Hydration Layer of Only a Few Molecules Controls Lipid Mobility in Biomimetic Membranes

Abstract

Self-assembly of biomembranes results from the intricate interactions between water and the lipids’ hydrophilic head groups. Therefore, the lipid–water interplay strongly contributes to modulating membrane architecture, lipid diffusion, and chemical activity. Here, we introduce a new method of obtaining dehydrated, phase-separated, supported lipid bilayers (SLBs) solely by controlling the decrease of their environment’s relative humidity. This facilitates the study of the structure and dynamics of SLBs over a wide range of hydration states. We show that the lipid domain structure of phase-separated SLBs is largely insensitive to the presence of the hydration layer. In stark contrast, lipid mobility is drastically affected by dehydration, showing a 6-fold decrease in lateral diffusion. At the same time, the diffusion activation energy increases approximately 2-fold for the dehydrated membrane. The obtained results, correlated with the hydration structure of a lipid molecule, revealed that about six to seven water molecules directly hydrating the phosphocholine moiety play a pivotal role in modulating lipid diffusion. These findings could provide deeper insights into the fundamental reactions where local dehydration occurs, for instance during cell–cell fusion, and help us better understand the survivability of anhydrobiotic organisms. Finally, the strong dependence of lipid mobility on the number of hydrating water molecules opens up an application potential for SLBs as very precise, nanoscale hydration sensors.

Influenza A virus hemagglutinin prevents extensive membrane damage upon dehydration

“…For GFPbilayers and protein-free bilayers, measurements were performed specifically on non-damaged regions. Irrespective of membrane structure, we observed that the lipid mobility was greatly reduced after dehydration, as previously observed for protein-free bilayers [14]. In comparison to hydrated samples, lipids in protein-free bilayers displayed a D reduction of ~ 96 % ((0.03 ± 0.008) µm 2 /s, Figure 2 A "dehydrated").…”

“…Solid supported lipid bilayers (SLBs) have been extensively used as model membranes in biophysical studies due to their high stability and versatility in physiological conditions [14].…”

Behavior of Citrate-Capped Ultrasmall Gold Nanoparticles on a Supported Lipid Bilayer Interface at Atomic Resolution

“…Simulation components were selected to adequately recreate the experimental in situ AuNP SLB systems discussed above. As such, the simulated systems included a single basal plane 10 nm ( X ) × 10 nm ( Y ) mica substrate, a lipid bilayer (either DOPC or DPPC), an intervening ∼1 nm thick adlayer of water, − which resides between the substrate and the lipid bilayer, and a solvated citrate-capped AuNP. The system itself can then be thought of as two components: (1) the supported bilayer, which includes the substrate, the water solvation layer, and the lipid bilayer, and (2) the solvated citrate-capped AuNP.…”

“…Citrate was equilibrated around the AuNP in a 10 × 10 × 10 nm 3 box containing 1 AuNP and 500 citrate ions solvated in 150 mM NaCl for 100 ns, with citrate within 0.5 nm of the AuNP retained. Each complete system was composed of a 1 nm thick complete layer of mica (10 nm 2 laterally), a solvation layer to include appropriate in situ membrane dynamics, − 288 lipid molecules, the AuNP of 5743 gold atoms and 157 citrate molecules, solvated in a CHARMM TIP3P water box with 0.15 M NaCl and appropriate counterions. Simulations were run using the MD code GROMACS 2020 .…”

Water as a Link between Membrane and Colloidal Theories for Cells

“…In contrast, from the colloidal point of view, cytoplasmic water is stabilized, essentially continuously, by interactions with proteins, forming an extensive, ordered lattice in which the water molecules have reduced translational and orientational freedom and ordered microscopic arrangements compared with free water [ 64 ]. However, the so-called “bound” water invoked by the Ling’s AIH can not only be ascribed to the presence of macromolecules in the microscopic heterogeneity of the cytoplasm (due to the influence of cell organelles) but also to the presence of lipid aggregates such as a membrane [ 65 , 66 , 67 ]. These concepts may be incorporated into membrane theories without entering into conflict with Ling’s theory.…”