Letter pubs.acs.org/JPCL
Water Librations in the Hydration Shell of Phospholipids Giulia Folpini,† Torsten Siebert,† Michael Woerner,† Stephane Abel,‡ Damien Laage,*,§,∥ and Thomas Elsaesser*,† †
Max-Born-Institut für Nichtlineare Optik und Kurzzeitspektroskopie, D-12489 Berlin, Germany Institut de Biologie Intégrative de la Cellule (I2BC), Institut Frédéric Joliot, CEA, CNRS, Univ Paris-Sud Université Paris-Saclay, 91405 Gif-Sur-Yvette Cedex, France § ́ Ecole Normale Supérieure, PSL Research University, UPMC Univ Paris 06, CNRS, Département de Chimie, PASTEUR, 24 rue Lhomond, 75005 Paris, France ∥ Sorbonne Universités, UPMC Univ Paris 06, ENS, CNRS, PASTEUR, 75005 Paris, France ‡
ABSTRACT: The hydrophilic phosphate moiety in the headgroup of phospholipids forms strong hydrogen bonds with water molecules in the first hydration layer. Timedomain terahertz spectroscopy in a range from 100 to 1000 cm−1 reveals the influence of such interactions on rotations of water molecules. We determine librational absorption spectra of water nanopools in phospholipid reverse micelles for a range from w0 = 2 to 16 waters per phospholipid molecule. A pronounced absorption feature with maximum at 830 cm−1 is superimposed on a broad absorption band between 300 and 1000 cm−1. Molecular dynamics simulations of water in the reverse micelles suggest that the feature at 830 cm−1 arises from water molecules forming one or two strong hydrogen bonds with phosphate groups, while the broad component comes from bulk-like environments. This behavior is markedly different from water interacting with less polar surfaces.
W
hindered rotation is mainly localized on individual water molecules with, however, a force constant determined by the hydrogen-bonding interactions with the neighboring water molecules. This behavior makes the L2 mode a probe of local structure, a fact that has been exploited in studies of the L2 band of water nanopools confined in sodium bis(2-ethylhexyl) sulfosuccinate (AOT) reverse micelle structures with sulfonate headgroups.6 The properties of the L2 mode have thus been analyzed for increasing confinement, when the water pool radius decreases from more than 50 to 10 Å. One finds a pronounced redshift of the L2 band maximum, from a bulk-like value of 670 cm−1 down to 500 cm−1 in the smaller reverse micelles. In parallel, the spectral envelope develops a peculiar shape consisting of at least two subcomponents. A theoretical analysis of such spectra has distinguished two main species in the nanopool: water molecules at the reverse micelle interface whose hydrogen-bond structure and rotational dynamics are changed, leading to red-shifted librations, and a bulk-like water core that prevails in large reverse micelles.7,8 Water librations in the first few hydration layers around a biomolecule have remained largely uncharacterized.9,10 In particular, the behavior of water molecules interacting with charged phosphate groups, which are major hydration sites in phospholipids and the backbone of DNA, is not understood. In this Letter, we study water librations in the first few layers of
ater molecules at surfaces and biomolecular interfaces are subject to particular boundary conditions arising from steric constraints, local interactions such as hydrogen bonds, and electric fields from electrically charged or polar units. As a result, the structure and dynamics of the first few layers of a hydration shell surrounding a biomolecule are different from bulk water.1,2 Steady-state and ultrafast timeresolved vibrational spectroscopy have provided insight into intra- and intermolecular excitations of water molecules in the hydration shell and their modification compared to bulk water. The strength and geometry of local hydrogen bonds as well as ultrafast structural fluctuations have been probed via the vibrational frequency positions and lineshapes of the intramolecular OH stretching and bending modes. Hindered rotations, the so-called librations of water molecules in a frequency range from several hundreds up to 1500 cm−1, can give complementary insight into both steric constraints and interactions at surfaces and interfaces. Their frequency depends sensitively on intermolecular interactions, e.g., the strength of hydrogen bonds. Moreover, the character of these librations ranges from high frequency localized modes involving essentially a single water molecule, down to collective low frequency modes which are delocalized on several water molecules. Librations in bulk water have been studied by linear infrared and microwave spectroscopy in a range from 10 to 1000 cm−1 (300 GHz to 30 THz).3−5 A most prominent feature is the socalled L2 band, which peaks around 670 cm−1 with a maximum extinction coefficient of some 30 M−1cm−1. The underlying © 2017 American Chemical Society
Received: July 26, 2017 Accepted: August 31, 2017 Published: August 31, 2017 4492
