Viability of superoxide-containing radical pairs as magnetoreceptors

The ability of night-migratory songbirds to sense the direction of the Earth's magnetic field is increasingly attributed to a photochemical mechanism in which the magnetic field acts on transient radical pairs in cryptochrome flavoproteins located in the birds' eyes. The magnetically sensitive species is commonly assumed to be [FAD^•- TrpH^•+], formed by sequential light-induced intraprotein electron transfers from a chain of tryptophan residues to the flavin adenine dinucleotide chromophore. However, some evidence points to superoxide, O₂ ^•-, as an alternative partner for the flavin radical. The absence of hyperfine interactions in O₂ ^•- could lead to a more sensitive magnetic compass, but only if the electron spin relaxation of the O₂ ^•- radical is much slower than normally expected for a small mobile radical with an orbitally degenerate electronic ground state. In this study we use spin dynamics simulations to model the sensitivity of a flavin-superoxide radical pair to the direction of a 50 μT magnetic field. By varying parameters that characterize the local environment and molecular dynamics of the radicals, we identify the highly restrictive conditions under which a O₂ ^•--containing radical pair could form the basis of a geomagnetic compass sensor. We conclude that the involvement of superoxide in compass magnetoreception must remain highly speculative until further experimental evidence is forthcoming.