Unveiling the Amphiphilic Nature of TMAO by ... - ACS Publications

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Unveiling the Amphiphilic Nature of TMAO by Vibrational Sum Frequency Generation Spectroscopy Tatsuhiko Ohto,*,† Ellen H. G. Backus,*,‡ Wataru Mizukami,§ Johannes Hunger,‡ Mischa Bonn,‡ and Yuki Nagata‡ †

Graduate School of Engineering Science, Osaka University, 1-3 Machikaneyama, Toyonaka, Osaka 560-8531, Japan Max Planck Institute for Polymer Research, Ackermannweg 10, 55128, Mainz, Germany § Department of Energy and Material Sciences, Faculty of Engineering Sciences, Kyushu University, 6-1 Kasuga-Park, Fukuoka, 816-8580, Japan ‡

S Supporting Information *

ABSTRACT: By combining heterodyne-detected sum-frequency generation (SFG) spectroscopy, ab initio molecular dynamics (AIMD) simulation, and a post-vibrational selfconsistent field (VSCF) approach, we reveal the orientation and surface activity of the amphiphile trimethylamine-N-oxide (TMAO) at the water/air interface. Both measured and simulated C−H stretch SFG spectra show a strong negative and a weak positive peak. We attribute these peaks to the symmetric stretch mode/Fermi resonance and antisymmetric in-plane mode of the methyl group, respectively, based on the post-VSCF calculation. These positive and negative features evidence that the methyl groups of TMAO are oriented preferentially toward the air phase. Furthermore, we explore the effects of TMAO on the interfacial water structure. The O−H stretch SFG spectra manifest that the hydrogen bond network of the aqueous TMAO-solution/air interface is similar to that of the amine-N-oxide (AO) surfactant/water interface. This demonstrates that, irrespective of the alkyl chain length, the AO groups have a similar impact on the hydrogen bond network of the interfacial water. In contrast, we find that adding TMAO to water makes the orientation of the free O−H groups of the interfacial water molecules more parallel to the surface normal. Invariance of the free O−H peak amplitude despite the enhanced orientation of the topmost water layer illustrates that TMAO is embedded in the topmost water layer, manifesting the clear contrast of the hydrophobic methyl group and the hydrophilic AO group of TMAO.

I. INTRODUCTION Trimethylamine-N-oxide (TMAO) is an osmolyte, which is composed of the hydrophilic amine-oxide (N−OTMAO) group and hydrophobic methyl groups (see Figure 1). Although TMAO is often used to counteract the osmotic stress due to urea1−6 owing to its stabilizing effect on the secondary structure of proteins,7,8 the detailed mechanism of protein stabilization due to TMAO is not yet known. Since the protein secondary structure is formed by hydrogen bonds between amide groups, electrostatic interactions between positively and negatively charged protein side chains, water-mediated interactions between residues, and hydrophobic forces driven by the hydrophobic side chains of proteins,9−14 it is essential to understand the molecular-level insight into the TMAO−protein interactions in an aqueous environment. In particular, a fundamental question arising here is how TMAO interacts with the hydrophobic/hydrophilic residues of a protein in an aqueous solution. Assessing the molecular conformation of TMAO near a model hydrophobic/hydrophilic interface and the amphiphilic nature of TMAO is therefore of importance for © XXXX American Chemical Society

specifying the interaction sites of TMAO with hydrophobic/ hydrophilic residues. A powerful tool to probe the interfacial molecular conformation of a solute at an aqueous interface is sumfrequency generation (SFG) spectroscopy.15−24 SFG probes the second-order nonlinear optical response, which is forbidden in centrosymmetric media and thus provides interfacial selectivity.25,26 The homodyne-detected SFG signal at ssp 2 (2),R polarization, |χ(2) ssp | , consists of a resonant contribution χssp and a nonresonant contribution χ(2),NR as ssp (2) 2 (2), R (2), NR 2 |χssp | = |χssp + χssp |

(1)

The signs of the imaginary part of the resonant signals, (2),R Im(χssp ) reflect the orientation of the transition dipole moments. To identify the molecular orientation of TMAO, Sagle et al. measured the homodyne-detected SFG signal in the Received: May 13, 2016 Revised: July 12, 2016

A

DOI: 10.1021/acs.jpcc.6b04852 J. Phys. Chem. C XXXX, XXX, XXX−XXX

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The Journal of Physical Chemistry C

simulation, and confirm that the methyl group points up toward the vapor phase. Subsequently, we compare the O−H stretch SFG spectra at the TMAO-solution/air, AO-surfactant/water, and water/air interfaces. The TMAO and AO-surfactant provide similar O−H stretch SFG spectra of water except the positive free O−H stretch band, indicating that the interfacial water structures are determined by the AO group. We also point out the orientation of the free O−H groups becomes more parallel to the surface normal by adding TMAO. The organization of this paper is as follows. In Section II, the experimental procedure is provided, while Section III describes the post-VSCF calculation and AIMD simulation protocols. In Section IV, we discuss the peak assignment of the C−H stretch mode of TMAO and then compare the simulated SFG spectra of the C−H stretch mode with the experimental data. Furthermore, we present the O−H stretch SFG spectra at the water/air interface with TMAO and discuss the effects of TMAO on orientation of the interfacial water molecules. Conclusions are given in Section V.

