Hamada Misato, Iwata Tatsuya, Fuki Masaaki, Kandori Hideki, Weber Stefan, Kobori Yasuhiro
Department of Chemistry, Graduate School of Science, Kobe University, 1‒1 Rokkodai‒cho, Nada‒ku, Kobe, 657‒8501, Japan.
Department of Pharmaceutical Sciences, Toho University, Funabashi, Chiba, 274‒8510, Japan.
Commun Chem. 2021 Sep 30;4(1):141. doi: 10.1038/s42004-021-00573-4.
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(H), W(H) and W(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(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.
在生物磁罗盘系统中，隐花色素的蓝光感光蛋白被认为是通过一系列色氨酸残基（W(H)、W(H)和W(H)）进行光诱导的连续长程电荷分离（CS）来感知地球磁场的。由于在终端自由基对（RP）状态之前产生的二级CS状态中，其几何结构、电子耦合及其受分子运动的调制尚未得到研究，因此产生弱场敏感自由基对（RP）的机制仍知之甚少。在本研究中，电子耦合的水动力学控制被揭示为感知弱磁场方向的关键概念。通过时间分辨电子顺磁共振，阐明了非洲爪蟾隐花色素DASH中由黄素腺嘌呤二核苷酸自由基阴离子（FAD）和自由基阳离子W(H)组成的光诱导二级CS状态的几何结构和交换耦合（单重态-三重态能隙：2J）。我们发现2J存在时间依赖性的能量无序现象，并将其解释为在120 K时捕获一个重新取向水分子的陷阱CS状态。研究还揭示了在升高温度下，水的振动增强了终端电荷分离事件的电子隧穿。这突出了优化电子耦合对于调节可能的磁罗盘感应上各向异性RP产率的重要性。
