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Perspective: Structure and ultrafast dynamics of biomolecular hydration shells
The structure and function of biomolecules can be strongly influenced by their hydration shells. A key challenge is thus to determine the extent to which these shells differ from bulk water, since the structural fluctuations and molecular excitations of hydrating water molecules within these shells can cover a broad range in both space and time. Recent progress in theory, molecular dynamics simulations, and ultrafast vibrational spectroscopy has led to new and detailed insight into the fluctuations of water structure, elementary water motions, and electric fields at hydrated biointerfaces. Here, we discuss some central aspects of these advances, focusing on elementary molecular mechanisms and processes of hydration on a femto-to picosecond time scale, with some special attention given to several issues subject to debate.
Phosphate Vibrations Probe Electric Fields in Hydrated Biomolecules: Spectroscopy, Dynamics, and Interactions
Electric interactions have a strong impact on the structure and dynamics of biomolecules in their native water environment. Given the variety of water arrangements in hydration shells and the femto- to subnanosecond time range of structural fluctuations, there is a strong quest for sensitive noninvasive probes of local electric fields. The stretching vibrations of phosphate groups, in particular the asymmetric (PO2)− stretching vibration νAS(PO2)−, allow for a quantitative mapping of dynamic electric fields in aqueous environments via a field-induced redshift of their transition frequencies and concomitant changes of vibrational line shapes. We present a systematic study of νAS(PO2)− excitations in molecular systems of increasing complexity, including dimethyl phosphate (DMP), short DNA and RNA duplex structures, and transfer RNA (tRNA) in water. A combination of linear infrared absorption, two-dimensional infrared (2D-IR) spectroscopy, and molecular dynamics (MD) simulations gives quantitative insight in electric-field tuning rates of vibrational frequencies, electric field and fluctuation amplitudes, and molecular interaction geometries. Beyond neat water environments, the formation of contact ion pairs of phosphate groups with Mg2+ ions is demonstrated via frequency upshifts of the νAS(PO2)− vibration, resulting in a distinct vibrational band. The frequency positions of contact geometries are determined by an interplay of attractive electric and repulsive exchange interactions.
Ultrafast phosphate hydration dynamics in bulk H2O
Phosphate vibrations serve as local probes of hydrogen bonding and structural fluctuations of hydration shells around ions. Interactions of H2PO4− ions and their aqueous environment are studied combining femtosecond 2D infrared spectroscopy, ab-initio calculations, and hybrid quantum-classical molecular dynamics (MD) simulations. Two-dimensional infrared spectra of the symmetric (𝜈𝑆(PO−2)) and asymmetric (𝜈𝐴𝑆(PO−2)) PO−2 stretching vibrations display nearly homogeneous lineshapes and pronounced anharmonic couplings between the two modes and with the δ(P-(OH)2) bending modes. The frequency-time correlation function derived from the 2D spectra consists of a predominant 50 fs decay and a weak constant component accounting for a residual inhomogeneous broadening. MD simulations show that the fluctuating electric field of the aqueous environment induces strong fluctuations of the 𝜈𝑆(PO−2) and 𝜈𝐴𝑆(PO−2) transition frequencies with larger frequency excursions for 𝜈𝐴𝑆(PO−2). The calculated frequency-time correlation function is in good agreement with the experiment. The 𝜈(PO−2) frequencies are mainly determined by polarization contributions induced by electrostatic phosphate-water interactions. H2PO4−/H2O cluster calculations reveal substantial frequency shifts and mode mixing with increasing hydration. Predicted phosphate-water hydrogen bond (HB) lifetimes have values on the order of 10 ps, substantially longer than water-water HB lifetimes. The ultrafast phosphate-water interactions observed here are in marked contrast to hydration dynamics of phospholipids where a quasi-static inhomogeneous broadening of phosphate vibrations suggests minor structural fluctuations of interfacial water.