DOI: 10.1021/acs.jpclett.7b01942 J. Phys. Chem. Lett. 2017, 8, 4492−4497
Letter
The Journal of Physical Chemistry Letters hydration shells by broadband time-domain terahertz (THz) spectroscopy in a range from 100 to 1000 cm−1. We measure for the first time the librational bands of water at the surface of phospholipid reverse micelles (Figure 1a) at different levels of hydration. The librational spectra of hydrating water display a prominent band around 830 cm−1, on top of a broad L2 absorption component extending from 300 to 900 cm−1. Molecular dynamics simulations allow decomposing the spectra in contributions from different water subensembles. The feature at 830 cm−1 is a hallmark of water molecules attached to phosphate groups via strong hydrogen bonds, while the broad component originates mainly from molecules interacting with their water environment. In our experiments, picosecond broadband THz transients are transmitted through the sample under study and detected in amplitude and phase by time-resolved free-space electrooptic sampling (EOS).11,12 A subsequent Fourier transform to the frequency domain provides the spectrum of the transmitted pulse. In Figure 1b, the time structure of the incoming THz pulses is presented. Their spectrum (Figure 1c) covers an extremely broad range from 10 to more than 1000 cm−1. The sharp features in the spectrum originate from vibrational resonances of the nonlinear OH1 crystal used for THz generation. The minimum around 150 cm−1 is caused by the strong absorption of the ZnTe crystal of the EOS system. It is absent when using a GaP electrooptic crystal, which is transparent in this range. Transmission of the THz transients through the two 450 μm thick diamond windows of the empty sample cell reduces their intensity by some 30% with a negligible reshaping of the spectrum. Broadband spectra of neat H2O films were recorded in order to benchmark the sensitivity and accuracy of the experiments. In Figure 2a, the absorbance A = −log(It/I0) of a water film is plotted as a function of frequency in the range of the prominent
Figure 2. (a) Absorption spectra of neat water as measured with the broadband THz source (blue line, sample thickness 15−18 μm). The absorbance is plotted as a function of wavenumber (cm−1, bottom) and of frequency in THz (top). The black solid line gives the spectrum from ref 3 with a characteristic error bar at 400 cm−1. The dashed line represents the spectrum reported in ref 5. (b) Absorption spectra of DOPC reverse micelles dissolved in benzene for different numbers w0 of water molecules per phosphate headgroup. The spectra display contributions from DOPC, water, and benzene. With increasing hydration level, the absorption strength of water librations increases and displays a distinct feature around 830 cm−1 (arrow).
Figure 1. (a) Molecular structure of DOPC and schematic view of a reverse micelle with a water nanopool in the center. (b) Time dependent electric field of the broadband THz transients as measured by free-space electrooptic sampling. (c) Spectrum of the THz transient. The narrow spectral features originate from vibrational bands in the nonlinear OH1 crystal.
L2 band (blue line, It: intensity transmitted through the water film; I0: intensity transmitted through the empty sample cell). The error bars account for both the accuracy of the electric field measurement by EOS and the uncertainty in sample thickness l (l = 15−18 μm). The broadband measurement allows for a large dynamic range in absorbance between A = 0.05 and A ≈ 3. Literature spectra from ref 3 (black solid line) and ref 5 (dashed line) are plotted for comparison. For calculating the absorbance A = ϵ·c·l, we take the molar extinction coefficients ϵ from the literature,3 the water concentration c = 56 M, and a sample thickness l = 17.5 μm. With such numbers, the calculated and the experimental peak absorbance at 670 cm−1 agree well within the experimental uncertainty. Moreover, the ratio of absorbance at 670 and 200 cm−1 is the same in the experimental and the literature spectra. In Figure 2b, we present librational spectra of water nanopools in dioleoylphosphatidylcholine (DOPC, Figure 1a) for different hydration levels w0, where w0 represents the number of water molecules per DOPC phosphate headgroup. The absorbance A = −log(It(w0)/I0) is plotted as a function of wavenumber. These spectra contain vibrational absorption bands of DOPC, water, and the benzene solvent. With increasing water content, a broad librational absorption develops between 300 and 900 cm−1 with a distinct absorption feature around 830 cm−1. The latter is absent in the librational spectrum of neat H2O (Figure 2a). The benzene solvent gives 4493
DOI: 10.1021/acs.jpclett.7b01942 J. Phys. Chem. Lett. 2017, 8, 4492−4497