Figure 1. (Left) Chemical structure of TMAO. (Right) Snapshot of the simulated aqueous TMAO-solution/air interface. The hydrogen, carbon, nitrogen, and oxygen atoms are represented by the white, green, blue, and red spheres, respectively. TMAO and water molecules are depicted in dense and light colors, respectively. The dashed lines are the unit cell boundaries.

frequency range of 2800−3800 cm−1 at the aqueous TMAOsolution/air interface.27 The frequency range used in that study includes both the C−H stretch mode of the methyl groups of TMAO and the O−H stretch mode of water. Using the maximum entropy method (MEM) to extract Im(χ(2),R ssp ) from 2 experimental |χ(2) ssp | spectra, they concluded that the methyl groups of TMAO point down to the bulk, suggesting that the methyl group of TMAO is not hydrophobic.27 Note that the MEM method can determine the sign of peaks in the Im(χ(2),R ssp ) by maximizing the noise of the spectra using the sign of a reference peak, such as the water’s free O−H band at ∼3700 cm −1.28 Similar conclusions have been drawn from a thermodynamics study.29 In contrast, a recent heterodynedetected SFG study by the Mondal group, which can access Im(χ(2),R ssp ) without fitting, revealed that the methyl group points up to the air.30,31 Nevertheless, based on the insensitivity of the free O−H stretch SFG peak to the presence of TMAO, it was concluded that TMAO is absent in the topmost water layer, implying that the TMAO methyl group is rather hydrophilic.31 These findings seem, however, at odds with several studies on bulk TMAO solutions using infrared (IR) spectroscopy and ab initio molecular dynamics (AIMD). These studies demonstrate that the OTMAO atom of TMAO has the ability to form strong hydrogen bonds with water, slowing down the rotational motion of water hydrogen bonded to the OTMAO atom dramatically, whereas the methyl group of TMAO has limited effects on the rotational motion of water.32,33 The moderate effect of the TMAO methyl group on the water rotational motion can be rationalized by excluded volume effects of TMAO in the angular jump model.34 This indicates that the TMAO methyl group acts as a hydrophobic moiety in water. To examine the amphiphilic nature of TMAO, we combine the heterodyne-detected SFG measurement, AIMD simulation, and post-vibrational self-consistent field (post-VSCF) calculation. Through the post-VSCF calculation of TMAO, we identify the frequencies of the symmetric and antisymmetric C−H stretch modes as well as the Fermi resonance. The postVSCF calculation based on the second-order vibrational quasidegenerate perturbation (VQDPT2)35 level of theory can predict the vibrational frequencies of TMAO within the error of 20 cm−1, which allows us to uniquely identify the vibrational modes. Based on the post-VSCF peak assignment, we interpret the C−H stretch SFG spectra of TMAO at the water/air interface obtained experimentally as well as from AIMD

II. EXPERIMENTAL PROCEDURES II-A. Sum Frequency Generation Experiments. For the heterodyne-detected SFG experiments part of the laser output (Spitfire Ace Spectra-Physics, 5 W, ∼40 fs, 1 kHz, 800 nm) is frequency converted in a TOPAS (Light Conversion) resulting in ∼5 μJ infrared (IR) pulses around 3000 nm. Another part of the laser output passes through an etalon and functions as the up-conversion pulse in the SFG experiment and has an intensity of ∼6 μJ with 25 cm−1 bandwidth. The visible and IR beams are focused and overlapped under grazing incidence on a gold mirror to generate the local oscillator. Subsequently, the beams are refocused by a curved mirror with a focal length of 50 mm onto the sample with an angle of incidence of roughly 45° and 40° with respect to the surface normal for the IR and visible, respectively. The local oscillator was delayed by a 1 mm fused silica plate. The SFG signal was detected with a spectrometer (Acton SP2300, Princeton Instruments) and EMCCD camera (Newton, Andor Technology). The data analysis was performed as described in ref 36 and z-cut quartz has been used as reference. A displacement sensor with a resolution of 200 nm (LK-G85, Keyence) verifies that the sample and reference are placed at the same height. The data were phase-corrected with D2O to correct for a potential small tilt in the position of the quartz reference and for evaporation of water during the acquisition time. As the phase of D2O is 170° instead of 180°,37 we corrected our data for this additional 10° phase shift. II−B. Fresnel Factor Correction. To allow comparison with simulated SFG spectra, the experimental data have to be corrected for the Fresnel factors, which are calculated following ref 38. We used the refractive index of water or water/TMAO for the interfacial layer. 39 For the correction of the dodecyldimethyl-N-amine oxide (DDAO) data (see Figure 3), the interfacial refractive index has been calculated following ref 38. As the refractive index of water/TMAO-solutions has not been previously reported in the literature, we measured the IR transmission spectrum of the solutions used in the SFG experiments between two CaF2 windows without a spacer. We observed a small red shift in the O−H stretch vibration for the TMAO-solutions compared to water without dissolved TMAO. Subsequently, we used the Kramers−Kronig relation to obtain the real part of the refractive index. As the thickness of our B


