Dehydration induced dynamical heterogeneity and ordering mechanism of lipid bilayers
03 May 2021-Journal of Chemical Physics (AIP Publishing LLCAIP Publishing)-Vol. 154, Iss: 17, pp 174904-174904
TL;DR: The analyses reveal that the microscopic mechanism of lipid ordering by dehydration is governed by dynamical heterogeneity, which can be applied to complex bio-membranes to trap functionally relevant gel-like domains at room temperature.
Abstract: Understanding the influence of dehydration on the membrane structure is crucial to control membrane functionality related to domain formation and cell fusion under anhydrobiosis conditions. To this end, we perform all-atom molecular dynamic simulations of 1,2-dimyristoyl-sn-glycero-3-phosphocholine dimyristoylphosphatidylcholine lipid membranes at different hydration levels at 308 K. As dehydration increases, the lipid area per head group decreases with an increase in bilayer thickness and lipid order parameters indicating bilayer ordering. Concurrently, translational and rotational dynamics of interfacial water (IW) molecules near membranes slow down. On the onset of bilayer ordering, the IW molecules exhibit prominent features of dynamical heterogeneity evident from non-Gaussian parameters and one-dimensional van Hove correlation functions. At a fully hydrated state, diffusion constants (D) of the IW follow a scaling relation, D∼τα−1, where the α relaxation time (τα) is obtained from self-intermediate scattering functions. However, upon dehydration, the relation breaks and the D of the IW follows a power law behavior as D∼τα−0.57, showing the signature of glass dynamics. τα and hydrogen bond lifetime calculated from intermittent hydrogen bond auto-correlation functions undergo a similar crossover in association with bilayer ordering on dehydration. The bilayer ordering is accompanied with an increase in fraction of caged lipids spanned over the bilayer surface and a decrease in fraction of mobile lipids due to the non-diffusive dynamics. Our analyses reveal that the microscopic mechanism of lipid ordering by dehydration is governed by dynamical heterogeneity. The fundamental understanding from this study can be applied to complex bio-membranes to trap functionally relevant gel-like domains at room temperature.
Citations
More filters
TL;DR: In this article, the effect of trimethylamine N-oxide (TMAO) and urea on lipid membrane was investigated under different hydration conditions. And the results indicated that urea significantly inhibits the dehydration-induced fluid-to-gel phase transition by strongly interacting with the lipid membrane via hydrogen bonds, which balances the reduced lipid hydration due to the decreasing water content.
Abstract: Living organisms are often exposed to extreme dehydration, which is detrimental to the structure and function of the cell membrane. The lipid membrane undergoes fluid-to-gel phase transition due to dehydration and thus loses fluidity and functionality. To protect the fluid phase of the bilayer these organisms adopt several strategies. Enhanced production of small polar organic solutes (also called osmolytes) is one such strategy. Urea and trimethylamine N-oxide (TMAO) are two osmolytes found in different organisms combating osmotic stress. Previous experiments have found that both these osmolytes have strong effects on lipid membrane under different hydration conditions. Urea prevents the dehydration-induced phase transition of the lipid membrane by directly interacting with the lipids, while TMAO does not inhibit the phase transition. To provide atomistic insights, we have carried out all-atom molecular dynamics (MD) simulation of a lipid membrane under varying hydration levels and studied the effect of these osmolytes on different structural and dynamic properties of the membrane. This study suggests that urea significantly inhibits the dehydration-induced fluid-to-gel phase transition by strongly interacting with the lipid membrane via hydrogen bonds, which balances the reduced lipid hydration due to the decreasing water content. In contrast, TMAO is excluded from the membrane surface due to unfavorable interaction with the lipids. This induces further dehydration of the lipids which reinforces the fluid-to-gel phase transition. We have also studied the counteractive role of TMAO on the effect of urea on lipid membrane when both the osmolytes are present. TMAO draws some urea molecules out of the membrane and thereby reduces the effect of urea on the lipid membrane at lower hydration levels. This is similar to the counteraction of urea's deleterious effects on protein by TMAO. All these observations are consistent with the experimental results and thus provide deep molecular insights into the role of these osmolytes in protecting the fluid phase of the membrane, the key survival strategy against osmotic-stress-induced dehydration.
7 citations
TL;DR: In this article , the authors review, analyze, and comment on recent works on the structure and dynamics of water around biomolecules and their role in specific biological functions, and they comment on the advances made in understanding the role of water inside a biological cell.
6 citations
TL;DR: In this paper , all atom molecular dynamics simulations of fully hydrated dimyristoylphosphatidylcholine lipid bilayers are performed for total 9.45 μs showing a fluid to a ripple to a gel phase transition.
Abstract: All atom molecular dynamics simulations of fully hydrated dimyristoylphosphatidylcholine lipid bilayers are performed for total 9.45 μs showing a fluid to a ripple to a gel phase transition. Changes in the radial distribution functions and angular distribution functions of the interface water (IW) signify a shift from a distorted tetrahedral to a tetrahedral arrangement upon decrease in temperature at the gel phase. The potential of mean forces of the IW follow two cross-overs near both phase transitions unlike the BW. Our analyses reveal a strong correlation between bilayer phase transitions and the structural properties of the IW.
3 citations
TL;DR: In this article , the authors selectively switched off the hydrogen bonds (one specific bond or their combinations in all the base pairs at a time) via manipulating the force fields for A-T and G-C base pairs.
3 citations
TL;DR: In this paper , the fluorescence spectrum of Laurdan embedded in solid-supported lipid bilayers as a function of hydration and compared it with the effect of cholesterol, a major membrane fluidity regulator.
