Periodic Reporting for period 3 - NONABVD (Nonadiabaticity in Biomolecular Vibrational Dynamics)
Berichtszeitraum: 2022-01-01 bis 2022-05-31
The ERC Starting Grant project NONABVD aims at the fundamental understanding of ultrafast biomolecular vibrational dynamics in the mid-IR/THz region. We investigate the impact of nonadiabatic effects in dipolar liquids, within nano-confined environments and in the vicinity of biological interfaces. In these scenarios, elementary charge carriers, like excess protons and hydrated electrons, or highly charged biomolecules, like DNA or RNA, couple to their aqueous environment through a variety of noncovalent interactions. Local structures are determined by hydrogen bonds with water molecules and complemented by non-specific electrostatic and many-body interactions. The structural fluctuations of the water shell result in fluctuating Coulomb forces and in a breaking and reformation of hydrogen bonds. The understanding of these processes via underlying interactions is of fundamental importance with applications covering microscopic descriptions of elementary proton transfer reactions, mechanisms of energy dissipation upon vibrational excitation and solvation dynamics in biological relevant crowded environments.
The NONABVD project will transfer paradigms of nonadiabatic electronic relaxation to the low energy mid-IR/THz domain of biomolecular vibrational dynamics. The approach provides a description of microscopic phenomena like structural fluctuations, vibrational lifetimes and dissipation of excess energy and fully accounts for the strong impact of the fluctuating environment on biomolecular structure and dynamics. The concise theoretical description of proton or electron solvation and transfer processes in the vicinity of biological interfaces is highly relevant as microscopic foundation of cell respiration that is driven by the gradient of proton concentration across membranes.
The NONABVD project will transfer paradigms of nonadiabatic electronic relaxation to the low energy mid-IR/THz domain of biomolecular vibrational dynamics. The approach provides a description of microscopic phenomena like structural fluctuations, vibrational lifetimes and dissipation of excess energy and fully accounts for the strong impact of the fluctuating environment on biomolecular structure and dynamics. The concise theoretical description of proton or electron solvation and transfer processes in the vicinity of biological interfaces is highly relevant as microscopic foundation of cell respiration that is driven by the gradient of proton concentration across membranes.
The NONABVD project addressed manifestations of vibrational nonadiabaticity in strongly fluctuating environments. In this context, the quantification of the solvation structures of elementary charge carriers and a characterization of the electrostatic scenario at biomolecular interfaces is of highest relevance for defining electrical and transport properties. New insight was obtained into the dynamics of excess protons and hydrated electrons in aqueous polar media. We achieved a quantitative characterization of the microscopic interactions at the phosphate-water interface for biological relevant RNA structures.
The mechanistic interplay between microscopic solvation structures and high mobility of hydrated excess protons has been one of the most enduring questions in solution chemistry. Simulations of protonated water clusters embedded in the confinement of fluctuating acetonitrile solvent revealed that the dimeric H5+O2 motif interacts with its closest water neighbor in an H7+O3 unit without persistent proton localization (J. Phys. Chem. Lett. 2019, 10, 2287). We further demonstrated how continuously evolving H7+O3 structures may support proton transport within larger water solvates (ChemPhysChem, 2021, 22, 716; see also Front Cover and Cover Profile of ChemPhysChem issue 08/2021). Our findings suggest that the unique hybrid structure of the asymmetric protonated water trimer H7+O3 defines the outstanding transport properties of solvated excess protons.
The water molecules of the liquid undergo ultrafast librational motions at room temperature that induce strong electric fields in their environment. We could quantify preferred directionality and peak values of the electric fields. In presence of an external terahertz field, the strong intermolecular interactions lead to tunneling ionization (J. Phys. Chem. Lett. 2020, 11, 7717). The results reveal new aspects of the strong intermolecular interactions and open up possibilities for a manipulation of the electric properties of liquids. Our findings of polaron oscillations induced by impulsively generated solvated electrons upon probing in the THz spectral region (Phys. Rev. Lett. 2021, 126, 097401) suggest a quasi-molecular view of hydrated electrons and the first few water shells.
We succeeded in quantifying the microscopic interactions at the phosphate-water interface of macromolecular RNA structures. The combination of two-dimensional infrared (2D-IR) spectroscopy and in-depth theoretical analysis allowed to discerned coexisting hydration geometries around the phosphate groups of the double stranded RNA helix at the molecular level (J. Phys. Chem. B 2020, 124, 2132). Our microscopic modeling demonstrates that the frequency position and line shape of RNA phosphate vibrational transitions map the local electric field the water molecules exert on the phosphate group (Phys. Chem. B. 2021, 125, 3899).
We achieved to unmask the central role of contact pairs in the structure stabilization of transfer RNA (tRNA) (Phys. Chem. B. 2021, 125, 740). Phosphate-contact ion interactions at biological interface of tRNA were quantified via the particular sensitivity of the phosphate stretching vibrations to their local environment (see Image attached to the Summary for publication). The approach allowed us to identify contact pairs of Mg2+ ions and phosphate groups as a decisive structural element for minimizing the electrostatic energy. Our theoretical analysis shows that the subtle balance of attractive electrostatic forces and repulsive forces due to exchange interaction govern the frequency position of the phosphate vibration (J. Phys. Chem. Lett. 2019, 10, 6281). The quantitative analysis gives insight in the electric properties of a key biomolecule and underscore the relevance of molecular probes for elucidating the relevant molecular interactions.
