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Letter

Hydrogen Bonding Structure at Zwitterionic Lipid/Water Interface Tatsuya Ishiyama, Daichi Terada, and Akihiro Morita J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.5b02567 • Publication Date (Web): 29 Dec 2015 Downloaded from http://pubs.acs.org on December 30, 2015

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The Journal of Physical Chemistry Letters

Hydrogen Bonding Structure at Zwitterionic Lipid/Water Interface Tatsuya Ishiyama,∗,† Daichi Terada,† and Akihiro Morita∗,‡ Department of Applied Chemistry, Graduate School of Science and Engineering, University of Toyama, Toyama 930-8555, Japan, Department of Chemistry Graduate School of Science Tohoku University Sendai 980-8578, Japan , and Elements Strategy Initiative for Catalysts and Batteries (ESICB), Kyoto University, Kyoto 615-8520, Japan E-mail: [email protected]; [email protected]

∗

To whom correspondence should be addressed Department of Applied Chemistry, Graduate School of Science and Engineering, University of Toyama, Toyama 930-8555, Japan ‡ Department of Chemistry Graduate School of Science Tohoku University Sendai 980-8578, Japan ¶ Elements Strategy Initiative for Catalysts and Batteries (ESICB), Kyoto University, Kyoto 615-8520, Japan †

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Abstract

Interface structure of water/[3-palmitoyl-2-oleoyl-D-glycero-1-phosphatidylcholine] (POPC) lipid layer is investigated with molecular dynamics (MD) simulation by analyzing the recent heterodyne-detected vibrational sum frequency generation (HD VSFG) spectroscopy. The MD simulation clearly reproduced the experimental HD VSFG spectrum of imaginary susceptibility (Im[χ]), which exhibits two positive bands in the OH stretching vibrations of water. With the help of decomposition MD analysis, we found three kinds of interfacial water in relation to the HD VSFG spectrum. The low-frequency positive band is attributed to the water pointing toward the lipid side, whose orientation is influenced by negatively charged phosphate and positively charged choline of POPC. The high-frequency positive band is attributed to the water bonding with the carbonyl groups of the lipid. The gap between the two positive bands indicates the interfacial water pointing toward the bulk water phase in the vicinity of the choline groups.

TOC Graphic

Water

POPC vis IR

SFG

Keywords: Molecular Dynamics Simulation, Vibrational Sum Frequency Generation Spectroscopy, Water, Phosphatidylcholine Lipid, Molecular Structure of Interface 2 ACS Paragon Plus Environment

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Molecular structure of water adjacent to phospholipid membrane plays crucial roles in the functions of the lipid such as permeability of solutes 1 and the stability of the biomolecules like membrane proteins. 2 Since the amount of interfacial water is far more limited than that in the bulk water, it is a quite challenging issue to selectively measure the water structure at a biomembrane surface. 3 Vibrational sum frequency generation (VSFG) spectroscopy 4 is quite suitable for detecting the local water structure adjacent to the lipid layer. 5 Recent development of the phase-sensitive (PS) 6,7 or heterodyne-detected (HD) 8,9 VSFG spectroscopy has enabled us to distinguish polar orientation of water molecules at the interfacial region, by measuring the imaginary part of the second-order nonlinear susceptibility, Im[χ]. A related HD VSFG study on surfactant-water interfaces demonstrated that the flip-flop of interfacial water orientation is governed by the net charge of the surfactants. 10 In the case of zwitterionic phospholipid membranes, however, the influence on the water orientation should be more subtle as these lipid molecules carry no net charge. A key HD VSFG study at the water/phospholipid membrane interface was reported by Mondal et al. 11 They measured the HD VSFG spectra for the interface of water and [3-palmitoyl-2-oleoyl-D-glycero-1-phosphatidylcholine] (POPC), a typical zwitterionic phosphatidylcholine lipid. They observed two distinct positive bands in the Im[χ] spectrum; an intense band at around 3300 cm−1 and a weak band at around 3580 cm−1 . The interpretation of the two-band spectrum has been a challenging issue toward understanding of the water structure near the phospholipid membrane. Among the two bands, the former low-frequency band was assigned to the water molecules around the phosphate groups of POPC with forming strong hydrogen bonds. 11 Recent molecular dynamics (MD) simulations have succeeded in reproducing the low-frequency band, and some interpretations have been attained. 12,13 On the other hand, the assignment of the latter band is less obvious, though it was also experimentally observed in the conventional homodyne VSFG spectra 14,15 in addition to the recent HD VSFG spectra. 16 Just recently, Ohto et al. carried out an ab initio MD simulation of the lipid/water interface reproducing the high-frequency band. 17 The present study has