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contained 80 H2O and four TMAO molecules for the TMAOsolution/air interface (2.78 m) and 80 H2O for the water/air interface. Periodic boundary conditions were used for the x-, y-, and z-directions. Previous AIMD simulations for TMAO in water show that the system composed of a TMAO molecule with 100 water molecules is adequate for describing the solvation shell dynamics around TMAO and vibrational spectra of water around TMAO.33,57 Furthermore, it has been reported that the orientation of TMAO is essentially independent of the TMAO concentration,58 which also suggests that the system size used here is sufficiently large to compare the current simulation with the experiment. For the simulations of the TMAO-solution, through the 2 ns force field MD simulations with the SPC/Fw water model59 and Kast’s TMAO model,60 we obtained four different initial coordinates. Using these four configurations of the aqueous TMAO-solution, the 10 ps AIMD simulations were conducted at 320 K in the NVT ensemble for equilibrating the systems. We used the technique of canonical sampling through velocity rescaling to control the temperature. Sequential 32 ps AIMD runs were performed for sampling the AIMD trajectories, and a total of 32 ps × 4 = 128 ps AIMD trajectories were used for analyzing the data and computing SFG spectra. For the water/ air interface, we prepared one sample and performed a 20 ps AIMD run for equilibrating the system. Subsequently, an 80 ps AIMD trajectory was used for analyzing the data. Information on the convergences of the C−H stretch SFG signal and the orientation of TMAO is given in the Supporting Information, SI. For both AIMD simulations, the time step for integrating the equation of motion was set to 0.4 fs. The force field MD simulation and AIMD simulation with the QUICKSTEP method61 were performed using the CP2K code.62 III−C. C−H Stretch SFG Signal of TMAO: Dipole Moment-Polarizability Correlation Function Approach. The resonant part of the SFG signal can be calculated from the time correlation function of the dipole moment (μ) and polarizability (α) as

sample is unknown, we scaled and offset the data in the following way: First, we scaled (imaginary and real part) and offset (real part) the pure water spectrum to the literature value from Bertie et al.40 Subsequently we scaled the refractive index of the isotopically diluted water (H2O:D2O = 1:3) such that the area under the OH stretch vibration in the imaginary part of the spectrum is 25% of that of pure water. For the TMAO-solution, we scaled the refractive index such that the area under the imaginary part of the O−H stretch vibration is equal to 0.82 times the area for the comparable water sample without TMAO based on the 18% reduced water concentration of a 3 m TMAO solution compared to pure water.41 The real parts of the refractive index of all samples are offset by the same value as used for pure water. II−C. Sample Preparation. TMAO-dihydrate (SigmaAldrich) was dissolved in pure Millipore water or isotopic diluted water (D2O (Cambridge Isotope Laboratories):H2O = 3:1) up to a concentration of 3 mol/kg solvent. The two water molecules in the dihydrate crystal are assumed to become solvent upon dissolution in water.

