Ultrafast structural and vibrational dynamics of the hydration shell around DNA

Two-dimensional infrared spectroscopy in the frequency range of OH- and NH stretch excitations serves for a direct mapping of hydration dynamics around DNA. A moderate slowing down of structural dynamics and resonant OH stretch energy transfer is observed in the DNA water shell compared to bulk water.

stretch mode of adenine and the lower one at 3200 cm -1 representing a superposition of the symmetric NH 2 stretch mode of adenine and the NH stretch vibration of thymine. The cross peaks reveal the coupling between the different NH stretch modes. As a function of population time T, the intensity of the cross peak at ( 1 , 3 )=( 3350,3200) cm -1 increases relative to the diagonal peaks, due to a downhill energy transfer from the asymmetric NH 2 stretch vibration of adenine to the NH stretch mode of thymine. All diagonal and cross peaks show minor spectral diffusion as a function of T.
For fully hydrated DNA (92% RH), the 2D spectra display a superposition of the NH stretch peaks and the OH stretch contribution of the water shell (Fig. 1). The latter shows a pronounced reshaping from a diagonal to an essentially round line shape on a time scale of 500 fs, much slower than the sub-100 fs spectral diffusion in bulk water [5]. The presence of the water shell leads to a moderate broadening of the NH stretch peaks only, pointing to a limited influence of water fluctuations on the NH stretch lineshapes.
For a more detailed comparison of the hydration shell dynamics with bulk water, we measured 2D spectra with pulses centered at 3400 cm -1 (Fig. 2a). Here, the OH stretch contributions strongly dominate and the reshaping due to spectral diffusion can be quantified by analyzing the slopes of center lines (thick solid lines in Fig. 2a) as a function of population time T. The reshaping from the initial inhomogeneously broadened elliptic line shape into a more homogeneous round shape leads to a decrease of the center line slopes within the first 500 fs (open circles in Fig. 2b). Fig. 2b also shows frequency-time correlation functions of bulk water calculated from molecular dynamics simulations which include resonant energy transfer between OH stretching oscillators (solid line) or neglect this mechanism (dashed line) [6]. Bottom: 2D infrared spectra measured for different population times T at a humidity level of 0% RH (upper row) and 92% RH (lower row). The femtosecond pulses were centered at 3250 cm -1 . The 2D signals above   3150 cm -1 are due to NH or OH stretch v=0 to 1 excitations, signals below to v=1 to 2 transitions. The amplitude change between neighboring contour lines is 10%. The 0% RH spectra are dominated by NH stretch excitations of the base pairs. The 92% RH spectra represent a superposition of NH stretch and OH stretch excitations of the water shell.

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Compared to such calculations and experimental results (squares, Ref. [5]) for bulk water, the DNA hydration shell displays a smaller amplitude of the fast sub-100 fs decay which is mainly due to librational motions, and a moderately slower time evolution between 100 and 500 fs. We attribute this behavior to the more rigid structure of the hydration shell, in particular of the first water layer interacting with DNA, and to a smaller rate of resonant OH stretch energy transfer at the reduced water concentration of c≈10 M.
Vibrational relaxation of NH and OH stretch excitations and energy dissipation in the water shell were studied in an independent series of experiments [4,7]. In both the water shell and in bulk water, a vibrationally hot ground state which is characterized by an enhanced fraction of structurally distorted and/or broken hydrogen bonds is formed on a 1 to 2 ps time scale.