Letter pubs.acs.org/JPCL
Mosaic of Water Orientation Structures at a Neutral Zwitterionic Lipid/Water Interface Revealed by Molecular Dynamics Simulations Suyong Re,† Wataru Nishima,†,¶ Tahei Tahara,‡,§ and Yuji Sugita*,†,#,⊥,¶ †
RIKEN Theoretical Molecular Science Laboratory, ‡Molecular Spectroscopy Laboratory, §Ultrafast Spectroscopy Research Team, RIKEN Center for Advanced Photonics (RAP), and ¶RIKEN iTHES, RIKEN , 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan # RIKEN Advanced Institute for Computational Science and ⊥RIKEN Quantitative Biology Center, International Medical Device Alliance (IMDA) 6F, RIKEN, 1-6-5 minatojima-minamimachi, Chuo-ku, Kobe, Hyogo 650-0047, Japan S Supporting Information *
ABSTRACT: Ordering of water structures near the surface of biological membranes has been recently extensively studied using interface-selective techniques like vibrational sum frequency generation (VSFG) spectroscopy. The detailed structures of interface water have emerged for charged lipids, but those for neutral zwitterionic lipids remain obscure. We analyze an all-atom molecular dynamics (MD) trajectory of a hydrated 1-palmitoyl-2-oleoyl-sn-glycero-3phosphocholine bilayer to characterize the orientation of interface waters in different chemical environments. The structure and dynamics of interfacial waters strongly depend on both their vertical position along the bilayer normal as well as vicinal lipid charged groups. Water orientation in the vicinity of phosphate groups is opposite to that around choline groups. The results are consistent with observed VSFG spectra and demonstrate that a mosaic of water orientation structures exists on the surface of a neutral zwitterionic phospholipid bilayer, reflecting rapid water exchange and the influence of local chemical environments. SECTION: Biomaterials, Surfactants, and Membranes
W
peaks originating from water structures in different vertical positions.36 The precise orientation of interface waters thus remains elusive, although the existence of diverse water orientations near the membrane surface, dependent on local charged groups, fits well with many MD simulations.17,22,24,28,34 The Im χ(2) spectrum obtained by heterodyne-detected VSFG (HD-VSFG) provides information about net polar orientations of interfacial waters. Peak assignments in a spectrum are, however, difficult due to indistinguishable contributions from water molecules in different chemical environments. In the present work, we analyze an all-atom MD trajectory of a neutral zwitterionic phospholipid bilayer to characterize interfacial waters that contribute to the observed spectrum. Previous MD simulation studies mostly analyzed water orientation as a function of distance from the bilayer center14−21,23−26,30,31,33,35 and have the drawback that waters around the phosphate and choline groups cannot be distinguished due to overlap in vertical position. We here characterize interfacial waters in terms of their closest phospholipid charged group as well as their vertical position. This approach successfully deconstructs contributions from different types of interface waters to the net polar orientation. We performed a 100 ns MD simulation in a NPT ensemble (300 K, 1 bar) using the NAMD program package37 for a structure ensemble of hydrated POPC (1-palmitoyl-2-oleoyl-sn-
ater−lipid interaction is essential for the dynamics, stability, and function of biological membranes. Water structure near the membrane surface affects important biological phenomena including cell−cell adhesions and virus infection and has been extensively studied experimentally as well as by computer simulations.1−3 Recent advances in interface-selective vibrational sum frequency generation (VSFG) spectroscopy4 with heterodyne detection enable the direct measurement of complex second-order nonlinear susceptibility, χ(2), whose imaginary part (Im χ(2)) contains unambiguous information about the up/down orientation of interface waters.5−8 The technique has provided evidence of preferentially oriented water molecules at the interface with anionic/cationic charged lipids.8−11 A neutral zwitterionic phospholipid/water interface has diverse chemical environments due to the coexistence of positive and negative charges in the phospholipid head group. A recent VSFG study using isotopically diluted water indicates that the waters at such interfaces have heterogeneous orientations in response to local charges,12 although another study suggests that they orient homogeneously like those at anionic lipid interfaces.11 Theoretical studies based on molecular dynamics (MD) simulations are also inconclusive.13−35 The analysis of water dipole orientations typically implies a particular ordering in the interface region.17,23,26,30,31,33,35 In contrast, radial distribution functions of the oxygen and hydrogen atoms of waters around the lipid head groups indicate the presence of characteristic local structures.15,17,19,22,23,28 Simulated VSFG spectra show three © 2014 American Chemical Society
