Unveiling Electron Dynamics and Structural Rearrangements: Insights into Photoinduced Processes in Biomolecules

Understanding the response of molecules to XUV-UV radiation, particularly for biomolecules like RNAs, DNAs, and other biomolecules, is crucial. When exposed to XUV-UV radiation, various photochemical processes occur, including photodamage and photoprotection. These processes encompass irreversible modifications in DNA/RNA caused by photodamage and reversible reactions like photo-tautomerization involved in photoprotection. Gaining insights into the factors influencing these processes at the molecular level is essential for both fundamental research and technological applications. Electron dynamics dominate the initial response of molecules to photoexcitation or ionization on sub- to few-femtosecond timescales. This electron rearrangement can affect the molecule’s relaxation pathways, weaken specific bonds, and trigger fragmentation. Therefore, comprehending electron dynamics on sub-femtosecond timescales is crucial for studying and controlling various photo-triggered biomolecular processes.

In a recent study published in the peer-reviewed Journal of Manufacturing Processes, Kalyani Chordiya, Balázs Nagyillés and Dr. Mousumi Upadhyay Kahaly from University of Szeged Hungary, Zsolt Diveki from ELI-ALPS, ELI-HU Non-Profit Ltd and Dr. Victor Despré, Felix Zeller and Alexander I. Kuleff from Universität Heidelberg conducted density functional theory calculations to optimize the geometry of uracil tautomers and explore electron dynamics resulting from ionization. They emphasized the importance of nuclear dynamics and non-adiabatic effects in understanding structural rearrangements. Uracil was chosen as a bio-relevant prototype molecule due to its presence in biological macromolecules as a nucleobase. Uracil exists in multiple tautomeric forms, with the “keto-U” and “enol U” forms having the lowest energy. By selecting uracil, the researchers aimed to examine ultrafast charge migration at the molecular level, shedding light on the fundamental mechanisms underlying the photoinduced response in biomatter.

Using density functional theory (DFT) and the Gamess-UK package, the research team performed a computational analysis of the electronic structures and dynamics of the keto and enol uracil tautomers. They optimized the tautomer geometry at the PBE0/def2-TZVP level and found excellent agreement between the resulting bond lengths and experimental values. Additionally, the researchers calculated the Hartree-Fock orbital energies of the tautomers using the same basis set. The analysis of orbital energies revealed significant differences in the electronic structures of the two tautomers, indicating distinct electronic properties even at the Hartree-Fock level. The ionization spectra of the molecules were computed using the non-Dyson method, revealing notable differences between the keto and enol forms and indicating the presence of strong correlation effects in both tautomers. The researchers also studied the charge dynamics initiated by ionization using hole density analysis, providing insights into charge migration within the molecules.

The authors shed light on the average behavior of ionized electrons and obtained crucial insights into charge migration processes in the keto and enol tautomers of uracil. By analyzing electron dynamics resulting from ionization, they acquired valuable information about the movement and redistribution of charges within the molecules. This information was essential for comprehending the underlying reactivity and properties of these tautomeric forms. Furthermore, the researchers acknowledged the significant influence of nuclear dynamics and nonadiabatic effects on electron dynamics. Nuclear dynamics referred to the movement of atomic nuclei within the molecule, while non-adiabatic effects encompassed the interactions between electrons and nuclei as they dynamically adjusted to fluctuating energy levels. Both factors played a crucial role in determining the overall behavior and structural rearrangements of uracil tautomers. To achieve a more accurate and comprehensive analysis of tautomeric behavior in uracil, it was necessary to consider the interaction between nuclear and electronic dynamics.

In summary, the researchers employed density functional theory calculations to investigate electron dynamics resulting from ionization in uracil tautomers. Their study shed light on charge migration processes and emphasized the significance of nuclear dynamics and non-adiabatic effects in understanding structural rearrangements and the photoinduced response in biomolecules. The analysis revealed distinct electronic properties between the keto and enol forms, highlighting the necessity of an approach that considers both electronic and nuclear dynamics to fully comprehend the behavior of these tautomeric molecules. The findings of this study have potential implications for technological applications related to biomolecules and photochemistry. Understanding the behavior of biomolecules under photoexcitation or ionization is crucial for the development of technologies such as photomedicine, DNA damage repair, and biomolecular imaging. By elucidating the underlying processes and factors influencing these reactions, this study contributes to the advancement of such technologies.