III. SIMULATION PROTOCOLS III-A. Gas-Phase Vibrational Frequency Calculation with Post-VSCF Technique. To assign the C−H stretch modes of TMAO, we calculated the vibrational frequencies of TMAO. The vibrational frequency calculation was made at a post-VSCF theory, i.e., at the VQDPT2 level of theory35 using the SINDO program.42 In the post-VSCF technique, the calculated vibrational frequency includes the effects of the potential anharmonicity and the mode couplings on the vibrational frequencies, beyond the vibrational frequency calculated based on the harmonic approximation. We used the thresholds for the quasi-degenerate states of VQDPT2 given in ref 35. We generated a semi quartic force field (QFF) for the vibrational normal modes of a TMAO molecule, based on which we calculated the vibrational frequency. We used 11 Gauss-Hermite functions (harmonic oscillators) per mode in the anharmonic calculations. The QFF consists of the harmonic, cubic, and quartic terms. The harmonic terms of QFF were computed at the CCSD(T)(F12*)43/cc-pVDZF1244 level of theory using the MOLPRO package.45,46 The cubic and quartic terms were calculated numerically at the B3LYP/6-311+G** level of theory by Gaussian 09.47 The step sizes of the grid were determined by using qi = δy ℏ/ωi , where ωi was a harmonic frequency of mode i and δy was set to 0.5.48 We also calculated the frequencies using the Hessian calculation, for comparing the post-VSCF data with the Hessian calculation. We used a scaling factor of 0.9639 for the vibrational frequencies obtained from the Hessian calculation.49 III−B. AIMD Simulation. We employed the Becke−Lee− Yang−Parr (BLYP)50,51 exchange-correlation functional and the triple-ζ valence plus two polarization (TZV2P) basis sets for AIMD simulation at the aqueous TMAO-solution/air interface and the water/air interface. The core electrons were described by the Goedecker-Teter-Hutter pseudopotential.52 The real-space density cutoff was set to 320 and 400 Ry for the TMAO-solution/air and water/air interfaces, respectively. The van der Waals correction was included via the Grimme’s D3 method.53 Since the BLYP/TZV2P+D3 AIMD simulation can reproduce both surface tension54,55 and SFG spectra56 at the water/air interface well, we used this level of theory in the current study. A 13.2 Å × 13.2 Å × 50 Å simulation cell

(2), R χxxz (ω) =

1 ω

∫0

∞

dt e−iωt

∑ gds(zi(0))μż ,i (0) i,j

αxx , j(t ) (2)

where μz,i(t) and αxx,j(t) are the z component of the dipole moment for the ith molecule and xx component of the polarizability for the jth molecule, respectively, at time t. ω is the frequency. μ̇z,i(t) is the time derivative of μz,i(t). The z-axis forms the surface normal and the xy plane is parallel to the interface. gds(zi(0)) is the function for extracting the vibrational response of molecules near one of two interfaces in order to avoid the correlation of the two interfaces. This is given by ⎧1 for zi ≥ zds gds(zi) = ⎨ ⎩−1 for zi < zds ⎪

⎪

(3)

where zds is the z-coordinate of the dividing surface and zi is the z-coordinate of the position of chromophore i. For the C−H stretch mode of TMAO, we took the position of the nitrogen atom of TMAO representing the position of the chromophore, while we took the position of the hydrogen atom of water representing the O−H stretch chromophore. The origin point C


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The Journal of Physical Chemistry C Table 1. Gas-Phase C−H Stretch Frequencies of TMAO and Methanola scaled (0.963949) harmonic

post-VSCF (VQDPT2)

experiment

methanol

TMAO

methanol

TMAO

methanol

TMAO

2832 2935 2942 2986

2931−2936 2948 3019−3024 2998−3006

2911 --2967 3027

2938−2949 --3069−3074 3040−3047

2845 2925 2961 2980

2931−2952 (2970) --3036 (3038) 3006−3018 (3038)

symmetric Fermi resonance out-of-plane antisymmetric in-plane antisymmetric

(in units of cm−1) The experimental data for methanol and TMAO (solid) are obtained from refs 71 and 73, respectively. The experimentally reported gas phase IR frequencies of TMAO74 are also shown in parentheses.

a

was set to the center of mass of the system and we set zds = 0. We computed the contribution of TMAO to the SFG signal via this equation. μz,i(t) and αxx,j(t) were obtained by extracting the TMAO conformations from the AIMD simulation of aqueous TMAO-solution/air interface every 4 fs. The μ and α of the extracted TMAO molecule conformations were subsequently calculated at the BLYP/DZP level of theory by using the ORCA program.63 Note that since SFG spectra are calculated by using AIMD trajectories, the vibrational modes are coupled,64,65 unlike the normal mode calculation where the modes are, by definition, not coupled.66,67 III-D. O−H Stretch SFG Signal of Water: ssVVCF Approach. In the previous section, we introduced the SFG calculation based on the μ−α correlation function for computing the C−H stretch mode. This approach uses the gas-phase ab initio data, by assuming that the transition dipole moment and polarizability of TMAO are not largely affected by the surrounding molecules. This assumption is supported by the fact that the gas-phase C−H stretch frequency of TMAO is very similar to the SFG peak frequencies at the TMAOsolution/air interface (see below). Contrarily, this assumption does not hold for water, as surrounding molecules lead to large fluctuations of μ and α. Such fluctuations result in slow convergence of the μ−α time correlation function,56 which prohibits the use of eq 2 with a short AIMD trajectory. To overcome these difficulties, we recently developed an ssVVCF algorithm,56 where the induced effects are treated separately from the vibrational density of states. In this formalism, χ(2),R xxz (ω) is given by (2), R χxxz (ω) =