Received: October 30, 2014 Accepted: December 2, 2014 Published: December 2, 2014 4343
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during the simulation. Water molecules associated with the phosphates (P) and the cholines (N) are evenly distributed on the surface, although the mosaic of the different types of interfacial waters changes from one snapshot to the next. N, the choline-associated water, is slightly more exposed to the bulk region than others, as is also evident from the electron density profile (Figure S1, Supporting Information). Using the five snapshots, we calculated the orientation of water dipoles (the angle θ between the water dipole and bilayer normal) for each type of interfacial water (Figure 2b). The value of θ is 180° if the water molecule orients with hydrogen atoms pointing toward the surface (H-up) and 0° if the oxygen atom points toward the surface (H-down). In comparison with Figure 2a, we found a tendency for the phosphate-associated waters to orient H-up and the choline-associated to orient H-down. In all snapshots, H-up and H-down water molecules coexist on the surface, implying that they orient in response to the closest positive or negative charge of the head groups. Figure 2c shows the water orientation (average cosine of the angle θ) as a function of distance z from the bilayer center. Consistent with earlier simulation studies,30,33 water molecules are weakly H-up oriented around 20 Å (the minimum position corresponds to θ of ∼102°), which is the average position of the head groups (Figure S1, Supporting Information). We further analyzed the local structure of waters around the phosphate and choline groups by deconstructing contributions from different types of interfacial waters. The phosphateassociated water molecules (P and P−N) are strongly H-up oriented with increasing z distance. In contrast, N, the cholineassociated water, orients H-up around 17 Å and changes to Hdown as z increases. Water molecules in both the hydrophobic region (HB) and near-bulk phase (NB) are weakly H-up oriented except for those at a small z distance ( 0) oriented water molecules in the vicinity of head groups (Figure 2d). For P, the phosphate-associated water, the populations of H-up and Hdown oriented molecules differ both in their size and average positions. H-up oriented water molecules are located on the bulk side of the head groups, while H-down ones sit on the lipid tail side of the head groups. The population size of the former is larger than that of the latter, and hence, the net orientation is H-up (Figure 2e). In contrast, for cholineassociated water N, the relative position of H-up and H-down populations is reversed; H-down oriented water molecules are located on the more bulk side than H-up oriented waters, as shown in Figure 2d. The integration of two populations indicates the existence of H-down oriented water molecules near choline groups (∼25 Å in Figure 2e). Results of MD simulation coincide with the experimental interpretation12 in that there is local structure in the vicinity of each phosphate and choline groups. The observed Im χ(2) spectrum shows double peaks on the positive (H-up) side. The dip separating the peaks is characteristic of a neutral zwitterionic POPC (not observed with negatively charged lipid). Moldal et al. have
glycero-3-phosphocholine) in a bilayer (100 lipids per leaflet). Lipids and water were simulated using the CHARMM C36 force field38 and the TIP3P model,39 respectively. Details are provided in the Supporting Information. Interfacial (|z| < 30 Å) and bulk (|z| ≥ 30 Å) regions were defined according to the electron density profile of water (Figure S1, Supporting Information). Waters at the interface were divided into five types in terms of their closest charged group in a POPC molecule (Figure 1a). The water molecules associated with a
Figure 1. (a) Molecular structure of the POPC head group (green: choline; blue: phosphate; pink: glycerol) and different types of interface water: water molecules associated with negatively charged phosphate (P, blue), positively charged choline (N, green), bridging phosphate and choline (P−N, cyan), and those in the hydrophobic region of the lipid (HB, pink). (b) Snapshot of the simulated system. Water molecules in the interface region are highlighted with a VDW representation using the same color scheme as that in (a) (dark blue: water molecules in the near-bulk region, NB).
