Ultraviolet Absorption Induces Hydrogen-Atom Transfer in G⋅C Watson-Crick DNA Base Pairs in Solution

• Published in: Angewandte Chemie International Edition 2015-12, Vol.54 (49), p.14719-14722
• Main Authors: Röttger, Katharina, Marroux, Hugo J. B., Grubb, Michael P., Coulter, Philip M., Böhnke, Hendrik, Henderson, Alexander S., Galan, M. Carmen, Temps, Friedrich, Orr-Ewing, Andrew J., Roberts, Gareth M.
• Format: Article
• Language: English
• Subjects: Absorption; Absorption, Physicochemical - radiation effects; Base Pairing - radiation effects; Base pairs; Bases (nucleic acids); biophysics; Cytosine; Deactivation; Deoxyribonucleic acid; DNA; DNA - chemistry; Guanine; Hydrogen; Hydrogen - chemistry; Hydrogen bonding; Hydrogen bonds; Infrared spectroscopy; Photochemistry; proton transfer; Solutions; Structural integrity; ultrafast spectroscopy; Ultraviolet absorption; Ultraviolet radiation; Ultraviolet Rays
• ISSN: 1433-7851; 1521-3773
• DOI: 10.1002/anie.201506940

Ultrafast deactivation pathways bestow photostability on nucleobases and hence preserve the structural integrity of DNA following absorption of ultraviolet (UV) radiation. One controversial recovery mechanism proposed to account for this photostability involves electron‐driven proton transfer (EDPT) in Watson–Crick base pairs. The first direct observation is reported of the EDPT process after UV excitation of individual guanine–cytosine (G⋅C) Watson–Crick base pairs by ultrafast time‐resolved UV/visible and mid‐infrared spectroscopy. The formation of an intermediate biradical species (G[−H]⋅C[+H]) with a lifetime of 2.9 ps was tracked. The majority of these biradicals return to the original G⋅C Watson–Crick pairs, but up to 10 % of the initially excited molecules instead form a stable photoproduct G*⋅C* that has undergone double hydrogen‐atom transfer. The observation of these sequential EDPT mechanisms across intermolecular hydrogen bonds confirms an important and long debated pathway for the deactivation of photoexcited base pairs, with possible implications for the UV photochemistry of DNA. Ultrafast energy‐dissipation processes after UV absorption render DNA intrinsically photostable. One of the most debated mechanisms in individual guanine–cytosine base pairs has been confirmed: A sequence of hydrogen transfers across the hydrogen bonds in the dimer lead to an efficient relaxation of the base pair back to the original structure, but up to 10 % of the excited molecules instead form a potentially mutagenic tautomer.