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succeeded in properly reproducing these bands by classical MD simulation, which greatly help clarifying the assignment of this band. This work provides a comprehensive and arguably reliable assignment of the HD VSFG spectra, and thereby reports a new insight into the H-bonding structure at water/POPC interface. A schematic picture of the POPC molecule is shown in Figure 1 (a), where the site names follow the CHARMM model: 18 N is the nitrogen of the choline group, P the phosphorus of the phosphate group, O22 (O32) the carbonyl oxygen of the oleoyl (palmitoyl) side, C21 (C31) the ester carbon, and C218 (C316) the terminal carbon. The force fields to generate present MD trajectories were TIP3P 19 for water and CHARMM36 20 for POPC with slight modification discussed below. The combination of TIP3P and CHARMM36 were widely used in previous related studies. 12,21 An MD cell contains 600 HOD and 20 POPC molecules with the dimensions of Lx × Ly × Lz = 24.45 ˚ A × 24.45 ˚ A × 150.0 ˚ A. In the preparation of initial conformation, the water molecules form a slab with a thickness of about 33.3 ˚ A along the z axis, and 10 POPC molecules are placed on each side of the slab surface. After equilibration, the POPC form a stable monolayer on each side of the slab with the surface ˚2 per lipid, consistent to the previous experimental settings. 11 Then the density of 59.78 A statistical sampling of surface structure and VSFG spectra was taken for 4 ns in total. The detailed settings and the computational methodologies are summarized in Section S1 of the Supporting Information (SI). In the VSFG spectroscopy, the second-order nonlinear susceptibility χ consists of the vibrationally resonant and non-resonant terms, χ = χres +χnonres , and the former is represented with the following time correlation function 22,23

χres pqr

iωIR = kB T

∫

∞

dt exp(iωIR t) 0

⟨ ∑∑ i

⟩ αi,pq (t)µj,r (0) ,

(1)

j

where ωIR is the angular frequency of the infrared light. kB and T are the Boltzmann constant and temperature, respectively. αi (t) and µi (t) denote the polarizability tensor and 4 ACS Paragon Plus Environment

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dipole moment vector of i-th molecule at time t. The suffixes p, q, r stand for the x ∼ z in the space-fixed coordinates to denote the tensor elements. We discuss the (pqr) = (xxz) element of the nonlinear susceptibility, χxxz , in this paper. This element corresponds to the SFG measurement of SSP polarization, consisting of S-polarized SFG, S-polarized visible and P-polarized infrared lights. In relation to the heterodyne-detected spectroscopy, we deal with the imaginary part, Im[χ] = Im[χres ], where the nonresonant term is safely omitted as it is a real quantity. The calculation of α and µ in Eq. (1) was carried out with the charge response kernel model of water, 24 where the instantaneous polarization takes account of the local field effect in the self-consistent manner. The details of the calculation were also given in Section 1 of the SI. Since the present study aims at elucidating the structure of interfacial water, we introduce a classification of the interfacial water molecules in terms of the adjacent functional groups of POPC in Figure 1 (a). The water molecules adjacent to the choline (red circle) are classified with “N”, those to the phosphate (blue circle) with “P”, and those to the ester oxygens (green circles) with “O”. The criteria of adjacent molecules are defined on the basis of the radial distribution functions in Section S3 of the SI. The whole classification scheme of interfacial water is summarized in Figure 1 (b). This scheme includes the overlapped regions such as NP, PO, NO, and NPO, which indicate the water molecules adjacent to more than one polar group simultaneously. These overlapped regions indicate either situation that the adjacent polar groups belong to the same POPC molecule or that they belong to different POPC molecules. The water molecules that are not adjacent to either of the above groups are denoted with “Others”. These classification of water at the water/POPC interface will be used in later analysis of VSFG spectra and MD simulation. Next, we analyze the spectral bands by using the classification of water in Figure 1 (b). For convenience of spectral decomposition, we introduce the “self-part” spectrum by

