What Is So Unique About Biomembrane Organization and Dynamics?

Hydration Dynamics in Biological Membranes: Emerging Applications of Terahertz Spectroscopy

“…Figure a highlights the influence of water molecules in the membrane interaction/insertion and subsequent folding of both short peptides and multidomain membrane-spanning proteins. In addition, water molecules have been shown to act as a “foldase” and catalyze large-scale conformational rearrangements of peptide dimers in a low dielectric environment, reminiscent of the membrane hydrophobic core . This recurring theme of water-mediated membrane interaction and organization observed across membrane-interacting peptides and integral transmembrane proteins is reflected in the pivotal functional role of water molecules in membrane biology (Figure b). In this Perspective, we provide a glimpse into the ever-broadening functional landscape of hydration dynamics in biological membranes in the backdrop of the unique physical chemistry of water molecules.…”

“…The membrane bilayer segregates the extracellular matrix from the cellular interior and acts as a structured catalytic scaffold for biochemical processes occurring at the membrane. Biological membranes have been characterized as deformable soft matter, , with depth-dependent gradients of various physicochemical properties. , These depth-dependent gradients arise, in part, as an immediate consequence of the amphiphilic structure of the constituent phospholipids (see Figure a for a representative chemical structure of phospholipids) and result in dynamic partitioning of each leaflet of the membrane bilayer into an anisotropic polar interface and an isotropic hydrocarbon core (Figure b). The sharp decrease in water penetration across the membrane depth (Figure b), with the largest magnitude of change spatially coinciding with the membrane interface, is arguably the most defining feature of biological membranes.…”

“…The most notable of these are dipolar relaxation of the extended water hydrogen-bond network, restricted solvation dynamics at charged or polar surfaces (including the membrane interface and protein surfaces), ,,, hydration dynamics at enzyme active sites, and water exchange with buried hydration sites . Incidentally, hydration dynamics at longer time scales (highlighted by a yellow bar in Figure ) could be influenced by biomembrane properties and coupled to membrane dynamics, possibly because of substantial temporal overlap in the two. In this context, we have recently reported faster solvent relaxation in the Golgi membrane of live cells relative to the plasma membrane, utilizing a fluorescence-based spectral relaxation imaging approach .…”

“…However, in the presence of membranes, water orientational dynamics is additionally influenced by the hydrogen-bonding capacity of lipid headgroups (and amino acid constituents of membrane proteins) present at the membrane interface. In other words, the physicochemical nature of the membrane interface, recognized to be important in myriad functional aspects of membrane biology, , is reflected in the dielectric relaxation of membrane-associated water. In fact, even subtle changes in the membrane microenvironment could be expected to significantly impact water microstructure and dynamics, on account of the responsive nature of water molecules encoded in their immense structural plasticity.…”

“…However, spatially resolved insights into these water subpopulations (e.g., spatial coordinates defined with respect to proximity to a nonaqueous hydrogen-bonding partner) remain scarce. Hydration sheaths associated with biomimetic and biological membranes are expected to be particularly amenable to THz-based studies investigating spatial heterogeneity in the water hydrogen-bond network because of the rich tapestry of existing knowledge regarding membrane organization and dynamics. ,,− ,,− Hydration sheaths associated with biomimetic and biological membranes are expected to be particularly amenable to THz-based studies investigating spatial heterogeneity in the water hydrogen-bond network because of the rich tapestry of existing knowledge regarding membrane organization and dynamics.…”