

“…Thus, the sugar distribution near the membrane surface at high sugar concentration becomes heterogeneous, which is proposed in the literature. 12,16,21 Note that, for C > 0.4 M, sugar molecules in the intermembrane solution interact with the membrane surface covered with sugar molecules, so this surface may possess different attractive/repulsive properties as compared with the pure lipid surface.…”

“…Also, it has been proposed that membrane–sugar interactions may be attractive at low sugar concentrations and repulsive at high concentrations . The importance of both attractive and repulsive membrane−sugar interactions was discussed in a number of publications. ,− …”

Molecular Dynamics Simulation of Small Molecules Interacting with Biological Membranes

“…It was shown that at temperatures high enough to cause thermal disruption, structural damage to the bilayer is prevented to a significant extent by the interaction of sugar molecules with the phospholipid head groups [119]. Recent MD simulations of the interaction of sucrose with DOPC bilayers at different levels of hydration have shown that sugar molecules interact preferentially with the lipid bilayer interface as described above at low concentration and/or high hydration, but at high concentration or low hydration they preferentially accumulate in the inter-bilayer solution as the bilayer interface becomes saturated with sugar molecules [121].…”

Effect of Cryopreservation Method Supported With Biochemical Analyses in the Axillary Bud of Jewel Orchid, Ludisia Discolor

“…Interactions in the sugar membrane are postulated to be responsible for preserving cell integrity during dehydration and freezing. According to Stachura et al (2019), the water replacement hypothesis occurred where the sucrose molecules interact with the bilayer phospholipid headgroups at low sucrose concentrations with high water content. These interactions and the network of hydrogen bonds with water molecules reinforce the stability of proteins and membrane bilayer during dehydration.…”