title: Ultrafast dynamics and anionic active states of the flavin cofactor in cryptochrome and photolyase.
abstract: We report here our systematic studies of the dynamics of four redox states of the flavin cofactor in both photolyases and insect type 1 cryptochromes. With femtosecond resolution, we observed ultrafast photoreduction of oxidized state flavin adenine dinucleotide (FAD) in subpicosecond and of neutral radical semiquinone (FADH(*)) in tens of picoseconds through intraprotein electron transfer mainly with a neighboring conserved tryptophan triad. Such ultrafast dynamics make these forms of flavin unlikely to be the functional states of the photolyase/cryptochrome family. In contrast, we find that upon excitation the anionic semiquinone (FAD(*-)) and hydroquinone (FADH(-)) have longer lifetimes that are compatible with high-efficiency intermolecular electron transfer reactions. In photolyases, the excited active state (FADH(-)*) has a long (nanosecond) lifetime optimal for DNA-repair function. In insect type 1 cryptochromes known to be blue-light photoreceptors the excited active form (FAD(*-)*) has complex deactivation dynamics on the time scale from a few to hundreds of picoseconds, which is believed to occur through conical intersection(s) with a flexible bending motion to modulate the functional channel. These unique properties of anionic flavins suggest a universal mechanism of electron transfer for the initial functional steps of the photolyase/cryptochrome blue-light photoreceptor family.
authors.affiliation: Department of Physics, The Ohio State University, Columbus, Ohio 43210, USA.
authors.forename: Ya-Ting
authors.initials: YT
authors.lastname: Kao
authors.forename: Chuang
authors.initials: C
authors.lastname: Tan
authors.forename: Sang-Hun
authors.initials: SH
authors.lastname: Song
authors.forename: Nuri
authors.initials: N
authors.lastname: Oztürk
authors.forename: Jiang
authors.initials: J
authors.lastname: Li
authors.forename: Lijuan
authors.initials: L
authors.lastname: Wang
authors.forename: Aziz
authors.initials: A
authors.lastname: Sancar
authors.forename: Dongping
authors.initials: D
authors.lastname: Zhong
mesh_terms: D000818:Animals; D002080:Butterflies / Q000201:enzymology; D003067:Coenzymes / Q000737:chemistry*; D056931:Cryptochromes; D004255:Deoxyribodipyrimidine Photo-Lyase / Q000737:chemistry*; D004579:Electron Transport; D044927:Electron-Transferring Flavoproteins / Q000737:chemistry*; D005182:Flavin-Adenine Dinucleotide / Q000737:chemistry*; D005415:Flavins / Q000737:chemistry*; D005420:Flavoproteins / Q000737:chemistry*; D010084:Oxidation-Reduction; D011487:Protein Conformation
chemical_list: D003067:Coenzymes; D056931:Cryptochromes; D044927:Electron-Transferring Flavoproteins; D005415:Flavins; D005420:Flavoproteins; D005182:Flavin-Adenine Dinucleotide; D004255:Deoxyribodipyrimidine Photo-Lyase