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The Journal of Physical Chemistry Letters rise to the strong absorption lines around 680 cm−1, which mask the water absorption in this range. Librational bands without residual contributions from the DOPC molecules and the solvent are presented in Figure 3, where the absorbance A = −log(It(w0)/It(w0 = 0)) normalized to the w0 = 0 spectrum of Figure 2b is plotted as a function of wavenumber. The dashed lines mark the range of strong benzene absorption in which the normalization does not work because of the very strong solvent absorption. The spectra in Figure 3 again display two main features: the broad librational band and the distinct spectral feature with a maximum at 830 cm−1. The librational spectra of the water nanopools in the DOPC reverse micelles consist of a broad absorption band between 300 and 900 cm−1, including a pronounced feature with maximum at 830 cm−1. The latter is absent in bulk water (Figure 2a) and in the librational spectra of water in AOT reverse micelles.6 There is a moderate increase of the overall spectral width of librational absorption compared to the L2 band of bulk water (cf. Figure 3b) but no red-shift for low w0, in contrast to the AOT case.6 The large spectral width reflects the presence of water environments with a different structure. Overall, the broad band bears a strong similarity with the bulk water spectrum and is assigned to L2 librations of H2O molecules forming hydrogen bonds with neighboring water
molecules. This species even exists at the low w0 = 2 water level, giving evidence of a markedly inhomogeneous clustering, i.e., strong variety of water sites in this system. With increasing size of the water pool (increasing w0), a larger fraction of water molecules is embedded in a bulk-like environment, leading to an enhancement of the broad absorption component relative to the feature at 830 cm−1. The two components display a strong spectral overlap, hampering a quantitative analysis of the relative changes of absorption with increasing w0. The frequency upshift of the 830 cm−1 component relative to the L2 absorption maximum corresponds to a higher force constant of the underlying librational motion. An enhancement of hydrogen bond strength and modified steric constraints can go along with a larger force constant of hindered rotations, and we thus assign the additional absorption feature to a subensemble of water molecules embedded in stronger, i.e., shorter, hydrogen bonds. In the phospholipid headgroups, the ionic phosphate groups represent prominent hydration sites.13 Each of the two free oxygen atoms of the PO−2 unit serves as an acceptor of up to 3 hydrogen bonds with OH groups of water molecules in the first hydration layer, a geometry markedly different from bulk water where a water oxygen typically accepts 2 hydrogen bonds. The phosphate−water hydrogen bonds are shorter and somewhat stronger than water−water hydrogen bonds.13,14 This particular structure at the DOPC surface favors higher librational frequencies of the water molecules involved. The spectral width of the 830 cm−1 component is distinctly smaller than that of the broad L2 contribution. Twodimensional infrared spectroscopy of phosphate vibrations has shown that interfacial water dynamics and the concomitant electric field fluctuations in DOPC reverse micelles are slowed down compared to bulk H2O.15 As a result, spectral diffusion of 830 cm−1 excitations and the corresponding contribution to the absorption line width are expected to be reduced. This interpretation assumes that the infrared absorption spectra of Figure 3 are dominated by dipole−dipole fluctuations involving water molecules. Possible other dipoles of the DOPC molecules may be influenced by the presence of water but play a negligible role compared to the water contribution in the absorption spectra. To validate our interpretation, we have performed molecular dynamics simulations of a series of DOPC reverse micelle structures with w0 = 2, 8, and 16. The water librational spectrum can be calculated as16,17 α(ω) =
πβω 2 3n(ω)cV ϵ0
+∞
∫−∞
dt e−iωt ⟨μ(t ) ·μ(0)⟩
(1)
where α(ω) is the absorption coefficient, n(ω) is the refractive index, ϵ0 is the vacuum permittivity, β = 1/kBT, c is the velocity of light, V is the volume of the sample, and μ(t) is the total dipole moment vector of the sample at time t. Here we are interested in the contributions to this spectrum arising from water molecules in different hydrogen-bond environments. The latter are determined by replacing the total dipole in eq 1 by the dipole moment of each individual water molecule, without considering cross-correlations between water molecules. This allows for different populations of water molecules to be distinguished, according to the number of hydrogen bonds formed with phosphate groups. We note that the SPC/E water potential employed in all of our simulations was shown18,19 to yield a bulk IR librational spectrum in fair agreement with experiments.