negatively charged phosphate (P) and a positively charged choline (N) are defined as within 3.5 Å of the phosphorus or methyl carbon atoms, respectively. Water molecules that exist, but are not associated, within 3.5 Å are classified as P−N. Note that the distance 3.5 Å is the first minimum position of the corresponding radial distribution function (Figure S2, Supporting Information). Residual water molecules are classified as those in the hydrophobic region of POPC (HB) or in the nearbulk phase (NB) depending on their vertical position (|z| < 20 Å for the former and 20 ≤ |z| < 30 Å for the latter). Figure 1b illustrates the simulated system with the interfacial region highlighted. The calculated values of the area per lipid and bilayer thickness are 64 Å2 and 39 Å, respectively (Figure S1, Supporting Information), which agree with previously reported values.33,38,40 In Figure 2a, spatial arrangements for the different types of interfacial waters are shown in five snapshots taken every 20 ns 4344
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Figure 2. (a) Snapshots from the simulation representing spatial arrangement of different types of interface water (P, N, P−N, and HB). (b) Distributions of the orientation of water dipoles (the angle θ between the water dipole and bilayer normal) calculated for each type of interface water using the same snapshots as those in (a), where the color gradually changes from blue to red upon the dipole orientation changes from H-up to Hdown. (c) The average cosine of the angle θ as a function of the distance from the bilayer center for different types of interface water. (d) The populations of H-up (Pnegative, cos θ < 0) and H-down (Ppositive, cos θ > 0) oriented water molecules in the vicinity of the head group and (e) their sum (−Pnegative + Ppositive ).
lipid−water hydrogen bonds for water molecules in the hydrophobic region is markedly less than the phosphateassociated waters (P and P−N). Conversely, for the cholineassociated water (N), water−water hydrogen bonds dominate, and lipid−water hydrogen bonds are rare. The result recalls the picture of “clathrate-like” hydration for which the positively charged choline groups act as a hydrophobic apolar solute.17,18,21,22,28,34 To summarize, the negatively charged phosphate holds associated water molecules by strong hydrogen bonds, while the choline group enhances formation of water−water hydrogen bonds in the first hydration shell. A previous computational analysis has shown that water−water hydrogen bonds are weaker than lipid−water hydrogen bonds.29 On the other hand, the water molecules in the hydrophobic region (HB) are either free to hydrogen bond to each other or held by weak hydrogen bonds with the lipid polar groups. The observed water OH stretch band of the Im χ(2) spectrum depends on the hydrogen bond strength. In general, the stronger the hydrogen bond, the lower the OH stretch frequency. Mondal et al. have assigned the OH stretch bands of ∼3380, ∼3452, and ∼3581 cm−1 to the phosphate-associated water (P and P−N), the choline-associated one (N), and water in the hydrophobic region (HB), respectively.12 Our simulation results supports these assignments. The five types of interfacial waters also exhibit different dynamics. Figure 4a shows the residence correlation functions
attributed this dip to the contribution of the H-down orientation, based on a systematic comparison with related systems and a fitting analysis.12 Our simulation predicts the positive contribution (cos θ > 0) near the choline groups, which is much smaller than one estimated from the VSFG data. There are several possible reasons for this discrepancy. First, the relative amount of positive and negative contributions could be modulated depending on the definition of interface water (P, P−N, and N). Second, we have classified water orientation by the positive/negative sign of cos θ values. In reality, the subtle differences in water orientation and its interacting neighbors could change the optical response of the water molecule. To compare with the experimental data more rigorously, a direct calculation of the HD-VSFG spectrum is inevitable.41 Even so, the possible existence of local structure in the vicinity of each phosphate and choline groups is evident from the current simulation. The present results imply that the observed Im χ(2) spectrum reflects local water structures on the surface of the head groups rather than those in the whole interfacial region. The five types of interfacial waters differ in their hydrogen bond characteristics. Water molecules associated with phosphatidylcholine are known to form strong hydrogen bonds.22,28 We found that net H-up oriented water molecules (P, P−N, and HB) exclusively form hydrogen bonds with lipid molecules as the donor (Figure 3). Note that the average number of 4345
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Figure 3. Average number of hydrogen bonds between different types of interface water (P, N, P−N, and HB) and their surroundings found in the simulation. A geometric definition was used to define the hydrogen bond X−H···Y (X−Y distance < 3.5 Å and X−Y−H angle < 20°). Different color bars are used to distinguish different types of hydrogen bonds (orange: lipid as an acceptor; yellow: lipid as a donor; blue: water as an acceptor; cyan: water as a donor). Snapshots from the simulation are given for P, N, and HB.
