Dual Photochemical Reaction Pathway in Flavin-Based Photoreceptor LOV Domain: A Combined Quantum-Mechanics/Molecular-Mechanics Investigation.

The primary photochemical reaction of the light, oxygen, and voltage (LOV) domain of the blue-light photosensor YtvA of Bacillus subtilis were investigated using high-level QM(DFT/MRCI)/MM methods. After blue-light excitation, the Sγ atom of the reactive cysteine forms a covalent bond with the C4a of the flavin mononucleotide (FMN) ring. Two conformations for the side chain of reactive cysteine with occupancies of 70% (conf A) and 30% (conf B) are observed in the X-ray crystallographic structures of the YtvA-LOV ( Möglich , A. ; Moffat , K. J. Mol. Biol. 2007 , 373 , 112 - 126 ). In conf A, the thiol group is directed toward the dimethylbenzene moiety of the FMN ring whereas it is placed directly above the N5 atom of the FMN ring in conf B. Starting from both conformations, the singlet and triplet excited pathways were evaluated. The singlet states excited from conf A decay nonradiatively to the triplet states by intersystem crossing (ISC). After the formation of a neutral biradical, the triplet states cross over to the electronic ground state by a second ISC and the adducts are efficiently formed. The singlet states excited from conf B are located near the S1/S0 conical intersection (CIn). A major fraction returns to the initial states through the CIn. The rest may directly reach the adduct state. Thus, the photoexcitation has a dual reaction pathway. In YtvA-LOV, it is inferred that the efficient triplet excitation from conf A was chosen by bypassing the less efficient singlet excitation from conf B.