χself pqr

iωIR = kB T

∫

∞

dt exp(iωIR t) 0

⟨ ∑

⟩ αi,pq (t)µi,r (0) .

i


(2)


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This formula is an approximation of Eq. (1) by neglecting the cross terms (i ̸= j) in the summation of Eq. (1). Equation (2) is a good approximation of Eq. (1) if the cross terms are insignificant to the qualitative features of the spectrum, and we confirmed that this is the case for the water/POPC spectrum in the SI. Equation (2) allows for straightforward decomposition of the Im[χ] spectrum into molecules, since χself pqr is represented with the sum of the i-th molecular contribution. The decomposition of Eq. (2) is carried out by classifying the molecule i into each category at t = 0 of the time correlation function. This classification is effectively well defined since the decay of the time correlation function is faster than the structural change. The VSFG spectra reported in this letter focus on χself pqr with its decomposition analysis. Figure 2 summarizes the Im[χ] spectra reported by previous experimental and theoretical studies for the phosphatidylcholine lipid/water interfaces. Though these studies treat different phosphatidylcholine species in acyl chains, their HD VSFG spectra are shown to be quite analogous by experiment, 11 indicating essentially common structure of interfacial water. Both the experimental spectra reported by Mondal et al. 11 (red line) and by Hua et al. 16 (black open circles) commonly exhibit the two-band structure of the Im[χ] spectra, consisting of the intense positive band near 3300 cm−1 and the minor positive band near 3580 cm−1 in the former or 3530 cm−1 in the latter. The present calculated Im[χ] spectrum (thick black line in Figure 2) well reproduces these features. We also note in passing that the original CHARMM36 FF did not reproduce the apparent minor high-frequency band, as other previous theoretical studies. We investigated the reason of missing band, and elucidated it because the polarity of the carbonyl groups in the lipid is somewhat overestimated by CHARMM36 FF. The partial charges of CHARMM36 implicitly take account of the solvation effects, while the carbonyl groups of POPC are rather located in the hydrophobic environment of the membrane. Thus we introduced the modified partial charges of the carbonyl groups in Table 1, called modified CHARMM36 (mCHARMM36), by ab initio and density functional calculations in the present paper. We found that this 6 ACS Paragon Plus Environment

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modification little alters the structure of lipid membrane, while it influences the vibrational spectrum of water in the lipid. The details of the argument are described in Section S2 of the SI. The decomposed Im[χ] spectra with TIP3P/mCHARMM36 FF are shown in Figure 3. This analysis elucidates the fundamental features of the experimental HD VSFG spectrum of Im[χ], i.e. two positive bands and a gap in between. The low-frequency positive band about 3300 cm−1 mainly originates from the NP water molecules (purple dash-dot line), which are adjacent to both the polar choline and phosphate groups of POPC molecules. The second feature is that the high-frequency band at about 3530 cm−1 comes mainly from the NPO water molecules, which contain weakly hydrogen-bonded OH moieties with the carbonyl oxygens. The third feature of Figure 3 is that the N water (red line) contributes negatively to the higher frequency region than 3400 cm−1 . This result is understood since the water molecules around the choline group direct their protons toward the water phase because of the net positive charge of the choline group. 25 Since the interaction between the choline group and water is not as strong as the direct hydrogen bonding interaction, the red shift of the frequency is expected to be modest. These types of water molecules at the water/lipid interface are schematically illustrated in Figure 4 (c). In relation to the above spectral assignments, we further explore the structure of the interfacial water near the lipid. Figure 4 (a) shows the number density profiles of the water oxygen and some representative sites of POPC along the surface normal direction zˆ, where the origin zˆ = 0 is set at the Gibbs dividing surface (G.D.S.) of water, 26 and zˆ < 0 (ˆ z > 0) indicates the water (lipid) side. The density profile of water, denoted with the black line in Panel (a), is apparently distorted from that of the air/water interface. The 10-90 thickness δ10−90 is estimated to be 9.96 ˚ A, which is larger than that at the air/water interface about ∼3˚ A. 27 The water density penetrates into the region of hydrophilic head groups of POPC from zˆ = 0 ˚ A to 10 ˚ A. Regarding the density profiles of the head groups, the site N (choline) has the maximum peak near the G.D.S., and the site P (phosphate) has the peak slightly 7 ACS Paragon Plus Environment


