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Radical pair-based magnetic sensing in migratory birds

Periodic Reporting for period 3 - QuantumBirds (Radical pair-based magnetic sensing in migratory birds)

Período documentado: 2022-04-01 hasta 2023-09-30

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?
The findings generated by QuantumBirds also address crucial broader scientific and societal questions such as: What are the fundamental principles required for quantum sensing at room temperature? How can we successfully protect and translocate endangered animals to preserve biodiversity? How can man-made devices navigate reliably without GPS support? Our research in QuantumBirds helps bridge the gaps in fundamental research knowledge needed for practical applications and provides new concepts for the future that will greatly improve the ability of society to answer and act on these questions.
Results from the first 48 months of the project have been published in 36 articles in the scientific literature with 2 more in press. Our most significant findings can be summarised as follows.
• The first crystal structure of an avian cryptochrome (pigeon Cry4a) has been determined.
• Spectroscopic studies of Cry4 from the night-migratory European robin show that it has many of the properties required of a magnetic compass sensor.
• Spin dynamics simulations have shown that the operation of a radical pair magnetoreceptor cannot satisfactorily be described without an exact quantum mechanical treatment. Avian magnetoreception may therefore be a genuine example of “quantum biology”.
• Six proteins have been found to interact with robin Cry4. Binding to the alpha-subunit of the cone-specific G protein might constitute the first biochemical signalling step in radical-pair-based magnetoreception.
• 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.
• Recruitment data from seabird colonies and ring recoveries of night-migratory songbirds correlate with the natural drift in the geomagnetic field and indicate that migratory birds use magnetic inclination as a stop sign when returning in spring.
• The detailed double-cone anatomy and connectivity of the neurons in a bird retina has been investigated with unprecedented precision. Our data indicate a much more complex connectivity network than originally expected. The Cry4-containing double cones in particular show an extremely rich connectivity.
• The distribution of Cry1a in the retinas of several bird species show that antibodies cannot, as previously claimed, be used to detect light-activated forms of Cry1a in night-migratory songbirds.
• 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.
• Computer simulations indicate that chiral-induced spin selectivity (CISS) might boost the sensitivity and/or precision of magnetic compass sensing in birds.
• A new information theory approach shows how the accuracy of a radical pair compass is related to the orientation of cryptochromes within photoreceptor cells, the distribution of cells in the retina, and the fundamental magnetic sensitivity of the proteins.
• Simulations have established a reliable baseline value of the “half-field” parameter which can be used to understand the impact of spin relaxation on the performance of Cry4 as a magnetic compass sensor.
• Spin dynamics simulations predict that radiofrequency fields with frequencies below 116 MHz should prevent birds using their magnetic compass while those with frequencies above 116 MHz should not. Meticulous testing of Eurasian blackcaps has confirmed this forecast.
• We have identified the 2H/13C/15N riboflavin isotopologues that have the greatest differences in magnetic sensitivity compared to the naturally occurring forms containing 1H/12C/14N.
• Double cones in the avian retina form an oriented mosaic which might facilitate magnetoreception and/or polarized light sensing.
• Newly developed viral-delivered calcium dyes are being tested and appear promising for the calcium imaging project as the ERG signals are now excellent and blinking cells are regularly seen.
• With a sample size of over 100,000 individuals, we could find no sign of magnetic sensory behaviour in Drosophila, which can therefore not replace songbirds as the key study species in magnetoreception research.
We have made progress that goes far beyond the state of the art at the beginning of the Quantum Birds project. Here are a few selected examples of what we hope to achieve in the next two years.
• New avian Cry4a mutants show extremely high sensitivity to applied magnetic fields (> 40%) which means that we should be able to measure, for the first time in any cryptochrome, effects of the Earth’s magnetic field, even in vitro for the isolated molecules.
• Isotopically substituted Cry4a molecules will enable us to study the effects of additional hyperfine interactions in vitro and probably in vivo. Here we will rely on studies of the disorienting effects of radiofrequency electromagnetic fields on night-migratory songbirds combined with detailed quantum mechanical simulations. Through such studies, Quantum Birds has provided the most compelling evidence to date that the magnetic compass of migratory birds operates by a mechanism involving flavin-containing radical pairs.
• An unprecedentedly magnetically quiet calcium imaging setup has been built and is being used to record magnetic modulation of retinal responses.
Migratory songbirds seem to have a chemical magnetic compass in their eyes