Essential elements of radical pair magnetosensitivity in Drosophila

Adam A. Bradlaugh, Giorgio Fedele, Anna L. Munro, Celia Napier Hansen, John M. Hares, Sanjai Patel, Charalambos P. Kyriacou, Alex R. Jones, Ezio Rosato () and Richard A. Baines ()
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Adam A. Bradlaugh: University of Manchester, Manchester Academic Health Science Centre
Giorgio Fedele: University of Leicester
Anna L. Munro: University of Manchester, Manchester Academic Health Science Centre
Celia Napier Hansen: University of Leicester
John M. Hares: University of Leicester
Sanjai Patel: University of Manchester
Charalambos P. Kyriacou: University of Leicester
Alex R. Jones: National Physical Laboratory
Ezio Rosato: University of Leicester
Richard A. Baines: University of Manchester, Manchester Academic Health Science Centre

Nature, 2023, vol. 615, issue 7950, 111-116

Abstract: Abstract Many animals use Earth’s magnetic field (also known as the geomagnetic field) for navigation1. The favoured mechanism for magnetosensitivity involves a blue-light-activated electron-transfer reaction between flavin adenine dinucleotide (FAD) and a chain of tryptophan residues within the photoreceptor protein CRYPTOCHROME (CRY). The spin-state of the resultant radical pair, and therefore the concentration of CRY in its active state, is influenced by the geomagnetic field2. However, the canonical CRY-centric radical-pair mechanism does not explain many physiological and behavioural observations2–8. Here, using electrophysiology and behavioural analyses, we assay magnetic-field responses at the single-neuron and organismal levels. We show that the 52 C-terminal amino acid residues of Drosophila melanogaster CRY, lacking the canonical FAD-binding domain and tryptophan chain, are sufficient to facilitate magnetoreception. We also show that increasing intracellular FAD potentiates both blue-light-induced and magnetic-field-dependent effects on the activity mediated by the C terminus. High levels of FAD alone are sufficient to cause blue-light neuronal sensitivity and, notably, the potentiation of this response in the co-presence of a magnetic field. These results reveal the essential components of a primary magnetoreceptor in flies, providing strong evidence that non-canonical (that is, non-CRY-dependent) radical pairs can elicit magnetic-field responses in cells.

Date: 2023
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DOI: 10.1038/s41586-023-05735-z

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