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Magnetic sensing by molecules, birds, and devices

Final Report Summary - CHEMNAV (Magnetic sensing by molecules, birds, and devices)

In 2007 a female bar-tailed godwit – a medium sized wading bird – was tracked by satellite flying non-stop from Alaska to New Zealand, an eight-day trip of more than 11,000 km across the Pacific Ocean. Countless godwits cover similar routes in both directions every year. Annually, billions of small migratory songbirds fly thousands of kilometres between wintering and breeding grounds over distances only slightly less awesome. One of the many questions raised by these spectacular migrations is how birds navigate over such large distances. Amongst a number of directional cues – the sun, stars, odours, landmarks – it is clear that birds can orient themselves in the Earth’s magnetic field. The aim of the ChemNav project was to elucidate the biophysical mechanism of avian magnetoreception, to understand the practical requirements for efficient chemical sensing of magnetic fields, and to explore the potential for bio-inspired magnetic sensing devices.
(1) The fundamental hypothesis on which ChemNav is based is that the magnetic compass relies on the photochemical formation of short-lived, magnetically sensitive radical pair states of photoreceptor proteins called cryptochromes located in the birds' retinas. Using specifically developed forms of spectroscopy we have established that cryptochromes possess the properties required to act as versatile magnetic sensors and that there is ample scope for evolution to have optimised one of the four known avian cryptochromes as a compass magnetoreceptor. Sensitive responses to weak magnetic fields have been shown to arise from the formation of long-lived flavin-tryptophan radical pairs by sequential photo-induced electron transfers along a chain of three or four tryptophan amino acid residues. An unexpected chemical amplification mechanism has been discovered with the potential to boost the magnitude of the primary directional information delivered by a cryptochrome sensor.
(2) A variety of aspects of radical pair magnetoreception have been explored using non-natural proteins known as maquettes. Inspired by cryptochromes, but with no sequence similarity to the natural proteins, these new model systems have the structural, kinetic and magnetic flexibility to allow the practical requirements for efficient chemical magnetic sensing to be tested, compared and optimised. Magnetic field effects on flavin-tryptophan radical pairs in maquettes, remarkably similar to those found for cryptochromes, have been characterized and studied as a function of the distance between the radicals.
(3) Efficient computational methods have been devised and used to guide experiments, interpret experimental data, and explore aspects of the magnetoreception mechanism that are currently beyond the scope of experiment. Important insights have included: potential mechanisms for amplifying weak magnetic field effects; how a light-dependent magnetic compass could be insensitive to the intensity and polarization of the incident light; cryptochrome properties that could result in a much more precise compass bearing than previously thought possible; and calculations of radiofrequency magnetic field effects to guide behavioural tests on migratory birds.
(4) Close parallels exist between radical pairs formed in cryptochromes and polaron pairs in organic semiconductors that have potential applications as magnetic sensors. Using methods devised for cryptochrome-based radical pairs, we have obtained a new relationship between experimentally measured magnetoelectroluminescence and magnetoconductance and the calculated yields of a polaron pair recombination reaction. Good agreement between theory and experimental data has been obtained for both normal and deuterated forms of an organic polymer.
In summary, we now have a detailed understanding of the spin dynamics of radical pairs in cryptochromes and strengthened evidence that cryptochromes are indeed the primary magnetic compass sensors in migratory birds.