The mechanistic interplay between microscopic solvation structures and high mobility of hydrated excess protons has been one of the most enduring questions in solution chemistry. Simulations of protonated water clusters embedded in the confinement of fluctuating acetonitrile solvent revealed that the dimeric H5+O2 motif interacts with its closest water neighbor in an H7+O3 unit without persistent proton localization (J. Phys. Chem. Lett. 2019, 10, 2287). We further demonstrated how continuously evolving H7+O3 structures may support proton transport within larger water solvates (ChemPhysChem, 2021, 22, 716; see also Front Cover and Cover Profile of ChemPhysChem issue 08/2021). Our findings suggest that the unique hybrid structure of the asymmetric protonated water trimer H7+O3 defines the outstanding transport properties of solvated excess protons.
The water molecules of the liquid undergo ultrafast librational motions at room temperature that induce strong electric fields in their environment. We could quantify preferred directionality and peak values of the electric fields. In presence of an external terahertz field, the strong intermolecular interactions lead to tunneling ionization (J. Phys. Chem. Lett. 2020, 11, 7717). The results reveal new aspects of the strong intermolecular interactions and open up possibilities for a manipulation of the electric properties of liquids. Our findings of polaron oscillations induced by impulsively generated solvated electrons upon probing in the THz spectral region (Phys. Rev. Lett. 2021, 126, 097401) suggest a quasi-molecular view of hydrated electrons and the first few water shells.
We succeeded in quantifying the microscopic interactions at the phosphate-water interface of macromolecular RNA structures. The combination of two-dimensional infrared (2D-IR) spectroscopy and in-depth theoretical analysis allowed to discerned coexisting hydration geometries around the phosphate groups of the double stranded RNA helix at the molecular level (J. Phys. Chem. B 2020, 124, 2132). Our microscopic modeling demonstrates that the frequency position and line shape of RNA phosphate vibrational transitions map the local electric field the water molecules exert on the phosphate group (Phys. Chem. B. 2021, 125, 3899).
We achieved to unmask the central role of contact pairs in the structure stabilization of transfer RNA (tRNA) (Phys. Chem. B. 2021, 125, 740). Phosphate-contact ion interactions at biological interface of tRNA were quantified via the particular sensitivity of the phosphate stretching vibrations to their local environment (see Image attached to the Summary for publication). The approach allowed us to identify contact pairs of Mg2+ ions and phosphate groups as a decisive structural element for minimizing the electrostatic energy. Our theoretical analysis shows that the subtle balance of attractive electrostatic forces and repulsive forces due to exchange interaction govern the frequency position of the phosphate vibration (J. Phys. Chem. Lett. 2019, 10, 6281). The quantitative analysis gives insight in the electric properties of a key biomolecule and underscore the relevance of molecular probes for elucidating the relevant molecular interactions.
We established a novel detection scheme of phosphate counter-ion interactions (J. Phys. Chem. Lett. 2019, 10, 6281) by demonstrating that the phosphate groups represent sensitive and noninvasive probes of ion geometries in a water environment. 2D-IR spectroscopy maps ions in direct contact with a phosphate group via a distinct feature in the 2D-IR spectrum. The lineshape and the time evolution of this new feature encode the fluctuations of the contact ion pair geometry and the embedding water shell. The ability of 2D-IR spectroscopy to characterize short-ranged phosphate-ion interactions in solution provides a novel analytical tool that complements currently available structural techniques. An extension of this approach to has been successfully demonstrated to complex folded tRNA (Phys. Chem. B. 2021, 125, 740) and the ionic environment of double stranded RNA (J. Phys. Chem. B. 2021, 125, 3899). The results underline the potential of 2D-IR spectroscopy as an analytical probe of phosphate-ion interactions in complex biological systems.
Our discovery of a novel generation mechanism of hydrated electrons demonstrates a multifaceted character of Coulomb interactions in the aqueous condensed phase environment (J. Phys. Chem. Lett. 2020, 11, 7717). We could quantify the electric field peak strength that result in spontaneous tunneling ionization of water molecules. Quasi-impulsively generated solvated electrons induce exceptionally long-lived polaron oscillations in the THz spectral domain (Phys. Rev. Lett. 2021, 126, 097401). The weak damping of the presumably longitudinal coherences is in stark contrast to the ultrafast decay of transverse excitations. The polaronic properties of hydrated electrons are a manifestation of the strong electric interactions in liquids.
Our discovery of a novel generation mechanism of hydrated electrons demonstrates a multifaceted character of Coulomb interactions in the aqueous condensed phase environment (J. Phys. Chem. Lett. 2020, 11, 7717). We could quantify the electric field peak strength that result in spontaneous tunneling ionization of water molecules. Quasi-impulsively generated solvated electrons induce exceptionally long-lived polaron oscillations in the THz spectral domain (Phys. Rev. Lett. 2021, 126, 097401). The weak damping of the presumably longitudinal coherences is in stark contrast to the ultrafast decay of transverse excitations. The polaronic properties of hydrated electrons are a manifestation of the strong electric interactions in liquids.