Electron-driven proton transfer relieves excited-state antiaromaticity in photoexcited DNA base pairs
Year: 2020
Type: article
Abstract: Before the development of an ozone layer in the Archean atmosphere, the flux of UV radiation reaching Earth was suggested to be several orders of magnitude higher than it is today. For the emerging biomolecules, constant exposure to strong UV irradiation meant that useful molecules had to be resistant to UV damage and harmful photochemical reactions. From this prebiotic environment, the Watson–Crick structures of A·T and G·C base pairs survived to encode genetic information—and the photostability of these winning pairs in this specific arrangement is astonishing. Upon UV irradiation, the photoexcited canonical base pairs undergo proton-coupled electron transfer (PCET), followed by non-radiative decay, and convert internally to the electronic ground state within picoseconds. But the underlying reason why this process happens so efficiently has not been explained. Here we show that efficient photodeactivation in isolated base pairs are driven by antiaromaticity relief during PCET. According to computed nucleus independent chemical shifts, the A·T and G·C base pairs are aromatic in the electronic ground state, but the purines become highly antiaromatic in the first 1 ππ* state, and PCET relieves this excited-state antiaromaticity. We found especially pronounced antiaromaticity relief for the major PCET pathway of isolated Watson–Crick A·T and G·C base pairs, when compared to alternative proton transfer routes or to PCET reactions in non-canonical pairs. Our findings suggest that excited-state deactivation of isolated base pairs are tied to sudden changes in aromaticity and antiaromaticity within the picoseconds that follow a strike of UV-light.
Source: Chemical Science
DOI: 10.1039/d0sc02294b
Institutions: University of Houston, Uppsala University
Language: English
Subfield: Physical and Theoretical Chemistry
Field: Chemistry
Domain: Physical Sciences
Open Access status: diamond
Awards: G154433060, MRI: Acquisition of a High Performance Computing System for Science and Engineering Research and Education at the University of Houston, Unravelling the Scope and Limitations of the Excited State Aromaticity and Antiaromaticity Concepts, CAREER: Computational Studies of Aromaticity-Modulated Interactions in Supramolecular Chemistry, Excited State (Anti)Aromaticity and Heavy Group 14 Element Chemistry: Fundamental Studies with Potentials for Applications, G767680462, G7799710285, Unlocking Biologically-Relevant Opportunities Through Applications of Excited-State Aromaticity and Antiaromaticity
OpenAlex ID: W3048769630