μ′(ω)α′(ω) ssVVCF χxxz (ω) iω 2

ssVVCF χxxz (ω) =

∫0

∞

dt e−iωt

In this paper, we consider that the O−H stretch chromophores are decoupled from the other O−H chromophores, which corresponds to the situation of isotopically diluted water (O−H in D2O). In the decoupled situation, we can neglect the cross correlations in eq 5, and thus the ssVVCF can be recast as ssVVAF (ω) = χxxz

∞

dt e−iωt

∑ gds(zi(0))rzOH ̇ , i (0) i

̇ (t ) · r OH(t ) ri⃗OH i⃗ | ri⃗OH(t )|

(8)

which is called the surface-specific velocity−velocity autocorrelation function (ssVVAF). To interrogate the contribution of the selected O−H chromophores to the SFG spectra, we used the following response function: ssVVAF (ω) = χxxz

∫0

∞

dt e−iωt

̇ (t ) · r OH(t ) ri⃗OH i⃗ | ri⃗OH(t )|

∑ gds(zi(0))θ(riO(0))rzOH ̇ , i (0) i

(9)

where O ⎧ ⎪1 for ri ≤ R c θ(riA) = ⎨ ⎪ O ⎩ 0 for ri > Rc

(10)

rOi (t) is the distance between the OTMAO atom at time t and the H atom of the O−H stretch chromophore i, and Rc is the radius of the cutoff sphere. The same approach has been also used in ref 70.

(4)

∑ gds(zi(0))rzOH ̇ , i (0) i,j

IV. RESULTS AND DISCUSSION IV-A. Gas-Phase TMAO Vibrational Mode. For a methyl group, three C−H stretch modes (symmetric, in-plane antisymmetric, and out-of-plane antisymmetric) and Fermi resonance contribute to the SFG experimental spectra at frequencies ranging from 2800 to 3100 cm−1, complicating the interpretation of the spectra even for simple alcohol molecules.71,72 Moreover, the frequency assignments of the C−H stretch modes are not trivial, since their vibrational frequencies shift largely for different moieties within a molecule. These modes have different SFG activities; when the C−H group points up along the surface normal, the symmetric mode shows a negative peak and the in-plane antisymmetric mode shows a positive peak, while the out-of-plane antisymmetric mode is normally invisible.65 The detailed assignment of the C−H stretching motion with the ssVVCF formalism is given in

̇ (t ) · r OH(t ) r j⃗OH j⃗ | r j⃗OH(t )|

(5)

The solvation effects are included separately by using the frequency dependent transition dipole moment μ′(ω) and polarizability α′(ω):68,69 ⎛ 53.03(3737 − ω) ⎞ 0 ⎟μ μ′(ω) ≡ ⎜1.377 + ⎝ ⎠ 6932.2

(6)

⎛ 5.287(3737 − ω) ⎞ 0 ⎟α α′(ω) ≡ ⎜1.271 + ⎠ ⎝ 6932.2

(7) −1

is the jth O−H bond vector. ω is in cm in eqs 6 and 7. μ and α0 are the gas-phase dipole-moment and polarizability. rOH j⃗ (t) 0