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in the lipid side. This segregation indicates an important consequence that the POPC membrane forms an electric double layer between the positive choline and the negative phosphate near the interface. 28 The electric double layer in the phospholipid zwitterionic membrane significantly orients the water molecules in between, and thus enhances the Im[χ] spectrum of water. This mechanism is manifested in the large positive contribution of the NP molecules in Figure 3. The spatial distribution of interfacial water molecules is further clarified through their density and orientation. We examine the profile of n(ˆ z )⟨cos θ(ˆ z )⟩ of water, the product of the number density n and cosine of the OH tilt angle θ, as a function of zˆ. This quantity is readily calculated from MD trajectories and is used as a convenient index of SFG activity, 29 because the SFG signal is governed by the number density of chromophores and its average orientation. The sign of n⟨cos θ⟩ also well corresponds to the sign of Im[χ], which reflects the polar orientation of the transition dipole. We plot the profile of n⟨cos θ⟩ for each class of interfacial water in Figure 4 (b). The plot of n⟨cos θ⟩ clearly supports the above assignment on the Im[χ] spectrum, in the following. Figure 4 (b) shows a large positive band of the NP water in −5 ˚ A < zˆ < 2 ˚ A. This band is located between the positive choline and the negative phosphate layers (see their density profiles in Figure 4 (a)), and the orientation of the NP water is largely influenced by the electric double layer. The large positive band of n⟨cos θ⟩ for the NP water is consistent to Figure 3, indicating that the NP water gives a major contribution to the positive Im[χ] spectrum. We furthermore examined the NP water whether they bridge the N and P groups of same POPC molecules or different POPC molecules. The probability ratio of the former to the latter turned out to be about 1 : 2, indicating that the NP water molecules often bridge the head groups of different POPC molecules, as shown in Figure 4 (c). We also notice that both the P and NPO water molecules show positive bands of n⟨cos θ⟩, which are influenced by the phosphate group of POPC. The NPO band is located more in the lipid side (larger zˆ) than the P molecules, implying that the NPO water molecules are located in


