Electron spin relaxation can enhance the performance of a cryptochrome-based magnetic compass sensor

The radical pair model of the avian magnetoreceptor relies on long‐lived electron spin coherence. Dephasing, resulting from interactions of the spins with their fluctuating environment, is generally assumed to degrade the sensitivity of this compass to the direction of the Earth's magnetic field. Here we argue that certain spin relaxation mechanisms can enhance its performance. We focus on the flavin‐tryptophan radical pair in cryptochrome, currently the only candidate magnetoreceptor molecule. Correlation functions for fluctuations in the distance between the two radicals in Arabidopsis thaliana cryptochrome 1 were obtained from molecular dynamics simulations and used to calculate the spin relaxation caused by modulation of the exchange and dipolar interactions. We find that intermediate spin relaxation rates afford substantial enhancements in the sensitivity of the reaction yields to an Earth‐strength magnetic field. Supported by calculations using toy radical pair models, we argue that these enhancements could be consistent with the molecular dynamics and magnetic interactions in avian cryptochromes

On the optimal relative orientation of radicals in the cryptochrome magnetic compass

This is the author accepted manuscript. The final version is available from AIP Publishing via the DOI in this record.Birds appear to be equipped with an innate magnetic compass. One biophysical model of this sense relies on spin dynamics in photogenerated radical pairs in the protein cryptochrome. This study employs a systematic approach to predict the dependence of the compass sensitivity on the relative orientation of the constituent radicals for spin systems comprising up to 21 hyperfine interactions. Evaluating measures of compass sensitivity (anisotropy) and precision (optimality) derived from the singlet yield, we find the ideal relative orientations for the radical pairs consisting of the flavin anion (F•-) coupled with a tryptophan cation (W•+) or tyrosine radical (Y•). For the geomagnetic field, the two measures are found to be anticorrelated in [F•- W•+]. The angle spanned by the normals to the aromatic planes of the radicals is the decisive parameter determining the compass sensitivity. The third tryptophan of the tryptophan triad/tetrad, which has been implicated with magnetosensitive responses, exhibits a comparably large anisotropy, but unfavorable optimality. Its anisotropy could be boosted by an additional ∼50% by optimizing the relative orientation of the radicals. For a coherent lifetime of 1 μs, the maximal relative anisotropy of [F•- W•+] is 0.27%. [F•- Y•] radical pairs outperform [F•- W•+] for most relative orientations. Furthermore, anisotropy and optimality can be simultaneously maximized. The entanglement decays rapidly, implicating it as a situational by-product rather than a fundamental driver within the avian compass. In magnetic fields of higher intensity, the relative orientation of radicals in [F•- W•+] is less important than for the geomagnetic field.Engineering and Physical Sciences Research Council (EPSRC

No evidence for magnetic field effects on the behaviour of Drosophila

Migratory songbirds have the remarkable ability to extract directional information from the Earth’s magnetic field1,2. The exact mechanism of this light-dependent magnetic compass sense, however, is not fully understood. The most promising hypothesis focuses on the quantum spin dynamics of transient radical pairs formed in cryptochrome proteins in the retina3,4,5. Frustratingly, much of the supporting evidence for this theory is circumstantial, largely because of the extreme challenges posed by genetic modification of wild birds. Drosophila has therefore been recruited as a model organism, and several influential reports of cryptochrome-mediated magnetic field effects on fly behaviour have been widely interpreted as support for a radical pair-based mechanism in birds6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23. Here we report the results of an extensive study testing magnetic field effects on 97,658 flies moving in a two-arm maze and on 10,960 flies performing the spontaneous escape behaviour known as negative geotaxis. Under meticulously controlled conditions and with vast sample sizes, we have been unable to find evidence for magnetically sensitive behaviour in Drosophila. Moreover, after reassessment of the statistical approaches and sample sizes used in the studies that we tried to replicate, we suggest that many—if not all—of the original results were false positives. Our findings therefore cast considerable doubt on the existence of magnetic sensing in Drosophila and thus strongly suggest that night-migratory songbirds remain the organism of choice for elucidating the mechanism of light-dependent magnetoreception

Data underpinning Fig 2A and 2B.

(MAT)</p

Reaction schemes used to explain the putative magnetic field effect of flavin semiquinone (FH^•)/superoxide radical pairs.

A) The radical pair-based process as suggested in [4]. The singlet and triplet radical pair states are indicated by superscripts 1 and 3, respectively. B) An alternative reaction scheme assuming a radical triad involving the additional radical A•−. Radical A•− can undergo a spin-selective scavenging reaction with FH•. If is subject to fast spin relaxation, the magnetosensitivity of this reaction can be modelled as that of an initially uncorrelated FH•/A•− pair. Spin multiplicities have not been indicated for simplicity; DHA stands for dehydroascorbic acid; the rate constants kX, and kF describe radical recombination processes in the singlet state of the respective pairs; kE and describe the escape of radicals; here, FH• is considered immobile, because it is assumed to be protein-bound. The reaction processes are described in detail in the Model section of the main text.</p

Quantum yield of escaping from the three-radical reaction process (B and D) and associated hypomagnetic field effect (A and C) for free (A and B) and bound (C and D) flavin.

The quantum yields and MFEs are plotted as a function of the scavenging rate constant kX (accounting for FH•/A•− recombination) and kΣ the effective depopulation rate constant of the triad system (defined in Eq (5)). φ = 0, i.e., we assume an efficient oxidation processes for which superoxide is only released if the FH• is scavenged by A•−. The magnetic field amounted to 55.26 μT and 0.29 μT for the geomagnetic reference field (GMF) and the hypomagnetic field (HMF), respectively. The MFE is reported as yield in the HMF relative to the GMF. The used hyperfine parameters are reported in Table A in S1 Text. For the bound flavin radical, the yields have been averaged over the orientation of the magnetic field with respect to the radicals. The raw simulation data have been provided as S1(A), S1(B), S2(C) and S2(D) Data.</p