∫0

D


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the 2980 cm−1 mode cannot be ascribed only to the symmetric stretch mode, because the Fermi resonance also contributes to the SFG feature in this frequency range. It is thus essential to determine the orientation of TMAO from both symmetric C− H stretch and antisymmetric in-plane C−H stretch mode. In general, a positive (negative) C−H stretch symmetric stretch signal in the Im(χ(2),R ssp ) spectrum indicates that the C−H group points down to the bulk water (up to the air).75−77 This is consistent with the trend observed in the heterodyne-detected SFG spectra of water/lipid or surfactant interfaces, where the lipid methyl group points up to the air and the symmetric stretch mode shows a negative peak.75,78 The negative band in the simulated and experimentally measured Im(χ(2),R ssp ) spectra manifests that the −CH3 groups point up to the air region. A very recent SFG study also showed a negative 2970 cm−1 peak at the neat H2O solution of TMAO/air interface, while the positive feature arising from the antisymmetric in-plane mode was not prominent, presumably due to the presence of the large negative amplitude of the water’s O−H signal.30,31 In the present study, we resolve the positive Im(χ(2),R ssp ) feature of the antisymmetric mode both experimentally and theoretically using isotopically diluted water, confirming the up-orientation of the methyl group. We note that in our calculation of the time-correlation function we do not include the surrounding water molecules as they lead to additional fluctuation of the time-correlation function, which results in slow convergence of the SFG spectra. Nevertheless, simulated spectra show good agreement with the experimentally measured SFG spectra. This suggests that the solvation of TMAO does not affect the C−H stretch mode SFG spectra. IV−C. O−H Stretch SFG Response. Subsequently, we explored the effects of TMAO molecules on the O−H stretch mode of water in the SFG spectra, by comparing the O−H stretch SFG spectra at the aqueous solution of TMAO/air interface, the AO-surfactant/water interface, and the water/air interface. Figure 3a displays the experimentally measured O−H stretch SFG spectra at the isotopically diluted water solution of TMAO as well as the neat H2O solution of TMAO, while Figure 3b displays the simulated SFG spectra of HDO in D2O. The negative peak of the O−H stretch mode at 3300 cm−1 vanishes when the neat H2O is replaced by the isotopically diluted water, consistent with bulk IR/Raman spectra68,79 and the SFG spectra at the water/air interface.80,81 The simulated spectra at the TMAO-solution/air interface show a 3000 cm−1 positive peak and a 3400 cm−1 negative peak, in addition to the free O−H stretch peak at 3700 cm−1. The simulated negative 3400 cm−1 peak is in good agreement with the experimental data, while the positive 3000 cm−1 peak is missing in the experiment, because the spectral overlap of this positive band and negative C−H stretch band discussed above. Furthermore, the insensitivity of the free O−H stretch SFG amplitude to the presence of TMAO in the simulation is consistent with refs 30 and 31 but not with ref 27. In ref 31 the insensitivity of the free O−H stretch peak to the presence of the TMAO was attributed to the absence of TMAO at the topmost water layer at the water/air interface, implying that TMAO alkyl chains are not so hydrophobic. The interpretation of these results for the free O−H stretch mode is discussed in the next section. To discuss the effects of the AO group and methyl groups on the interfacial water conformation, we compared the SFG spectra of the interfacial water in the presence of the TMAO and AO-surfactant molecules. Both experiment and simulation

the SI. As such, it is essential to predict the vibrational frequencies of the C−H stretch modes accurately and to connect these modes with the SFG spectra. Calculated C−H stretch vibrational frequencies of TMAO based on the post-VSCF technique are summarized in Table 1, together with those of methanol. The calculated frequencies of TMAO and methanol are in much better agreement with the experimental data than the frequencies calculated from the harmonic approximation with a scale factor. For TMAO, our post-VSCF calculation indicates that the 2931−2936 cm−1 modes represent the symmetric C−H stretch mode, while the 3019−3024 cm −1 modes arises from the out-of-plane antisymmetric mode. Moreover, a strong Fermi resonance between the symmetric C−H stretch fundamental and the C− H bend overtone gives a frequency of 2948 cm−1, where the weights of the C−H stretching and bending bands are 0.2 and 0.6, respectively. This resonance band overlaps with the symmetric stretch bands at 2931−2936 cm−1 and therefore cannot be resolved in the experimental SFG spectra. Contrarily, methanol has the Fermi resonance peak at 2935 cm−1 and the splitting is as large as 100 cm−1. IV−B. SFG Spectra of C−H Stretch Mode. Having the assignment of the vibrational mode established, we now proceed to analyze the orientation of TMAO at the air/water interface from the SFG spectra. The simulated and experimentally measured SFG features in the frequency range of the C−H stretch modes are shown in Figure 2. The

Figure 2. Comparison of simulated and experimentally measured Imχ(2),R ssp (ω) SFG spectra for a solution of TMAO (3 molal) in isotopically diluted water (H2O:D2O = 1:3) at the aqueous TMAOsolution/air interface. The measured heterodyne detected-SFG spectra have been corrected for the Fresnel factors. The MEM fit spectra27 are also plotted.

simulated spectral features from the μ−α time correlation function show a strong negative peak at 2980 cm−1 and a weak positive peak at 3060 cm−1, which is in good agreement with the experimentally measured heterodyne-detected data. This negative peak is also consistent with the fits using the MEM analysis,27 although a weak positive peak at 3060 cm−1 was not observed, presumably because of the low resolution of the homodyne-detected SFG spectra. The gas-phase vibrational frequencies (Table 1) are blue-shifted in the SFG spectra by ∼40 cm−1, which can be attributed to the solvation of TMAO. This is in line with the previous study combining the ab initio calculation with Raman spectra of TMAO.73 Therefore, the negative 2980 cm−1 and positive 3060 cm−1 SFG signatures can be assigned to the symmetric/Fermi resonance and antisymmetric in-plane modes, respectively. It should be stressed that E


