Sensitivity enhancement of radical-pair magnetoreceptors as a result of spin decoherence.

Electron spin relaxation is, on many occasions, considered an elephant in the room that challenges the idea of a radical-pair compass, a leading hypothesis for the navigation of migratory avian species. It has been widely recognized that an effective radical-pair magnetoreceptor requires a relaxation time that is long enough for an external magnetic field as weak as the geomagnetic field to significantly modify the coherent spin dynamics. However, previous studies proposed that certain spin relaxation, far quicker than the radical recombination reactions, could enhance, rather than degrade, the directional sensitivity of a radical-pair magnetoreceptor. Here, I investigate relaxation effects on the singlet-triplet interconversion of a model radical pair and find that the enhancement effect originates from population relaxation over a period of several microseconds as a result of efficient spin decoherence. Insights into the truncated spin systems shed light on the physics behind them. I further investigate the possibilities of such enhancement in cryptochrome-based magnetoreception, in which electron hopping takes place between tryptophan residues.

Singlet-triplet dephasing in radical pairs in avian cryptochromes leads to time-dependent magnetic field effects.

Cryptochrome 4a (Cry4a) has been proposed as the sensor at the heart of the magnetic compass in migratory songbirds. Blue-light excitation of this protein produces magnetically sensitive flavin-tryptophan radical pairs whose properties suggest that Cry4a could indeed be suitable as a magnetoreceptor. Here, we use cavity ring-down spectroscopy to measure magnetic field effects on the kinetics of these radical pairs in modified Cry4a proteins from the migratory European robin and from nonmigratory pigeon and chicken. B1/2, a parameter that characterizes the magnetic field-dependence of the reactions, was found to be larger than expected on the basis of hyperfine interactions and to increase with the delay between pump and probe laser pulses. Semiclassical spin dynamics simulations show that this behavior is consistent with a singlet-triplet dephasing (STD) relaxation mechanism. Analysis of the experimental data gives dephasing rate constants, rSTD, in the range 3-6 × 107 s-1. A simple "toy" model due to Maeda, Miura, and Arai [Mol. Phys. 104, 1779-1788 (2006)] is used to shed light on the origin of the time-dependence and the nature of the STD mechanism. Under the conditions of the experiments, STD results in an exponential approach to spin equilibrium at a rate considerably slower than rSTD. We attribute the loss of singlet-triplet coherence to electron hopping between the second and third tryptophans of the electron transfer chain and comment on whether this process could explain differences in the magnetic sensitivity of robin, chicken, and pigeon Cry4a's.

On the anisotropic weak magnetic field effect in radical-pair reactions.

For more than 60 years, scientists have been fascinated by the fact that magnetic fields even weaker than internal hyperfine fields can markedly affect spin-selective radical-pair reactions. This weak magnetic field effect has been found to arise from the removal of degeneracies in the zero-field spin Hamiltonian. Here, I investigated the anisotropic effect of a weak magnetic field on a model radical pair with an axially symmetric hyperfine interaction. I found that S-T± and T0-T± interconversions driven by the smaller x and y-components of the hyperfine interaction can be hindered or enhanced by a weak external magnetic field, depending on its direction. Additional isotropically hyperfine-coupled nuclear spins preserve this conclusion, although the S → T± and T0 → T± transitions become asymmetric. These results are supported by simulating reaction yields of a more biologically plausible, flavin-based radical pair.

Magnetic sensitivity of cryptochrome 4 from a migratory songbird.

Night-migratory songbirds are remarkably proficient navigators1. Flying alone and often over great distances, they use various directional cues including, crucially, a light-dependent magnetic compass2,3. The mechanism of this compass has been suggested to rely on the quantum spin dynamics of photoinduced radical pairs in cryptochrome flavoproteins located in the retinas of the birds4-7. Here we show that the photochemistry of cryptochrome 4 (CRY4) from the night-migratory European robin (Erithacus rubecula) is magnetically sensitive in vitro, and more so than CRY4 from two non-migratory bird species, chicken (Gallus gallus) and pigeon (Columba livia). Site-specific mutations of ErCRY4 reveal the roles of four successive flavin-tryptophan radical pairs in generating magnetic field effects and in stabilizing potential signalling states in a way that could enable sensing and signalling functions to be independently optimized in night-migratory birds.