Figure 4. (a) Residence correlation functions for the water molecules in the first solvent layer of the head groups calculated for the phosphate-associated (P and P−N) and the choline-associated (N) water molecules. The time correlation functions were calculated in the standard way.50 The first solvent layer was defined as the area within either 4.5 Å from the phosphorus atom or 6.0 Å from the nitrogen atom based on the respective radial distribution functions (Figure S2, Supporting Information). Residence times were estimated by fitting functions to two exponentials for all times (dashed line), A0 exp(−t/ A1) + A2 exp(−t/A3), with the amplitudes (A0 and A2) and time constants (A1 and A3) being 0.06, 0.94, 9.39, and 57.50 ps (P), −0.04, 1.16, 5.43, and 71.69 ps (P−N), and 0.46, 0.52, 11.43, and 43.63 ps (N). Water molecules that reside in the first solvent layer for more than 100 ps were excluded from the analysis. (b) Distributions of the exit time of water molecules from the first solvent layer. Only the water molecules that reside in the first solvent layer for more than 100 ps were considered. In the analysis (a,b), water molecules in a restricted area (|x| < 10 Å and |y| < 10 Å) were considered in order to avoid artifacts arising from the periodic boundary condition.
for water molecules in the first solvent layer of the head groups (see also Figure S4, Supporting Information). We found a faster decay of the correlation function of N, choline-associated water than that of the phosphate-associated water (P and P−N). The estimated residence times, obtained by exponential fits, are 57.5 ± 4.3, 71.7 ± 1.6, and 43.6 ± 3.9 for P, P−N, and N, respectively. We found that choline-associated water (N) also shows a fast component (11.4 ± 0.7 ps). Our calculated times are slightly longer than previous computational estimates (6− 40 ps).17,23,29,42 Recent studies using non-surface-selective vibrational techniques show biexponential dynamics in vibrational and orientational relaxation of water43−46 and show 10 ps as a lower limit for the water residence time on membrane surfaces.47 There is evidently rather rapid reorganization of a mosaic of different types of interface waters on the time scale of a few tens of ps. Interestingly, ∼10% of analyzed water molecules have an order of magnitude slower dynamics. Figure 4b shows the distributions of their exit times from the first solvent layer. The slower group is more associated with the phosphate-associated water (P and P−N) than the cholineassociated water (N). Note that the simulated dynamic properties depend on the water model. We used the TIP3P water model, which is known to give faster dynamics than experiments,48,49 and hence, the values we present could be considered a lower limit. This study demonstrates that a mosaic of water orientation structures exists on the surface of a neutral zwitterionic phospholipid bilayer associated with a rapid motion of water and the influence of different local chemical environments. The presence of site-specific local structures has a bearing on local
pH at lipid/water interfaces,51 water diffusion,42,52 and proton translocation on membrane surfaces.53,54 For instance, rapid reorganization of a mosaic of oriented water structures likely changes the local surface potential and could impact the protonation mechanism of membrane-associated proton transporters.55 The present results also have implications for the interpretation of Im χ(2) spectra. The consistency found between the present MD simulation and observed spectra implies that HD-VSFG detects local water structures on the surface of head groups at the water/lipid interface in a highly selective manner. Further study of combined MD simulation and VSFG spectroscopy could provide more molecular details at the membrane/water interface that are relevant for the many functions of biological membranes. 4346
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ASSOCIATED CONTENT
S Supporting Information *
Details of computations and trajectory analysis, including the radial distribution function, electron density profile, time course of the area per lipid and bilayer thickness, orientational order parameter, and residence correlation function. This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This research was supported in part by the RIKEN basic science interdisciplinary research projects (molecular systems research, iTHES, and integrated lipidology research), MEXT Grant-in-Aid for Scientific Research on Innovative Areas Grant Number 26119006 (to Y.S.), 25104005 (to T. T.), and MEXT/ JSPS KAKENHI Grant Number 26220807 (to Y.S.), 24245006 (to T. T.), Center of Innovation Program from Japan Science and Technology Agency, JST (to Y.S.). This research used computational resources of the HPCI system provided by the University of Tokyo through the HPCI System Research Project (Project ID: hp140157), the RIKEN Integrated Cluster of Clusters (RICC), and MEXT SPIRE Supercomputational Life Science (SCLS).
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