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Radical pair-based magnetic sensing in migratory birds

Periodic Reporting for period 2 - QuantumBirds (Radical pair-based magnetic sensing in migratory birds)

Reporting period: 2020-10-01 to 2022-03-31

The navigational abilities of night-migratory songbirds, travelling alone over thousands of kilometres, are absolutely staggering. The successful completion of these magnificent voyages depends crucially on the birds’ ability to sense the Earth’s magnetic field. Exactly how this magnetic sense works is one of the most significant open questions in biology and biophysics. The experimental evidence suggests something extraordinary. The birds’ magnetic compass sensor seems to rely on coherent quantum phenomena that indirectly allow astonishingly weak magnetic interactions to be detected in biological tissue. QuantumBirds brings together quantum physics, spin chemistry, behavioural biology, biochemistry, and molecular biology in an ambitious, imaginative and synergetic research programme that will prove whether the primary magnetic detection event occurring in the birds’ retinas involves the quantum spin dynamics of photochemically formed radical pairs in cryptochrome proteins.

We are addressing three specific questions:

1. Are avian cryptochromes capable of functioning as magnetic compass receptors?

2. Do retinal neurons encode light-dependent, cryptochrome-derived magnetic information?

3. Are cryptochromes the primary magnetoreceptor molecules for magnetic compass orientation?
Results from the first 24 months of the project have been published in 18 articles in the scientific literature. The main findings can be summarised as follows.

1. The crystal structure of pigeon Cry4 has been determined.

2. We have shown that the photochemistry of cryptochrome 4 (Cry4) from the night-migratory European robin (Erithacus rubecula) is magnetically sensitive in vitro, and more so than that of 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.

3. Behavioural experiments suggest that the spin coherence lifetime of the magnetically sensitive radical pair in Eurasian blackcaps is in the range 2-10 microseconds.

4. Spin dynamics simulations have shown that the operation of a radical pair magnetoreceptor cannot be satisfactorily be described without an exact quantum mechanical treatment and it therefore deserves a place in the field of “Quantum Biology”.

5. Six proteins have been identified as having interactions with robin Cry4 that could play a role in the magnetic signal transduction pathway.

6. Spin dynamics simulations have identified the highly restrictive conditions under which a flavin-superoxide radical pair could form the basis of a geomagnetic compass sensor.

7. A novel isoform of robin Cry4 has been identified; its circadian expression patterns suggest that it has a different function to the previously described form of robin Cry4.

8. Recruitment data from seabird colonies in the UK correlate with the natural drift in the geomagnetic field and thus indicate that these birds use a magnetic map.

9. Using serial sectioning, multibeam scanning electron microscopy, we investigated the detailed double-cone anatomy and connectivity of the neurons in a bird retina with unprecedented precision. Our data indicate a much more complex connectivity network in the avian retina than originally expected, and the Cry4-containing double cones in particular show an extremely rich connectivity.

10. The distribution of Cry1a in the retina of several bird species at night and during the day show that antibodies cannot be used to detect any light-activated form of Cry1a. Light-dependent differences in antibody-stainings had formerly been claimed to be a major indication that Cry1a should be the magnetoreceptor in night-migratory songbirds. This does not hold.

11. We were involved in a major bird genome project, which sequenced and made 363 genomes from 92.4% of bird families, including 267 newly sequenced bird genomes, available to the scientific community.
1. An Information Theory approach has been developed to assess the performance of Cry-based radical pairs under the low light levels experienced by nocturnal migrants.

2. Confocal fluorescence microscopy techniques have been developed for the investigation of magnetic field effects on radical pair reactions in cryptochromes.

3. An unprecedentedly magnetically quiet calcium imaging setup has been built and can be used to record retinal responses.

4. New evidence more clearly demonstrating that at least some bird species ranging from songbirds to seabirds have a magnetic map and that they use it both to return to a breeding location and to correct for directional mistakes during migration.

We are on track to answer the three questions mentioned above.
Migratory songbirds seem to have a chemical magnetic compass in their eyes