Molecular Mechanism of Cell Membrane Protection by Sugars: A Study of Interfacial H-Bond Networks

Abstract

Sugars function as bioprotectants by stabilizing biomolecules during dehydration, thermal stress, and freeze–thaw cycles. A buildup of sugars occurs in many organisms upon their exposure to extreme conditions. Understanding sugar’s bioprotective effects on membranes is achieved by characterizing the H-bond networks at the lipid–water interface. Here, we report the headgroup H-bond populations, structures, and dynamics of 1,2-dimyristoyl-sn-glycero-3-phosphocholine vesicles in concentrated glucose solutions using ultrafast two-dimensional infrared spectroscopy in conjunction with molecular dynamics simulations. H-Bond populations and dynamics at the ester carbonyl positions are largely unaffected even at very high, 600 mg/mL, sugar concentrations. In addition, dynamics exhibit a slight nonmonotonic dependence on sugar concentration. Simulations, which are in near-quantitative agreement with measured dynamics, show that the H-bond structure remains largely intact by the existence of sugar. This study shows that the bioprotection of sugar is realized through stable lipid–saccharide–water H-bond networks at the membrane interface that mimic the H-bond networks in pure water.