Interfacial Water Facilitates Energy Transfer by Inducing Extended Vibrations in Membrane Lipids

Abstract

ABSTRACT:We report the complete assignment of the vibrational spectrum of dipalmitoylphosphatidylcholine (DPPC), which belongs to the most ubiquitous membrane phospholipid family, phosphatidylcholine. We find that water hydrating the lipid headgroups enables efficient energy transfer across membrane leaflets on sub-picosecond time scales. The emergence of spatially extended vibrational modes upon hydration, underlies this phenomenon. Our findings illustrate the importance of collective molecular behavior of biomembranes and reveal that hydrated lipid membranes can act as efficient media for the transfer of vibrational energy. ■ INTRODUCTIONCell membranes are subject to energy input from various sources such as the sun, exothermic chemical reactions, and mechanical perturbation by the cytoskeleton and the extracellular matrix. To understand the stability and functioning of membranes, it is thus important to acquire a better understanding of how the membrane deals with the influx of energy. An important role is played by the water molecules hydrating the membrane phospholipid molecules.1,2 Hence to gain a deeper understanding of energy-transfer phenomena, we have to know the molecular mechanisms of energy storage and transfer of the combined phosphilipid−water system. 3 This is also highly relevant in nanotechnology where membranes are often the soft material of choice for nanoscale devices. 4 To obtain molecular insights into energy transfer in combined lipid−water systems is challenging, as lipid headgroups are complex structures, involving hydrophobic patches with an otherwise highly hydrophilic area. Interfacial water on the hydrophilic parts has characteristic structures and dynamics, distinct from those of water layers on hydrophobic surfaces. Experimentally, progress in the study of assembled interfacial water structures has been made using ultrafast electron crystallography, and it was found that the energy transfer in these structures happens on ultrashort time scales. 5 The energytransfer dynamics of a lipid monolayer interfacing aqueous environment has also been studied with time-resolved surface sum-frequency generation. 6 The results of this study indicated the presence of two distinct categories of water molecules, showing fast and slow energy-transfer dynamics, and fast energy transfer across a monolayer of lipids. 7 However, a molecularscale assignment of the mechanism behind the energy transfer and the different types of water has remained challenging. 8Classical (molecular dynamics and Monte Carlo) approaches have been extensively used to probe energy transfer in a wide range of materials with significant success. 4 Density functional theory (DFT) treatments are in principle more accurate 9,10 but have not been tractable for large molecular systems because of the enormous computational cost as a result of the cubic scaling of the cost with the number of atoms. Here, we circumvent those limitations by adopting an approach developed recently in the realm of condensed matter physics. 11,12 In this a...

Poisson’s Ratio and Young’s Modulus of Lipid Bilayers in Different Phases

“…The approach could also be combined with more accurate simulation of bilayers. Full atomistic simulations and in particular ab initio simulations, could in principle provide more accurate descriptions of the system but comes with a huge computational burden (Mashaghi et al, 2012, 2013a). …”

Enhanced Autoionization of Water at Phospholipid Interfaces

“…14,16 The calculated ground state structure is used as the starting configuration for AIMD and AIMC simulations at 300 K (Figure 1a). The AIMD simulations are performed 14,19,20 up to a time of 3 ps with a time step Δt = 0.1 fs, which is about one hundredth of the shortest vibration period in this system.…”

“…The AIMD simulations are performed 14,19,20 up to a time of 3 ps with a time step Δt = 0.1 fs, which is about one hundredth of the shortest vibration period in this system. 16 The temperature is kept fixed with a Nose−Hoover thermostat.…”

The Stability of Silver Nanoparticles in a Model of Pulmonary Surfactant

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