Essential elements of radical pair magnetosensitivity inDrosophila

Abstract

SummaryMany animals use the Earth’s magnetic field (geoMF) for navigation1. The favored mechanism for magnetosensitivity involves a blue-light (BL) activated electron transfer reaction between flavin adenine dinucleotide (FAD) and a chain of tryptophan (Trp) residues within the photoreceptor protein, CRYPTOCHROME (CRY). The spin-state of the resultant radical pair (RP) and hence the concentration of CRY in its active state is influenced by the geoMF2. The canonical CRY-centric radical pair mechanism (RPM) does not, however, explain many physiological and behavioural observations2–8. Here, using electrophysiology and behavioural analyses, we assay magnetic field (MF) responses at single neuron and organismal level. We show that the 52 C-terminal (CT) amino acids of CRY, which are missing the FAD binding domain and the Trp chain, are sufficient to facilitate magnetoreception. We also show that increasing intracellular FAD potentiates both BL-induced and MF-dependent effects on the activity mediated by the CT. Additionally, high levels of FAD alone are sufficient to cause BL neuronal sensitivity and, remarkably, potentiation of this response in the co-presence of a MF. These unexpected results reveal the essential components of a primary magnetoreceptor in flies, providing strong evidence that non-canonical (i.e., non-CRY-dependent) RPs can elicit MF responses in cells.

Radical pairs may explain reactive oxygen species-mediated effects of hypomagnetic field on neurogenesis

“…Let us also note that this model could be adapted for other possible radical pairs involving superoxide such as tryptophan–superoxide and tyrosine-superoxide pair [ 14 , 31 , 66 – 70 ]. There is also a possibility that these HMF effects might be due to some non-superoxide radical pair such as tyrosine-tryptophan.…”

Magnetic field effects in biology from the perspective of the radical pair mechanism

“…It has been shown that magnetic fields can modulate the circadian clock [ 115 – 117 ]. Yoshii et al [ 80 ] showed that the effects of static magnetic fields affected the circadian clock of Drosophila and reported that exposure to these fields slowed down the clock rhythms in the presence of blue light, with a maximal change at 300 μT, and reduced effects at both lower and slightly higher field strengths.…”

“…They further reported that an increase in FAD intracellular concentration enhanced neuronal sensitivity to blue light in the presence of a magnetic field. The authors concluded that the magnetosensitivity in cells may be well explained based on non-cryptochrome-dependent radical pair models [ 117 ]. However, the question whether fruit flies use a magnetic compass demands more experimental evidence.…”

Magnetic field effects in biology from the perspective of the radical pair mechanism

“…It has been shown that magnetic fields can modulate the circadian clock [78][79][80] . Yoshii et al 81 showed that the effects of static magnetic fields affected the circadian clock of Drosophila and reported that exposure to these fields slowed down the clock rhythms in the presence of blue light, with a maximal change at 300 µT, and reduced effects at both lower and slightly higher field strengths.…”

“…They further reported that increase in FAD intracellular concentration enhanced neuronal sensitivity to blue light in the presence of a magnetic field. The authors concluded that the magnetosensitivity in cells may be well explained based on non-cryptochrome-dependent radical pair models 80 .…”