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more hydrophobic environment than the P water (see also Figure 4 (c)). These P and NPO water also give the lower and the higher positive amplitudes to Im[χ] in Figure 3. Another feature in Figure 4 (b) is a negative band of n⟨cos θ⟩ for the N water in −10 ˚ A < zˆ < −3 ˚ A. This type of N water is located near the choline group of POPC (see Figure 4 (a) and (c)), arguably contributing negatively in the Im[χ] spectrum. All these features in Figure 4 (b) are consistent to the assignment of the Im[χ] spectrum. In the following, we discuss the present results in comparison with previous experimental and calculated works in Figure 2. The experimental study by Mondal et al. 11 (red line in Figure 2) conducted their Gaussian fitting analysis, and thus concluded that the low- and high-frequency positive bands of Im[χ] are attributed to the OH moieties bonding with the phosphate groups and those in a hydrophobic region near the carbonyl group, respectively. They also argued that the negative Im[χ] component near 3500 cm−1 originates from the water interacting with the choline groups. The calculated results of our work are mostly consistent to their assignments, and further revealed that the high-frequency positive peak is attributed to the OH moieties bonding with the carbonyl groups of POPC, rather than the water in the interior of the hydrophobic lipid membranes. 5,15 The classical MD simulation by Nagata and Mukamel 12 (blue line in Figure 2) predicted the double peaked structure of Im[χ] at about 3300 cm−1 and 3500 cm−1 . They assigned the former peak to the OH stretching vibration near the bulk water and the latter peak to the water with hydrogen bonds to the polar head groups. We notice that their calculated spectrum showed comparable peak amplitudes, whereas the experiment shows much smaller amplitude of the high-frequency band than the low-frequency one. It is rather questionable that the calculated high-frequency band corresponds to the experimental minor band. Roy et al. 13 (orange line in Figure 2) reported the positive band of Im[χ] spectrum peaked at 3300 cm−1 . Their assignment of the main peak is same as ours, while the high-frequency component is almost missing in their calculated spectrum. Recently, Ohto et al. 17 (green line in Figure 2) carried out ab initio MD simulation to calculate Im[χ] spectrum at the 9 ACS Paragon Plus Environment


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lipid/water interface, and also reported the double-band structure. Their assignment of the high-frequency band is same as ours, while they attributed the low-frequency band to the water molecules influenced by the carbonyl groups rather than those between the phosphate and the choline groups. Their calculation did not found the negative Im[χ] component around the choline group, which is inconsistent to Mondal et al. 11 and the present study. Currently ab initio MD simulation requires much more computational cost than classical simulation, and hence system size and simulation time to equilibrate the system are often very limited. Further efforts to augment the system size and simulation time of ab initio MD simulation may be needed to reach a definite conclusion. In summary, we carried out a classical MD simulation of water/POPC interface with TIP3P/ mCHARMM36 FF. A slight modification of CHARM36 FF, a reduction of polarity in the carbonyl group of the lipid, is required to reproduce the higher frequency peak of Im[χ] spectrum. The present study concluded that the lower frequency positive band at about 3300 cm−1 is attributed to the water molecules influenced by the electrostatic field between phosphate and choline groups, and thus pointing their OH toward the lipid side. The higher frequency peak at 3530 cm−1 is assigned to the stretching vibration of OH bonding with the carbonyl group in the lipid. The water interacting with the choline group pointing toward the water side is also found. The present findings provide a quite consistent interpretation of the HD VSFG spectra to the structural analysis of membrane by MD and previous HD SFG experiments. Reliable knowledge on the spectra and structure will become a physical basis for understanding stability and functions of solutes and membrane proteins at lipid/water interfaces in future experimental and theoretical studies.

Acknowledgement We are grateful to Drs. Tahei Tahara and Satoshi Nihonyanagi for stimulating discussion. The MD calculations were performed using the supercomputers at Research Center for Computational Science, Okazaki, Japan. This work was supported by the Grants-in-Aid (Nos. 10 ACS Paragon Plus Environment

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25410001, 25104003) by the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan.

Supporting Information Available Supporting Information Available: Details of computational methodology, modification of carbonyl charges, and radial distribution functions of water and polar sites of lipid.

This

material is available free of charge via the Internet at http://pubs.acs.org/.

