Orientations and water dynamics of photoinduced secondary charge-separated states for magnetoreception by cryptochrome

In the biological magnetic compass, blue-light photoreceptor protein of cryptochrome is thought to conduct the sensing of the Earth’s magnetic field by photoinduced sequential long-range charge-separation (CS) through a cascade of tryptophan residues, W(A)(H), W(B)(H) and W(C)(H). Mechanism of generating the weak-field sensitive radical pair (RP) is poorly understood because geometries, electronic couplings and their modulations by molecular motion have not been investigated in the secondary CS states generated prior to the terminal RP states. In this study, water dynamics control of the electronic coupling is revealed to be a key concept for sensing the direction of weak magnetic field. Geometry and exchange coupling (singlet–triplet energy gap: 2J) of photoinduced secondary CS states composed of flavin adenine dinucleotide radical anion (FAD(−•)) and radical cation W(B)(H)(+•) in the cryptochrome DASH from Xenopus laevis were clarified by time-resolved electron paramagnetic resonance. We found a time-dependent energetic disorder in 2J and was interpreted by a trap CS state capturing one reorientated water molecule at 120 K. Enhanced electron-tunneling by water-libration was revealed for the terminal charge-separation event at elevated temperature. This highlights importance of optimizing the electronic coupling for regulation of the anisotropic RP yield on the possible magnetic compass senses.