Photoinduced Radical Pairs in Cryptochromes: Possible Candidates for the Magnetic Compass of Migratory Birds
Final Report Abstract
The biophysics and biochemistry behind the birds’ magnetic compass are for the most part obscure. Of the two currently popular hypotheses, one is based on magnetically sensitive photochemical reactions in the retina, namely light-induced radical pairs in cryptochrome, a blue-light photoreceptor. If this mechanism proves to be correct, it will be one example of Nature using fundamentally quantum behaviour to achieve something that would be essentially impossible by means of more conventional chemistry, in this case the coherent spin dynamics of radical pairs. A key property of radical pairs allowing them to be sensitive to magnetic interactions orders of magnitude smaller than kBT is the conservation of electron spin during their chemical transformations. As a consequence, radical pairs are formed with the same spin multiplicity (singlet or triplet) as their precursors. In general, neither of these is an eigenstate of the spin Hamiltonian, consequentially leading to coherent evolution of the radical pair that is determined by the hyperfine interaction between the electron spins of the radical pair and the surrounding nuclei and, crucially for a compass, also by their interactions with an external magnetic field. The research program extended previous studies on the magnetic field effects exhibited by photolyase, a close relative of cryptochromes, and involved the search for and characterisation of effects in cryptochromes of magnetic fields, both experimentally and theoretically. Questions addressed included: Do cryptochromes show magnetic field effects as previously found for photolyase? Can magnetic field effects be regarded as a more general feature of radical pairs formed in proteins of the cryptochrome/photolyase family? Are cryptochromes capable of sensing such weak magnetic fields as the Earth’s? What determines the strength of the magnetic field effect and the sensitivity to weak fields? Experimentally, the focus was on characterising different cryptochromes, both from Xenopus laevis (XlCry) and Drosophila melanogaster (DmCry), using transient absorption spectroscopy to probe the influence of small external magnetic fields on the radical-pair kinetics. Both cryptochromes exhibited magnetic field effects. For XlCry, experimental parameters such as solution viscosity, concentration of added redox agents, and buffer conditions were systematically altered, resulting in interesting effects. A general trend observed is the increase of magnetic field effects with increasing viscosity. The maximum magnetic field effect observed for XlCry, approx. 35%, is much higher and unprecedented for any protein of the cryptochrome/photolyase family investigated so far. Furthermore, the shape of the MARY curves recorded for XlCry are much steeper compared to both EcPL and AtCry1. This points towards differences in the kinetics of the ET steps in the proteins and in particular to the stabilisation of the charge separation on the terminal Trp, resulting in altered relaxation rates of the radical pair. The theoretical modelling focussed on two different aspects. One was the effect of different hyperfine coupling schemes on the “Zeeman resonance” reported in vivo for migratory birds exposed to radiofrequency fields of different frequency in order to try to understand this behaviour of the radical pairs from a theoretical perspective. The other focussed on the role of entanglement and sources of magnetic anisotropy in radical pair-based avian magnetoreceptors. Here we could show that a radical pair can exhibit magnetic compass properties even when its initial electron spin state is neither entangled nor coherent. Furthermore, the compass properties of a radical pair with many mutually cancelling hyperfine interactions could be “rescued” by having a triplet, rather than a singlet, precursor state, given that the triplet is spin-polarised by anisotropic intersystem crossing, as it is usually the case.
Publications
- Unexpected Electron Transfer in Cryptochrome Identified by Time-Resolved EPR Spectroscopy. Angew. Chem. Int. Ed. 50 (2011) 12647–12651
T. Biskup, K. Hitomi, E. D. Getzoff, S. Krapf, T. Koslowski, E. Schleicher, and S. Weber
- Entanglement and Sources of Magnetic Anisotropy in Radical Pair-Based Avian Magnetoreceptors. Phys. Rev. Lett. 109 (2012) 220501
H. J. Hogben, T. Biskup, and P. J. Hore
- Magnetically sensitive light-induced reactions in cryptochrome are consistent with ist proposed role as a magnetoreceptor. Proc. Natl. Acad. Sci. U.S.A. 109 (2012) 4774–4779
K. Maeda, A. J. Robinson, K. B. Henbest, H. J. Hogben, T. Biskup, M. Ahmad, E. Schleicher, S. Weber, C. R. Timmel, and P. J. Hore
(See online at https://doi.org/10.1073/pnas.1118959109)