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(8) Yamaguchi, S.; Tahara, T. Heterodyne-Detected Electronic Sum Frequency Generation: Up versus Down Alignment of Interfacial Molecules. J. Chem. Phys. 2008, 129, 101102. (9) Nihonyanagi, S.; Mondal, J. A.; Yamaguchi, S.; Tahara, T. Structure and Dynamics of Interfacial Water studied by Heterodyne-Detected Vibrational Sum-Frequency Generation. Annu. Rev. Phys. Chem. 2013, 64, 579–603. (10) Nihonyanagi, S.; Yamaguchi, S.; Tahara, T. Direct Evidence for Orientational FlipFlop of Water Molecules at Charged Interfaces: a Heterodyne-Detected Vibrational Sum Frequency Generation Study. J. Chem. Phys. 2009, 130, 204704. (11) Mondal, J. A.; Nihonyanagi, S.; Yamaguchi, S.; Tahara, T. Three Distinct Water Structures at a Zwitterionic Lipid/Water Interface Revealed by Heterodyne-Detected Vibrational Sum Frequency Generation. J. Am. Chem. Soc. 2012, 134, 7842–7850. (12) Nagata, Y.; Mukamel, S. Vibrational Sum-Frequency Generation Spectroscopy at the Water/Lipid Interface: Molecular Dynamics Simulation Study. J. Am. Chem. Soc. 2010, 132, 6434–6442. (13) Roy, S.; Gruenbaum, S. M.; Skinner, J. L. Theoretical Vibrational Sum-Frequency Generation Spectroscopy of Water near Lipid and Surfactant Monolayer Interfaces. J. Chem. Phys. 2014, 141, 18C502. (14) Watry, M. R.; Tarbuk, T. L.; Richmond, G. L. Vibrational Sum-Frequency Studies of a Series of Phospholipid Monolayers and the Associated Water Structure at the Vapor/Water Interface. J. Phys. Chem. B 2003, 107, 512–518. (15) Ma, G.; Chen, X.; Allen, H. C. Dangling OD Confined in a Langmuir Monolayer. J. Am. Chem. Soc. 2007, 129, 14053–14057. (16) Hua, W.; Verreault, D.; Allen, H. Solvation of Calcium-Phosphate Headgroup Complex at the DPPC/Aqueous Interface. ChemPhysChem 2015, 16, 3910–3915. 12 ACS Paragon Plus Environment

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(17) Ohto, T.; Backus, E.; Hsieh, C.; Sulpizi, M.; Bonn, M.; Nagata, Y. Lipid Carbonyl Groups Terminate the Hydrogen-Bond Network of Membrane-Bound Water. J. Phys. Chem. Lett. 2015, 6, 4499–4503. (18) Feller, S. E.; MacKerell, Jr., A. D. An Improved Empirical Potential Energy Function for Molecular Simulations of Phospholipids. J. Phys. Chem. B 2000, 104, 7510–7515. (19) Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of Simple Potential Functions for Simulating Liquid Water. J. Chem. Phys. 1983, 79, 926–935. (20) Klauda, J. B.; Venable, R. M.; Freites, J. A.; amd D. J. Tobias, J. W. O. C.; MondragonRamirez, C.; Vorobyov, I.; MacKerell Jr., A. D.; Pastor, R. W. Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types. J. Phys. Chem. B 2010, 114, 7830–7843. (21) Re, S.; Nishima, W.; Tahara, T.; Sugita, Y. Mosaic of Water Orientation Structures at a Neutral Zwitterionic Lipid/Water Interface Revealed by Molecular Dynamics Simulations. J. Phys. Chem. Lett. 2014, 5, 4343–4348. (22) Morita, A.; Ishiyama, T. Recent Progress in Theoretical Analysis of Vibrational Sum Frequency Generation Spectroscopy. Phys. Chem. Chem. Phys. 2008, 10, 5801–5816. (23) Ishiyama, T.; Imamura, T.; Morita, A. Theoretical Studies of Structures and Vibrational Sum Frequency Generation Spectra at Aqueous Interfaces. Chem. Rev. 2014, 114, 8447–8470. (24) Ishiyama, T.; Morita, A. Analysis of Anisotropic Local Field in Sum Frequency Generation Spectroscopy with the Charge Response Kernel Water Model. J. Chem. Phys. 2009, 131, 244714.