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frequency appears higher. Except for this point, the spectral features at the TMAO-solution/air interface and the AOsurfactant/water interface are similar, indicating that the hydrogen bond network of the interfacial water are similar, independent of the alkyl chain length. This manifests that the AO part governs the hydrogen bond network of the interfacial water. The similar hydrogen-bonded O−H stretch SFG spectra at aqueous TMAO-solution/air interface and the AO-surfactant/ water interface are further confirmed by a spectral decomposition. The decomposed spectra were calculated by using the selected O−H stretch chromophores based on eq 9 with the cutoff of Rc = 2.6 and 3.5 Å. The decomposed spectra plotted in Figure 3c demonstrate that the O−H stretch chromophores hydrogen bonded to the OTMAO atom contribute to the positive ∼3100 cm−1 SFG feature, while the other half O−H stretch chromophores weakly contribute to the negative ∼3400 cm−1 feature. This positive 3100 cm−1 peak illustrates that the O−H groups are strongly hydrogen bonded to the OTMAO atom and, as a consequence, pointing up toward the air region. This is consistent with our finding that the N−O group points down to the bulk as discussed above. IV-D. Structure of TMAO at Water−Air Interface. We demonstrated above that the AIMD simulations successfully reproduce the SFG spectra and identify that the TMAO methyl group orients to the air region and AO part of TMAO impacts the interfacial water conformation in a very similar manner to that of the AO surfactant. This confirms that the methyl group and AO part are hydrophobic and hydrophilic, respectively. Nevertheless, we have still two remaining questions: Is the description of AIMD simulation consistent with that of the force field MD simulation? Is TMAO excluded from the topmost water layer at the water−air interface, although the methyl group of TMAO is hydrophobic? First, we discuss the difference/agreement between the force field MD simulation and AIMD simulation. To do so, we calculated the distribution of the angle formed by the N−O group of TMAO near the interface and the surface normal in a similar manner as in ref 58. We calculated the angle only for the TMAO molecules whose nitrogen atom is located within 5 Å distance from the Gibbs dividing surface. The result is plotted in Figure 4a. This is similar to the plot obtained from the force field MD simulation.58 However, the average angle of the N−O group and the surface is ∼24°, which is larger than the angle of ∼15° (i.e., almost parallel to the surface) predicted by the force field MD simulation,58 indicating that the N−O group points more down to the bulk in the AIMD simulation than in the force field MD simulation. Since the hydrogen bond strength of O−H···OTMAO is underestimated in the force field MD simulation,34 the alignment of the N−O group in the force field MD simulation was weaker. Nevertheless, both AIMD and force field MD simulations predict similar surface activity of the TMAO; TMAO molecules can be found in the topmost layer of the water interface as well as in the bulk (see Figure 1). This is not quite in line with the conclusion from a recent SFG study, in which Mondal and coworkers found that the free O−H stretch SFG band of water is insensitive to the presence/absence of TMAO. They attributed this insensitivity to the same number of the free O−H stretch chromophore at the TMAO-solution/air interface and water/ air interface, meaning that TMAO is excluded from the topmost water layer at the water/air interface.31 However, since the SFG amplitude is governed by both the number of the

Figure 3. (a) Experimental, Fresnel factor corrected imaginary parts of the SFG spectra (Imχ(2) ssp (ω)) from (i) the aqueous 3 m TMAOsolution/air interface for both neat H2O (red broken line) and isotopic diluted water (H2O:D2O = 1:3, red solid line); (ii) the water/air interface for both pure water (blue broken line) and isotopic diluted water (H2O:D2O = 1:3, blue solid line), and (iii) at the DDAO/ isotopic diluted (H2O:D2O = 1:4) water interface (green line).70 The DDAO spectral amplitude was normalized to the same C−H negative amplitude as TMAO. Note that the frequency range covered in the experiment is given by the finite bandwidth of the IR pulse. (b) Simulated SFG spectrum (Imχ(2),R ssp (ω)) of the O−H stretch modes for HDO in D2O at TMAO-solution/air interface, together with the spectra at the DTAO/isotopically diluted water interface70 and at the isotopically diluted water/air interface.39 The spectral amplitudes were scaled to fit to the experiments of isotopically diluted water in (a). (c) Contributions from the O−H chromophores within the cutoff spheres with the radii of Rc centered at the OTMAO atom to the SFG spectra at the TMAO-solution/air interface. We note that the simulated spectra in panels (b) and (c) only account for the OH stretch vibration and do not contain the C−H vibrations.

