Magnetically Sensitive Radical Photochemistry of Non-natural Flavoproteins

Abstract

It is a remarkable fact that ∼50 μT magnetic fields can alter the rates and yields of certain free-radical reactions and that such effects might be the basis of the light-dependent ability of migratory birds to sense the direction of the Earth's magnetic field. The most likely sensory molecule at the heart of this chemical compass is cryptochrome, a flavin-containing protein that undergoes intramolecular, blue-light-induced electron transfer to produce magnetically sensitive radical pairs. To learn more about the factors that control the magnetic sensitivity of cryptochromes, we have used a set of de novo designed protein maquettes that self-assemble as four-α-helical proteins incorporating a single tryptophan residue as an electron donor placed approximately 0.6, 1.1, or 1.7 nm away from a covalently attached riboflavin as chromophore and electron acceptor. Using a specifically developed form of cavity ring-down spectroscopy, we have characterized the photochemistry of these designed flavoprotein maquettes to determine the identities and kinetics of the transient radicals responsible for the magnetic field effects. Given the gross structural and dynamic differences from the natural proteins, it is remarkable that the maquettes show magnetic field effects that are so similar to those observed for cryptochromes.

Magnetically modulated photochemical reaction pathways in anthraquinone molecules and aggregates

“…It is noted that the decay of AQH, radical becomes slower when magnetic field is applied. The decay profile of AQH, radicals (Figure 2C) can be fitted by a sum of two first-order decays (Zollitsch et al, 2018) (See Table S1 in supplemental information), in which the fast (solid line) and slow (dashed line) components are corresponding to AQH, radicals in the spin parallel and anti-parallel RPs, respectively. The weight ratio of fast/slow components is thus regarded as the ratio between singlet/triplet RPs (S/T ratio) in photochemical process.…”

On the optimal relative orientation of radicals in the cryptochrome magnetic compass

“…In fact, Cry has previously been used as an optogenetic tool [60] and can render the activity of a system that do not naturally contain Cry magnetically-sensitive [61]. Additionally this research could guide endeavors to experimentally observe anisotropic MFEs in cryptochromes in vitro or in chemically engineered model compounds such as that reported in [62,63]. Finally, our study will provide indirect insight into the current debate surrounding the identity of the crucial radical pair, by providing a more complete picture of the magnetosensitivity of [F…”

Deazaflavin reductive photocatalysis involves excited semiquinone radicals

“…Fl cofactors in their fully reduced form participate in photo-induced electron transfer (PET) reactions in DNA photolyases repairing pyrimidine dimers formed upon exposure to ultraviolet (UV) light 23,24 . Fls in their oxidised form are responsible for bacterial bioluminescence 25 or perform various functions in photoreceptors 7,[26][27][28] . dFl dF 0 in its oxidised form serves as a light-harvesting antenna in photolyases 29 .…”