First-principles modeling of redox and ultrafast photoinduced charge transfer processes in biomolecules
Embargo Date
2021-03-17
OA Version
Citation
Abstract
Redox and photoinduced charge transfer processes are ubiquitous in nature and industry. They play a crucial role in energy storage, photovoltaic devices, and biological processes, including photosynthesis, respiration, DNA repair, magnetoreception, and many more. While an experiment often provides a convoluted overall picture, typically on ensembles of molecules, first-principles theoretical description in turn enables atomistic description of the process of interest. This description also allows one to disentangle multiple factors contributing to the overall efficiency of the process, e.g. the role of specific interactions on electron transfer or redox processes in proteins. Therefore, accurate tools enabling predictive simulation of redox conversions and electron transfer events are highly desirable.
The focus of this dissertation is two-fold. First, new computational models and protocols that enable robust and reliable simulations of redox and electron transfer processes in a heterogeneous environment such as protein-solvent environment are proposed. Second, the developed techniques were used to study the redox and photoactivation processes in a cryptochrome protein, a candidate for a molecular compass in migratory birds. This work consists of four major components: (i) development of a computational protocol for accurate simulations of redox potentials of molecules in homogeneous solutions; (ii) formulation of a computational model enabling robust calculation of redox potentials of proteins; (iii) development and implementation of eMap, an online platform for mapping electron/hole hopping pathways in proteins; and (iv) simulation of photoinduced electron transfer, the first step of photoactivation in Cryptochrome 1, employing state-of-the-art electronic structure theory, hybrid polarizable QM/MM, and quantum dynamics methods. The approaches and protocols discussed in the dissertation enable robust and accurate first-principles evaluation of redox potentials and description of dynamics of ultrafast photoinduced electron transfer in a complex environment. The results point to the key role of polarization and long-range electrostatic interactions for the accuracy of the computed energetic parameters. The electronic-nuclear interactions are found to be crucial in driving nonadiabatic electron transfer in a complex environment. The results of the present work shed light onto the role of ATP and other cellular metabolites on formation of semireduced FAD in cryptochromes.