Abstract
The mechanism of the magnetic compass sense of migratory songbirds is thought to involve magnetically sensitive chemical reactions of light-induced radical pairs in cryptochrome proteins located in the birds' eyes. However, it is not yet clear whether this mechanism would be sensitive enough to form the basis of a viable compass. In the present work, we report spin dynamics simulations of models of cryptochrome-based radical pairs to assess whether accumulation of nuclear spin polarization in multiple photocycles could lead to significant enhancements in the sensitivity with which the proteins respond to the direction of the geomagnetic field. Although buildup of nuclear polarization appears to offer sensitivity advantages in the more idealized model systems studied, we find that these enhancements do not carry over to conditions that more closely resemble the situation thought to exist in vivo. On the basis of these simulations, we conclude that buildup of nuclear polarization seems unlikely to be a source of significant improvements in the performance of cryptochrome-based radical pair magnetoreceptors.
Highlights
To model the configuration of FAD⋅− and TrpCH⋅+ in avian cryptochrome, we considered the x-ray crystal structure of pigeon cryptochrome 4 (ClCry4)
We performed the same calculation on the averaged radical positions obtained from a molecular dynamics (MD) trajectory of a homology model of robin cryptochrome 4a (ErCry4a) modeled from the ClCry4 crystal structure
Given that both the differential decay (DD) and differential relaxation (DR) nuclear polarization mechanisms depend on the degree of asymmetry in the decay rates of the singlet and triplet radical pairs, we considered additional values of the rate between constants 0.1 and 5
Summary
Night-migratory songbirds can sense the direction of the Earth’s magnetic field as an aid to navigation. The primary sensors, located in the eyes, pass information to a specific part of the bird’s visual system in the brain for processing and integration with other orientation cues. The leading hypothesis for the mechanism of this remarkable ability is the radical pair mechanism (RPM) involving photochemical reactions of proteins known as cryptochromes, which have been found in various cell types in the birds’ retinas. Spin-selectivity in the decay pathways of light-induced radical pairs in these proteins is thought to allow the direction of the geomagnetic field to influence the yield of a signaling state, providing the basis for a chemical inclination compass. Studies of the purified proteins indicate that cryptochromes may be fit for purpose as magnetic compass sensors.. RP1, which comprises FAD⋅− and TrpH⋅+ radicals, can either revert to the ground state by back electron transfer (rate constant, kS) or form a stabilized radical pair, RP2, in which the tryptophan radical (Trp⋅) has been deprotonated (rate constant, kF). Arising in the reactions of organic radicals, is an attractive hypothesis for avian magnetoreception It rationalizes the light-dependence of the magnetic compass sense, is consistent with the observation that the compass is axial rather than polar, and, at least qualitatively, can account for the effects of radiofrequency magnetic fields on the ability of caged songbirds to orient using the geomagnetic field.. Nuclear polarization generated by intra-protein radical pairs has been observed by solid-state NMR (nuclear magnetic resonance) in mutant forms of the LOV (light-oxygen-voltage) domains of the flavoprotein phototropin, but not, so far, in any cryptochrome
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