data show that the negative band has a similar shape and central frequency for the TMAO-solution/air and water/air interfaces, whereas for the AO-surfactant/water interface the response is substantially blue-shifted. The apparent blue-shift observed for the surfactant can be explained by the full coverage of the water surface by the surfactant, giving rise to the absence of the high frequency positive SFG feature associated with the free O−H stretch mode. With no free O−H peak, no cancellation of the negative and positive peaks occurs and thus the negative peak F


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normal by adding TMAO at the water/air interface. As such, despite the number of the free O−H chromophores at the water/air interface decreases due to the excluded volume of TMAO, the free O−H stretch SFG signature is unchanged. Moreover, we have explored the effects of the TMAO on the water conformation. We find that the TMAO and AOsurfactant provide similar O−H stretch SFG spectra of water, demonstrating that the interfacial water structures are determined by the AO group in both cases, and are independent of the length of the alkyl chains. The N−O group simulated by AIMD points down to the bulk with the tilt angle of 20° with respect to the surface, which is larger than the angle predicted with force field MD. This can be ascribed to the underestimation of the N−O···H hydrogen bond strength in the force field MD simulation, consistent with the previous AIMD study.33 On the other hand, the orientation of the water’s free O−H groups is more parallel to the surface normal at the aqueous TMAO solution/air interface than at the water/ air interface. This accounts for the insensitivity of the free O−H stretch band to the TMAO concentration, even though TMAO is located at the topmost layer of water. Through this study, we also demonstrate that it is not so straightforward to connect the C−H stretch mode to the orientation of TMAO, since the C−H stretch frequencies are easily shifted with the different moiety of molecule as well as the contribution of the Fermi resonance. This study also highlights the importance of the combined AIMD simulation, VSCF calculation with the SFG measurement.

Figure 4. (a) Probability distribution of the angle formed by the N−O group of TMAO at the interface and the surface normal, which is denoted by red bars. The angle distribution with the force field MD (3 M TMAO concentration) was taken from ref 58 for comparison, and is shown as the blue line. (b) Probability distribution of the angle formed by the free O−H group and the surface normal. The black line of unity probability indicates the distribution where the orientation is completely random. (c) Schematic pictures of water orientations at the TMAO-solution/air and water/air interfaces. The red arrows represent the directions of the free O−H groups of water.

chromophores and the orientation of the transition dipole moment, the insensitivity of the SFG amplitude cannot be directly connected to the same number of the chromophores at the interface. To resolve the apparent contradiction between the unchanged free O−H, yet TMAO being present at the surface, we calculated the axial profile of the average angle formed by the free O−H group and the surface normal for the water/air interface and TMAO-solution/air interface, which are plotted in Figure 4b. Here, we define the free O−H group whose hydrogen atom cannot find any intermolecular oxygen atom within a 3.3 Å cutoff sphere. The data indicate that the angular distribution of the free O−H groups is indeed affected by the presence of TMAO; due to TMAO, the water molecule points more up to the air region, as is schematically illustrated in Figure 4c. As such, although the surface area of water is decreased due to the presence of TMAO, and the number of free O−H groups will accordingly be reduced, the free O−H stretch SFG signal seems invariant, thanks to the enhanced uporientation of the remaining free O−H groups. This clearly demonstrates that the TMAO methyl groups are hydrophobic and are present near the hydrophobic surface, despite the free O−H signal remaining largely constant.

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcc.6b04852. C−H stretch modes, convergence of physical qualities (PDF)

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. Phone: +81-6-6850-6433. *E-mail: [email protected]. Phone: +49-6131-379536. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by JSPS KAKENHI Grant Numbers JP16H00835, JP16K17855, and JP15K17815. We thank Dr. Kiyoshi Yagi at RIKEN for sharing the SINDO code with us. The simulations were performed by using the computational facilities in the Institute of Solid State Physics, the University of Tokyo, Japan, Cybermedia Center, Osaka University, Japan, and Institute for Molecular Science, Japan.

V. CONCLUDING REMARKS We have measured and simulated SFG spectra at the aqueous TMAO-solution/air interface to clarify the orientation of TMAO near the hydrophobic interface. Simulation shows good agreement with the experimental data for both the C−H stretch mode of TMAO and the O−H stretch mode of water. With the help of the post-VSCF calculation, the observed negative ∼2980 cm−1 and positive ∼3060 cm−1 SFG feature are assigned to the symmetric C−H stretch mode/Fermi resonance and the antisymmetric in-plane C−H stretch mode, respectively. This shows that the methyl groups of TMAO point up to the air. Moreover, we have found that the free O−H group of the topmost water layer points more parallel to the surface

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