Alternative radical pairs for cryptochrome-based magnetoreception - PubMed (original) (raw)

Alternative radical pairs for cryptochrome-based magnetoreception

Alpha A Lee et al. J R Soc Interface. 2014.

Abstract

There is growing evidence that the remarkable ability of animals, in particular birds, to sense the direction of the Earth's magnetic field relies on magnetically sensitive photochemical reactions of the protein cryptochrome. It is generally assumed that the magnetic field acts on the radical pair [FAD•- TrpH•+] formed by the transfer of an electron from a group of three tryptophan residues to the photo-excited flavin adenine dinucleotide cofactor within the protein. Here, we examine the suitability of an [FAD•- Z•] radical pair as a compass magnetoreceptor, where Z• is a radical in which the electron spin has no hyperfine interactions with magnetic nuclei, such as hydrogen and nitrogen. Quantum spin dynamics simulations of the reactivity of [FAD•- Z•] show that it is two orders of magnitude more sensitive to the direction of the geomagnetic field than is [FAD•- TrpH•+] under the same conditions (50 µT magnetic field, 1 µs radical lifetime). The favourable magnetic properties of [FAD•- Z•] arise from the asymmetric distribution of hyperfine interactions among the two radicals and the near-optimal magnetic properties of the flavin radical. We close by discussing the identity of Z• and possible routes for its formation as part of a spin-correlated radical pair with an FAD radical in cryptochrome.

Keywords: animal navigation; flavin; magnetic compass; radical pair mechanism; spin dynamics.

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Figures

Figure 1.

Figure 1.

Representations of the seven largest hyperfine tensors in (a) FAD_•−_ and (b) TrpH_•_+ superimposed on the structures of the parent molecules. The orientation of TrpH relative to FAD is that of Trp-342 relative to the FAD cofactor in the cryptochrome from D. melanogaster [28,29]. The hyperfine tensors, which are listed in the electronic supplementary material, tables S1 and S2, were calculated in Gaussian-03 [30] at the UB3LYP/EPR-III level of theory. The adenine group of FAD is omitted and the ribityl side chain is truncated after the first carbon. Only the side chain and the β-CH2 group of TrpH are shown.

Figure 2.

Figure 2.

Singlet yield anisotropy plots for the radical pairs (a) [FAD_•−_ TrpH_•_+], (b) [Z_•_ TrpH_•_+] and (c) [FAD_•−_ Z_•], where Z_• is a radical with no hyperfine interactions. The spherical average of the reaction yield, formula image i.e. the part of Φ_S that is independent of the magnetic field direction, has been subtracted to reveal the anisotropic component, which contains the directional information. The distance in any direction from the centre of the pattern to the surface is proportional to the value of formula image when the magnetic field has that direction. Red/blue regions correspond to reaction yields larger/smaller than formula image FAD_•− and TrpH_•_+ each have the seven hyperfine interactions shown in figure 1. The values of Δ_Φ_S for the three radical pairs are as shown. The three anisotropy patterns are not drawn to scale. The coordinate system is that of FAD_•−_ (figure 1_a_). The orientation of TrpH_•_+ relative to FAD_•−_ is as shown in figure 1. Details of the simulations are given in the electronic supplementary material.

Figure 3.

Figure 3.

Singlet yield anisotropy plots for radical pairs containing a single hyperfine interaction selected from those in FAD_•−_ and TrpH_•_+ (electronic supplementary material, tables S1 and S2). The values of Δ_Φ_S for the 10 spin systems are as shown. The anisotropy patterns are not drawn to scale. The coordinate system is that of FAD_•−_ (figure 1_a_). The orientation of TrpH_•_+ relative to FAD_•−_ is as shown in figure 1. Details of the simulations are given in the electronic supplementary material.

Figure 4.

Figure 4.

Calculations of the reaction yield anisotropy Δ_Φ_S of simple model systems. (a) Two nitrogens in the same radical (solid line) and in different radicals (dashed line). Axx = Ayy = 0 for both nuclei, parallel hyperfine _z_-axes, formula image The graphs show Δ_Φ_S as a function of formula image the isotropic hyperfine coupling of the second nitrogen. (b) Two nitrogens in the same radical (solid line) and in different radicals (dashed line). Axx = Ayy = 0 for both nuclei, formula image formula image The graphs show Δ_Φ_S as a function of the angle _ξ_12 between the _z_-axes of the two hyperfine tensors. (c) Two nitrogens and a hydrogen with an isotropic hyperfine interaction, formula image The hydrogen is either in the same radical as the nitrogens (solid line) or in the other radical (dashed line). Axx = Ayy = 0 for both nitrogens, formula image formula image parallel hyperfine axes. The graphs show Δ_Φ_S as a function of formula image

Figure 5.

Figure 5.

Ascorbyl radical. The isotropic 1H hyperfine interactions are as indicated [52]. (Online version in colour.)

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References

    1. Mouritsen H, Hore PJ. 2012. The magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds. Curr. Opin. Neurobiol. 22, 343–352. (10.1016/j.conb.2012.01.005) - DOI - PubMed
    1. Lohmann KJ. 2010. Q&A animal behaviour: magnetic-field perception. Nature 464, 1140–1142. (10.1038/4641140a) - DOI - PubMed
    1. Wiltschko R, Stapput K, Thalau P, Wiltschko W. 2010. Directional orientation of birds by the magnetic field under different light conditions. J. R. Soc. Interface 7, S163–S177. (10.1098/rsif.2009.0367.focus) - DOI - PMC - PubMed
    1. Kirschvink JL, Winklhofer M, Walker MM. 2010. Biophysics of magnetic orientation: strengthening the interface between theory and experimental design. J. R. Soc. Interface 7, S179–S191. (10.1098/rsif.2009.0491.focus) - DOI - PMC - PubMed
    1. Ritz T, Adem S, Schulten K. 2000. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78, 707–718. (10.1016/S0006-3495(00)76629-X) - DOI - PMC - PubMed

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