Figure 3. Librational absorption spectra of water nanopools in DOPC reverse micelles (black lines). The absorbance of water molecules is plotted as a function of wavenumber between 300 and 900 cm−1 for different numbers w0 of water molecules per phosphate headgroup. All spectra display a distinct feature around 830 cm−1 due to water molecules forming hydrogen bonds with the phosphate groups. The dashed lines mark the range in which the water absorption is masked by the strong absorption of the solvent benzene. The blue line in panel b gives the L2 band of bulk water taken from Figure 2 and normalized to the peak absorbance of the micelle spectrum. 4494
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The Journal of Physical Chemistry Letters
restoring force. Our results further suggest that the librational frequencies of water molecules engaged in different types of hydrogen bonds can also be sensitive to, e.g., the degree of confinement. This is shown by the increasing blueshift of the librational band for the water molecules hydrogen-bonded to phosphate groups when going from a moderate confinement in the w0 = 8 and 16 reverse micelles (Figures 4b,c) to the strong confinement in the w0 = 2 reverse micelle (Figure 4a). The greater strength of the water−phosphate hydrogen bonds relative to the water−water bonds also results in shorter oxygen−oxygen distances. A comparison of the oxygen−oxygen radial distribution functions from our simulations shows that the water oxygen− phosphate oxygen distribution functions in DOPC reverse micelles exhibit a first maximum at ≃2.65 Å, a distance significantly shorter than the 2.75 Å oxygen−oxygen separation in bulk water. This can be explained by the negative charge of the PO−2 phosphate group, which enhances the electrostatic contribution to hydrogen bonding. We note that in AOT reverse micelles with SO−3 headgroups, no blueshift of the librational spectrum was found,8 and the hydrogen bonds between the sulfonate oxygen atoms and water molecules do not seem to be stronger than water−water bonds. This is due to the lower charge density on the oxygen atoms, since the anion negative charge is now delocalized on three oxygen atoms versus only two for phosphate. This is also reflected in the partial charges which are used in typical force fields and have values of −0.78 for the phosphate oxygen atom20 versus −0.60 for the sulfonate oxygen atom21 in the CHARMM force-field. In conclusion, our results show that water librations can be used as sensitive reporters of the hydrogen bond strength in the hydration layers around biomolecules. In bulk water, the broad librational band is due to the variety of different fluctuating local environments and hydrogen bond strengths. Next to phosphate groups in DOPC reverse micelles of various sizes, a blueshifted peak is visible in the librational spectrum above 800 cm−1. The combination of time-domain terahertz spectroscopy and molecular dynamics simulations assigns this feature to water molecules forming strong hydrogen bonds with the phosphate groups. The methodology employed in this study demonstrates a general access to the state of water in different interfacial environments and the capability to extract detailed information about specific subensembles of water within the complex hydration shell of biomolecular systems.
The contributions to the librational spectra show that water molecules hydrogen-bonded to phosphate groups exhibit a strongly blueshifted librational band (Figure 4). This is most visible for the w0 = 2 DOPC reverse micelle, where this population represents a large fraction (77%) of the total number of water molecules (Figure 4a). The librational band of water molecules doubly bonded to phosphate groups exhibits a maximum at 840 cm−1, that of singly bonded water molecules presents a peak at 800 cm−1, while the remaining water molecules in the reverse micelle yield a broad librational band with a maximum at approximately 650 cm−1. Water molecules hydrogen-bonded to phosphate groups in the larger w0 = 8 and 16 reverse micelles also exhibit a librational band shifted to higher frequencies than in the bulk (Figure 4b,c). This therefore supports an assignment of the 830 cm−1 feature observed in the experimental spectra to water molecules strongly hydrogen-bonded to the phosphate groups. While there is qualitative agreement between the calculations and the experimental librational spectra, the absorption lineshapes display some differences, especially in the larger reverse micelles. For the w0 = 2 system, the contribution from water molecules hydrogen-bonded to phosphate groups leads to a prominent peak, consistent with the experimental spectrum; however, we note the strongly non-Gaussian character of this contribution. For larger reverse micelles, the amplitude of this contribution is too limited to lead to a visible peak in the total spectrum, in contrast with the experimental spectra. This difference may be caused by intermolecular correlations and non-Condon effects, which are both neglected here. It is interesting to note the opposite frequency shifts of the water OH stretch and librational modes upon a change in the H-bond strength: while stronger H-bonds lead to a frequency redshift for the water OH stretch (because the OH elongation is facilitated by the strong H-bond acceptor), they lead to a frequency blueshift of the librations, because any deviation from a linear H-bond costs more energy due to the stronger
