Molecular dynamics of water in oriented DPPC multilayers studied by quasielastic neutron scattering and deuterium-nuclear magnetic resonance relaxation

Abstract

The dynamics of water between highly oriented multilayers of 1,2-dipalmitoyl-sn-glycero-3-phosphocholine (DPPC) has been studied in two time domains at different hydration levels. Incoherent quasielastic neutron scattering (QENS) and deuterium-nuclear magnetic resonance (NMR) longitudinal (T1) relaxation were employed to investigate both the high-frequency motions of water (10−9–10−11 s time scale) and their anisotropy, while 2H-NMR transverse (T2) relaxation was used for obtaining information on low frequency dynamical processes (microsecond time scale). Our results show that high frequency dynamics (picosecond-time scale) at low hydration (three to four water molecules per lipid) can be understood solely as a uniaxial rotation of the water molecules tightly bound to DPPC head groups with a correlation time τrot≊62 ps at 55 °C and a rotational radius of 1±0.1 Å, but with no detectable translational degrees of freedom. The 2H-NMR T1 data (nanosecond-time scale) can be explained satisfactorily on the basis of fast rotations with the correlation time above and a slower reorientation of the rotational axis (correlation time τ1≊6 ns). Both QENS and 2H-NMR T1 measurements provide an apparent activation energy of Ea=32±1.0 kJ/mol for this process. Increasing the hydration level of the multilayers leaves the rotational motion essentially unchanged, but enables additional translational motion which can be considered as a jump diffusion process (diffusion coefficient D=16±1×10−10 m2/s at 44 °C and a mean residence time of τ0=2.0±0.5 ps) of nonbound water. It is interesting to note that this diffusion is completely isotropic on the characteristic length scale of this QENS experiment (≤10 Å). Temperature variation shows that the phase state of the lipids has no significant effect on the high frequency dynamics of the water molecules. Measurements of the 2H-NMR quadrupolar splitting of water (D2O) at temperatures around the phase transition temperature Tm of the oriented DPPC multilayers clearly show a coexistence of the crystalline Lβ′ phase and of the fluid Lα phase over a range of up to 4 °C at both sides of Tm. The intermediate Pβ′ (‘‘ripple’’) phase is suppressed as we worked at hydration levels below saturation. In the coexistence range, exchange of water takes place between crystalline and fluid lipid domains due to water diffusion. This exchange causes a pronounced minimum of the 2H-NMR transverse relaxation time T2 at Tm since this low frequency process satisfies approximately a critical damping condition for a two-site chemical exchange process.

Molecular motions in lipid bilayers studied by the neutron backscattering technique

“…15% freeze already in the region of critical swelling of the bilayers which may be accompanied by coexisting gel and fluid microdomains, as discussed in Ref. 21 and also reported from NMR experiments 9 . We attribute the second freezing transition at T f w =271 K, which is observed in D5 and D6, to freezing ).…”

“…Here, we report on a high energy-resolution neutron backscattering study to investigate slow motions on nanosecond time scales in highly oriented solid supported phospholipid bilayers of the model system DMPC -d54 (deuterated 1,2-dimyristoylsn-glycero-3-phoshatidylcholine), hydrated with heavy water. The spectrum of fluctuations in biomimetic and biological membranes covers a large range of time and length scales 1,8,9,10,11,12,13,14,15 , ranging from the long wavelength undulation and bending modes of the bilayer with typical relaxation times of nanoseconds and lateral length scales of several hundred lipid molecules to the short wavelength density fluctuations in the picosecond range on nearest neighbor distances of lipid molecules. Local dynamics in lipid bilayers, i.e.…”

“…König et al 9 have investigated the molecular dynamics of water in DPPC multilayers by quasielastic neutron scattering (QENS) and nuclear magnetic resonance (NMR). Neutron diffraction and QENS experiments on the interaction of hydration water and purple membranes have been reported by Lechner The lamellar spacing d z proves to be a very fine measure for the water content in between the membrane stacks as it is sensitive to the number of water layers (hydration shells) between two bilayers (which have a thickness of about 3.5-4Å).…”

“…From QENS measurements at different degrees of hydration and orientations (with the scattering vector Q parallel and perpendicular to the plane of the bilayers), the different water dynamics and anisotropy can be extracted 9 . At low hydration of the bilayers, rotation of water molecules is the dominant motion without signs of translational diffusion.…”

Structure and dynamics of water and lipid molecules in charged anionic DMPG lipid bilayer membranes

“…A number of different experimental techniques like NMR, [1][2][3] time-resolved fluorescence spectroscopy, 4 neutron scattering, [5][6][7][8]11,18 ultrafast spectroscopy, 9 and IR absorption spectroscopy 10 have been used to study hydration water dynamics at the interface between a lipid bilayer membrane and bulk water. Most of these studies have been conducted a) Author to whom correspondence should be addressed.…”