Rotational Dynamics of Water at the Phospholipid Bilayer Depending on the Head Groups Studied by Molecular Dynamics Simulations

Abstract

Hydration states are a crucial factor that affect the self-assembly and properties of soft materials and biomolecules. Although previous experiments have revealed that the hydration state strongly depends on the chemical structure of lipid molecules, the mechanisms at the molecular level remain unknown. Classical and density-functional tight-binding (DFTB) molecular dynamics (MD) simulations are employed to determine the mechanisms underlying dissimilar water dynamics between lipid membranes with phosphatidylcholine (PC) and phosphatidylethanolamine (PE) head groups. The classical MD simulation shows that rotational relaxations of water are faster on the PE lipid than on the PC lipid, which is consistent with a previous experimental study using terahertz spectroscopy. Furthermore, DFTB-MD simulation of N(CH 3 ) 4 + and NH 4 + ions, which correspond to the different head groups in PC and PE, respectively, shows qualitative agreement with the classical MD simulation. Remarkably, the PE lipids and the NH 4 + ions break hydrogen bonds between water molecules in the secondary hydration shell. In contrast, the PC lipids and the N(CH 3 ) 4 + ions bind water molecules weakly in both the primary and secondary hydration shells and increase hydrogen bonds between water. Our atomistic simulations show that these changes in the hydrogen-bond network of water molecules cause the different rotational relaxation of water molecules between the two lipids.

Effect of Osmolytes on Water Mobility Correlates with Their Stabilizing Effect on Proteins

“…Although terahertz spectroscopy has been used to analyze TMAO, urea, and sugars independently, there are no reports comparing various osmolytes under the same conditions, and the relation between water molecular dynamics and protein stability is still a mystery. Using MD simulations and THz spectroscopy, one of the present authors have shown that the rotational dynamics of water in solutions can be faster than that of bulk water, even when there is strong hydrogen bonding between the solute and water. , In other words, the long-range structure of water can be broken even when each hydrogen bond is strengthened. Therefore, terahertz spectroscopy may help resolve the puzzling aspects of water-structure-making/breaking.…”

“…This means that the slow relaxation mode measured in this study is only from bulk-like water. Since some water molecules become hydration water and will not be observed in the THz region, the signal from bulk-like water and ε″ both decrease according to the amount of hydration water. ,, On the other hand, it has also been reported that ε″ could increase in the THz region, indicating that the slow relaxation is shifted to a higher frequency, which corresponds to the acceleration of rotational dynamics. , The acceleration will be discussed later. If we look at the fast relaxation mode due to collision dynamics, it can also be affected by solutes, and the strengthening of this mode indicates solute-induced isolation of water molecules from the hydrogen bond network.…”

“…In contrast, a negative n hyd corresponds to a strong water-structure-breaking effect from the osmolyte.. , The size of water clusters is reduced owing to the structure-breaking effect, and their collective rotational dynamics are likely accelerated. Our recent MD simulations of phospholipid bilayers/water systems showed that the rotational dynamics of water can be accelerated in the weakly hydrated water layer even when there is strong direct hydrogen bond between solute and water . The results indicated that the water–water hydrogen bonds were broken owing to the strong interaction between water and solute, resulting in accelerated rotational dynamics.…”

“…Using MD simulations and THz spectroscopy, one of the present authors have shown that the rotational dynamics of water in solutions can be faster than that of bulk water, even when there is strong hydrogen bonding between the solute and water. 29,44 In other words, the long-range structure of water can be broken even when each hydrogen bond is strengthened. Therefore, terahertz spectroscopy may help resolve the puzzling aspects of water-structuremaking/breaking.…”

Surprising Rigidity of Functionally Important Water Molecules Buried in the Lipid Headgroup Region

“…Figure schematically illustrates the lipid bilayer structure using hydrated dimyristoylphosphatidylcholine (DMPC) lipids as a model. In the hydrophilic surface of the bilayer, the interfacial water layers have an approximate thickness of ∼1 nm between the fatty acyl chains and the choline nitrogen, with the first water layer in the vicinity of the glycerol C3 ester linkage that has the slowest exchange rate . The hydration shells in the headgroup region can be graded by the stability of the water molecules.…”