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MATERIALS AND METHODS The neat water sample consisted of a 15−18 μm thick liquid film held in-between two 450 μm thick diamond windows. Reverse micelles were generated by preparing 0.25 M solutions of dioleoylphosphatidylcholine (DOPC) (Echelon Inc., dried in vacuum over P2O5) in benzene (Sigma-Aldrich, anhydrous 99.8%). Water nanopools within the reverse micelles were created by adding appropriate amounts of water to cover a hydration range from w0 = 2 water molecules per phosphate head up to w0 = 16. The DOPC samples had a layer thickness of 250 μm in between two diamond windows (thickness 450 μm). The geometric shape and diameters of DOPC reverse micelles in benzene have been studied in dynamic light scattering experiments22 and by molecular dynamics simulations.20 Both experiment and simulation suggest a close to spherical shape of the reverse micelles with the reverse micelle (respectively inner water pool) diameters ranging from some 40 Å (respectively 7 Å) at w0 = 2 to 75 Å (respectively 19 Å) at
Figure 4. Calculated water librational spectra in DOPC reverse micelles for (a) w0 = 2, (b) w0 = 8, and (c) w0 = 16. The contributions of individual water dipoles to the librational spectrum [eq 1] were separated according to the hydrogen-bonding environment: one hydrogen bond to a phosphate group (red), two hydrogen bonds to phosphate (green), and no hydrogen-bond to phosphate (blue). The sum of these contributions is shown in black. All spectra were normalized by the total spectrum maximum intensity. 4495
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The Journal of Physical Chemistry Letters w0 = 16. More detailed results and discussion have been presented in refs 20 and 22. Infrared spectroscopy of intermolecular motions and librations in aqueous systems requires a broad spectral range extending from some 10 to 1000 cm−1. For a sample thickness on the order of 10 μm, neat liquid water and hydrated biomolecular systems display a peak absorbance A = -log(T) ≃ 2−4 in this frequency range, i.e., a sample transmission between 0.01 and 1%. As the preparation of liquid samples of sub-10 μm thickness represents a substantial technical challenge, absorption measurements with a very high dynamic range are mandatory. Broadband terahertz (THz) pulses were generated by optical rectification of 25 fs pulses in a (2-(3-(4-hydroxystyryl)-5,5dimethylcyclohex-2-enylidene)malononitrile (OH1) crystal (thickness 0.35 mm). The input pulses with a center wavelength of 800 nm, a duration of 25 fs, and a pulse energy of 200 μJ were generated in an amplified Ti:sapphire laser system (repetition rate 1 kHz). The experimental setup has been described in ref 11. Electric field transients were detected in the time domain by free space electro-optic sampling in a 10 μm thick ZnTe crystal. Pulses of 12 fs duration from the synchronized laser oscillator of the Ti:sapphire system served for sampling.12 The spectra presented here demonstrate a large dynamic range in absorbance of approximately A = 3.5. The latter exceeds the absorbance range typically covered by high-end Fourier transform infrared (FTIR) spectrometers implementing thermal and/or large-scale accelerator-based radiation sources in the same spectral range. On the other hand, FTIR methods offer a superior accuracy in measurements with samples of A ≤ 1. A systematic comparison of broadband THz and FTIR spectroscopies for studying aqueous systems of large optical thickness is beyond the scope of the present study but represents an interesting topic of future research. We performed molecular dynamics simulations of DOPC reverse micelles with w0 = 2, 8, and 16, following the same procedures as described in detail in ref 20. The structure of the simulated DOPC reverse micelles was characterized in ref 20. Water is described with the SPC/E potential and the DOPC reverse micelles with the CHARMM36 force field. Configurations were saved every 1 fs from trajectories propagated at 300 K respectively during 1, 0.5, and 0.1 ns for the w0 = 2, 8, and 16 reverse micelles. The presence of hydrogen-bonds between water molecules and phosphate groups was defined by geometric criteria including the distances between water and phosphate oxygen atoms (ROwOp < 3.5 Å) and between water hydrogen and phosphate oxygen atoms (RHwOp < 2.5 Å), and the angle between the OwHw and OwOp directions (θHwOwOp < 30°). The contribution of each type of hydrogen-bond population to the libration spectrum is calculated by determining the hydrogen-bond acceptor at time t = 0 in the dipole time-correlation function in eq 1. Each time correlation function is calculated up to delays of 10 ps, which are shorter than the time scale to exchange hydrogen-bond partners in these reverse micelle systems.
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ORCID
Stephane Abel: 0000-0002-1980-0839 Damien Laage: 0000-0001-5706-9939 Thomas Elsaesser: 0000-0003-3056-6665 Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This work was granted access to the CCRT/CINES HPC resources under allocation t2014077266 by GENCI (Grand Equipement National de Calcul Intensif) and with a generous allocation by CEA/CCRT.
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REFERENCES
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