Abstract: Studies of biological membrane heterogeneity particularly benefit from the use of the environment-sensitive fluorescent probe Laurdan, for which shifts in the emission, produced by any stimulus (e.g. fluidity variations), are ascribed to alterations in hydration near the fluorophore. Ironically, no direct measure of the influence of membrane hydration level on Laurdan spectra has been available. To address this, we investigated the fluorescence spectrum of Laurdan embedded in solid-supported lipid bilayers as a function of hydration and compared it with the effect of cholesterol – a major membrane fluidity regulator. The effects are illusively similar, hence the results obtained with this probe should be interpreted with caution. The dominant phenomenon governing the changes in the spectrum is the hindrance of the lipid internal dynamics. Furthermore, we unveiled the intriguing mechanism of dehydration-induced redistribution of cholesterol between domains in the phase-separated membrane which reflects yet another regulatory function of cholesterol.
2 citations
References
More filters
TL;DR: In this paper, a method is described to realize coupling to an external bath with constant temperature or pressure with adjustable time constants for the coupling, which can be easily extendable to other variables and to gradients, and can be applied also to polyatomic molecules involving internal constraints.
Abstract: In molecular dynamics (MD) simulations the need often arises to maintain such parameters as temperature or pressure rather than energy and volume, or to impose gradients for studying transport properties in nonequilibrium MD A method is described to realize coupling to an external bath with constant temperature or pressure with adjustable time constants for the coupling The method is easily extendable to other variables and to gradients, and can be applied also to polyatomic molecules involving internal constraints The influence of coupling time constants on dynamical variables is evaluated A leap‐frog algorithm is presented for the general case involving constraints with coupling to both a constant temperature and a constant pressure bath
25,256 citations
TL;DR: An N⋅log(N) method for evaluating electrostatic energies and forces of large periodic systems is presented based on interpolation of the reciprocal space Ewald sums and evaluation of the resulting convolutions using fast Fourier transforms.
Abstract: An N⋅log(N) method for evaluating electrostatic energies and forces of large periodic systems is presented. The method is based on interpolation of the reciprocal space Ewald sums and evaluation of the resulting convolutions using fast Fourier transforms. Timings and accuracies are presented for three large crystalline ionic systems.
24,332 citations
TL;DR: It is demonstrated that arbitrary accuracy can be achieved, independent of system size N, at a cost that scales as N log(N), which is comparable to that of a simple truncation method of 10 A or less.
Abstract: The previously developed particle mesh Ewald method is reformulated in terms of efficient B‐spline interpolation of the structure factors This reformulation allows a natural extension of the method to potentials of the form 1/rp with p≥1 Furthermore, efficient calculation of the virial tensor follows Use of B‐splines in place of Lagrange interpolation leads to analytic gradients as well as a significant improvement in the accuracy We demonstrate that arbitrary accuracy can be achieved, independent of system size N, at a cost that scales as N log(N) For biomolecular systems with many thousands of atoms this method permits the use of Ewald summation at a computational cost comparable to that of a simple truncation method of 10 A or less
17,897 citations
TL;DR: A new implementation of the molecular simulation toolkit GROMACS is presented which now both achieves extremely high performance on single processors from algorithmic optimizations and hand-coded routines and simultaneously scales very well on parallel machines.
Abstract: Molecular simulation is an extremely useful, but computationally very expensive tool for studies of chemical and biomolecular systems Here, we present a new implementation of our molecular simulation toolkit GROMACS which now both achieves extremely high performance on single processors from algorithmic optimizations and hand-coded routines and simultaneously scales very well on parallel machines The code encompasses a minimal-communication domain decomposition algorithm, full dynamic load balancing, a state-of-the-art parallel constraint solver, and efficient virtual site algorithms that allow removal of hydrogen atom degrees of freedom to enable integration time steps up to 5 fs for atomistic simulations also in parallel To improve the scaling properties of the common particle mesh Ewald electrostatics algorithms, we have in addition used a Multiple-Program, Multiple-Data approach, with separate node domains responsible for direct and reciprocal space interactions Not only does this combination of a
14,032 citations
TL;DR: The software suite GROMACS (Groningen MAchine for Chemical Simulation) that was developed at the University of Groningen, The Netherlands, in the early 1990s is described, which is a very fast program for molecular dynamics simulation.
Abstract: This article describes the software suite GROMACS (Groningen MAchine for Chemical Simulation) that was developed at the University of Groningen, The Netherlands, in the early 1990s. The software, written in ANSI C, originates from a parallel hardware project, and is well suited for parallelization on processor clusters. By careful optimization of neighbor searching and of inner loop performance, GROMACS is a very fast program for molecular dynamics simulation. It does not have a force field of its own, but is compatible with GROMOS, OPLS, AMBER, and ENCAD force fields. In addition, it can handle polarizable shell models and flexible constraints. The program is versatile, as force routines can be added by the user, tabulated functions can be specified, and analyses can be easily customized. Nonequilibrium dynamics and free energy determinations are incorporated. Interfaces with popular quantum-chemical packages (MOPAC, GAMES-UK, GAUSSIAN) are provided to perform mixed MM/QM simulations. The package includes about 100 utility and analysis programs. GROMACS is in the public domain and distributed (with source code and documentation) under the GNU General Public License. It is maintained by a group of developers from the Universities of Groningen, Uppsala, and Stockholm, and the Max Planck Institute for Polymer Research in Mainz. Its Web site is http://www.gromacs.org.
13,116 citations