Kattnig Daniel R, Solov'yov Ilia A, Hore P J
Department of Chemistry, University of Oxford, Physical and Theoretical Chemistry Laboratory, OX1 3QZ, UK.
Phys Chem Chem Phys. 2016 May 14;18(18):12443-56. doi: 10.1039/c5cp06731f. Epub 2016 Mar 29.
The magnetic compass sense of migratory birds is thought to rely on magnetically sensitive radical pairs formed photochemically in cryptochrome proteins in the retina. An important requirement of this hypothesis is that electron spin relaxation is slow enough for the Earth's magnetic field to have a significant effect on the coherent spin dynamics of the radicals. It is generally assumed that evolutionary pressure has led to protection of the electron spins from irreversible loss of coherence in order that the underlying quantum dynamics can survive in a noisy biological environment. Here, we address this question for a structurally characterized model cryptochrome expected to share many properties with the putative avian receptor protein. To this end we combine all-atom molecular dynamics simulations, Bloch-Redfield relaxation theory and spin dynamics calculations to assess the effects of spin relaxation on the performance of the protein as a compass sensor. Both flavin-tryptophan and flavin-Z˙ radical pairs are studied (Z˙ is a radical with no hyperfine interactions). Relaxation is considered to arise from modulation of hyperfine interactions by librational motions of the radicals and fluctuations in certain dihedral angles. For Arabidopsis thaliana cryptochrome 1 (AtCry1) we find that spin relaxation implies optimal radical pair lifetimes of the order of microseconds, and that flavin-Z˙ pairs are less affected by relaxation than flavin-tryptophan pairs. Our results also demonstrate that spin relaxation in isolated AtCry1 is incompatible with the long coherence times that have been postulated to explain the disruption of the avian magnetic compass sense by weak radiofrequency magnetic fields. We conclude that a cryptochrome sensor in vivo would have to differ dynamically, if not structurally, from isolated AtCry1. Our results clearly mark the limits of the current hypothesis and lead to a better understanding of the operation of radical pair magnetic sensors in noisy biological environments.
候鸟的磁罗盘感知被认为依赖于视网膜中隐花色素蛋白通过光化学作用形成的对磁场敏感的自由基对。该假说的一个重要条件是电子自旋弛豫足够缓慢，以便地球磁场能对自由基的相干自旋动力学产生显著影响。一般认为，进化压力导致了对电子自旋的保护，使其不会不可逆地失去相干性，从而使潜在的量子动力学能够在嘈杂的生物环境中存续。在此，我们针对一个结构已明确的隐花色素模型来探讨这个问题，该模型预计与假定的鸟类受体蛋白具有许多共同特性。为此，我们结合全原子分子动力学模拟、布洛赫 - 雷德菲尔德弛豫理论和自旋动力学计算，以评估自旋弛豫对该蛋白作为罗盘传感器性能的影响。我们研究了黄素 - 色氨酸和黄素 - Z˙自由基对（Z˙是一种没有超精细相互作用的自由基）。弛豫被认为是由自由基的摆动运动以及某些二面角的波动对超精细相互作用的调制引起的。对于拟南芥隐花色素1（AtCry1），我们发现自旋弛豫意味着自由基对的最佳寿命约为微秒量级，并且黄素 - Z˙对受弛豫的影响比黄素 - 色氨酸对小。我们的结果还表明，孤立的AtCry1中的自旋弛豫与为解释弱射频磁场对鸟类磁罗盘感知造成的干扰而假定的长相干时间不相符。我们得出结论，体内的隐花色素传感器在动力学上（即便不是结构上）必定与孤立的AtCry1不同。我们的结果清楚地标明了当前假说的局限性，并有助于更好地理解自由基对磁传感器在嘈杂生物环境中的运作。