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(25) Lopez, C. F.; Nielsen, S. O.; Klein, M. L.; Moore, P. B. Hydrogen Bonding Structure and Dynamics of Water at the Dimyristoylphosphatidylcholine Lipid Bilayer Surface from a Molecular Dynamics Simulation. J. Phys. Chem. B 2004, 108, 6603–6610. (26) Adamson, A. W.; Gast, A. P. Physical Chemistry of Surfaces, 6th ed.; Wiley: New York, 1997. (27) Garrett, B. C.; Schenter, G. K.; Morita, A. Molecular Simulations of the Transport of Molecules across the Liquid/Vapor Interface of Water. Chem. Rev. 2006, 106, 1355– 1374. (28) Ishiyama, T.; Morita, A. Molecular Dynamics Study of Gas-Liquid Aqueous Sodium Halide Interfaces. I. Flexible and Polarizable Molecular Modeling and Interfacial Properties. J. Phys. Chem. C 2007, 111, 721–737. (29) Ishihara, T.; Ishiyama, T.; Morita, A. Surface Structure of Methanol/Water Solutions via Sum-Frequency Orientational Analysis and Molecular Dynamics Simulation. J. Phys. Chem. C 2015, 119, 9879–9889.


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Table 1: Partial charges of the carbonyl sites for the CHARMM36 FF and for the modified CHARMM36 (mCHARMM36) FF.

CHARMM36 mCHARMM36

O22(O32) −0.63 −0.53

C21(C31) 0.9 0.8



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(C218)

(a) (O22) O

(C21)

-

O O P

O

(O21)

O O

(C316)

(C31)

+

N

(b)

O

O

(O31)

(O32)

Others

P PO

NP NPO

N

NO

O

Figure 1: (a) Schematic of a POPC molecule. The colored circles show the categorized polar sites used in the present analysis. (b) Classification scheme of water near the polar head groups. Water molecules adjacent to the choline (red) are classified with N, those adjacent to both choline (red) and phosphate (blue) are classified with NP, etc. (see the text)


Page 17 of 19

Mondal et al. (exptl, POPC/HOD) Hua et al. (exptl, DPPC/H2O) Nagata and Mukamel (calcd, DMPC/H2O) Roy et al. (calcd, POPC/HOD) Ohto et al. (calcd, DPPC/HOD) The present result (calcd, POPC/HOD)

Amplitude (arb.unit)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


1.2 1 0.8 0.6 0.4 0.2 0

3200

3400

Frequency

3600

(cm¡1 )

Figure 2: Comparison of experimental and calculated spectra for Im[χ] spectra of phosphatidylcholine lipid/water interfaces. The red line and black circles are experimental results, 11,16 the thick black line is the present result, and the others are calculated ones. 12,13,17 The species of the interfacial systems are shown in the legend. Each spectrum is normalized with its maximum.


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Amplitude (arb.unit)


Page 18 of 19

N P O NP PO NO NPO Others

0.2

0.1

0 3200

3400

Frequency

3600

(cm¡1 )

Figure 3: The site-decomposition spectra of Im[χ] for water at POPC/water interface, where TIP3P/mCHARMM36 FF is used for calculation. For the decomposition scheme, see the text.


Page 19 of 19

Number density (mol/L)

10 N P

Water

O22 O32 60 C218 C316 40

5

20

(a)

(mol/L)

0

6

-10

0

10

PO NO NPO Others

N P O NP

4 2

0

20

(b)

OH

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


0 -2

-10

0

10

z^ (º A)

(c) Lipid

Glycerol Oxygen

NPO

O

(H-bonding water with O) O

Phosphate O

Water

O

Phosphate Choline

Choline

NP (H-bonding water with P and N) N (Weekly interacting water with N)

Figure 4: (a) Number density profiles of the water oxygen (black) and some representative sites of POPC molecule as a function of the interfacial depth zˆ. The site names of POPC refer to those of the CHARMM model 18 (see Figure 1 (a)). Note the right ordinate indicates the scale for water while the left ordinate for the other POPC sites. (b) n · ⟨cos θOH ⟩ profiles of water. The simulations were conducted with TIP3P/mCHARMM36 FF. (c) A schematic picture of water molecules classified as N, NP, and NPO components. 19 ACS Paragon Plus Environment

Water Interface - The

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