Ultrafast dynamics and anionic active states of the flavin cofactor in cryptochrome and photolyase.
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.
Kao
Ya-Ting
YT
Department of Physics, The Ohio State University, Columbus, Ohio 43210, USA.
Tan
Chuang
C
Song
Sang-Hun
SH
Oztürk
Nuri
N
Li
Jiang
J
Wang
Lijuan
L
Sancar
Aziz
A
Zhong
Dongping
D
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
D003067:Coenzymes; D056931:Cryptochromes; D044927:Electron-Transferring Flavoproteins; D005415:Flavins; D005420:Flavoproteins; D005182:Flavin-Adenine Dinucleotide; D004255:Deoxyribodipyrimidine Photo-Lyase