Analysis of the primary photocycle reactions occurring in the light, oxygen, and voltage blue-light receptor by multiconfigurational quantum-chemical methods

The photocycle reactions occurring between the flavin mononucleotide cofactor and the reactive cysteine residue in the blue-light photoreceptor domain light, oxygen, and voltage (LOV) were modeled for a system consisting of lumiflavin and thiomethanol. The electronic structure and energies of the reactive species were estimated using the CASSCF and MCQDPT2 quantum-chemical methods. The reaction pathway for the S-C4a covalent adduct formation in the triplet state was determined. Concerted electron and proton transfer from the thiol to the flavin in the triplet electronic state results in a biradical complex that is, however, unstable because its structure corresponds to a triplet-singlet crossing. The covalent adduct dissociation in the ground electronic state is a reverse of the photoreaction proceeding via a single energy barrier for hydrogen transfer. Thus, both photo- and dark reactions were found to be single-step chemical transformations occurring without stable intermediates. The photoreaction yielding the S-C4a covalent adduct is an intrinsic property of the isoalloxazine-thiol complex in the specific geometry arranged by the protein in LOV. The S-C4a covalent adduct between lumiflavin and thiomethanol is rather stable implying that in LOV its dissociation is facilitated by the protein.