Effect of Phospholipid Headgroup Charge on the Structure and Dynamics of Water at the Membrane Interface: A Terahertz Spectroscopic Study

Abstract

Biological membranes are highly organized supramolecular assemblies of lipids and proteins. The membrane interface separates the outer (bulk) aqueous phase from the hydrophobic membrane interior. In this work, we have explored the microstructure and collective dynamics of the membrane interfacial hydration shell in zwitterionic and negatively charged phospholipid membrane bilayers using terahertz time-domain spectroscopy. We show here that the relaxation time constants of the water hydrogen bond network exhibit a unique "rise and dip" pattern with increasing lipid concentration. More importantly, we observed a dependence of the critical lipid concentration corresponding to the inflection point on the charge of the lipid headgroup, thereby implicating membrane electrostatics as a major factor in the microstructure and dynamics of water at the membrane interface. These results constitute one of the first experimental evidences of the modulation of the dielectric relaxation response of membrane interfacial water by membrane lipid composition in a concentration-dependent manner. Lipid-stringent membrane hydration could be relevant in the broader context of lipid diversity observed in biological membranes and the role of negatively charged lipids in membrane protein structure and function.

Hydration Shells of DPPC Liposomes from the Point of View of Terahertz Time-Domain Spectroscopy

“…Pal et al. 17 documented non-monotonous concentrated dependencies of dielectric parameters related to orientational dynamics of water molecules in liposome suspensions, as well as the influence of the charge of hydrophilic surface of liposomes on water dynamics.…”

Hydration Dynamics in Biological Membranes: Emerging Applications of Terahertz Spectroscopy

“…Effect of phospholipid headgroup charge (membrane interfacial electrostatics) and crowding on water microstructure and dynamics at the membrane interface. Panel a shows the unique “rise and dip” trend in relaxation time constants characteristic of membrane interfacial water as a function of lipid concentration reported recently by us . Membrane interfacial water molecules characterized by shorter relaxation time constants (i.e., faster hydrogen-bond reorganization) are shown in light blue (panels b and d) and those with longer relaxation time constants (i.e., slower hydrogen-bond reorganization) are in dark blue (panel c).…”

“…In this context, we have recently explored the microstructure and collective dynamics of the water hydrogen-bond network associated with zwitterionic and negatively charged model membrane bilayers as a function of lipid concentration using THz-TDS . These experimental conditions allowed us to probe how changes in crowding and membrane interfacial electrostatics, factors commonly encountered by membranes in cellulo , can shape hydration dynamics in biological membranes.…”

Functional Hydration Behavior: Interrelation between Hydration and Molecular Properties at Lipid Membrane Interfaces

“…In dielectric relaxation spectroscopy, it is possible to observe the behavior of the dipole moments of water molecules [51][52][53][54]. If the system is swept by an alternating electric field, the dipole of the water molecule exhibits a Debye relaxation.…”