Coherent vibrational wave packet motion in ErCry4a proteins monitors the redox state of the flavin chromophore
Cryptochromes are blue-light-sensitive flavoproteins that play central roles in biological function. In European robin (Erithacus rubecula) ErCry4a proteins, optical excitation of their flavin chromophore forms a long-lived radical pair through a sequence of electron transfer steps across a tetradic chain of tryptophan residues, making them primary candidates for magnetoreception in night migratory songbirds. Recent quantum chemical calculations indicate that nonadiabatic couplings play a central role in the energy and charge transfer processes initiated by optical excitation. Here, we study these dynamics in ErCry4a using ultrafast transient absorption spectroscopy with 10-fs time resolution in the 450-nm spectral range. We uncover a rapid, sub-50 fs red shift in stimulated emission, quenched within 360 fs by electron transfer from a nearby tryptophan moiety. While high-frequency excited state vibrations are rapidly damped, coherent motion involving several low-frequency vibrations persists during both the initial energy relaxation and the subsequent electron transfer. This is evidenced by probing the coherent vibrational motion of the formed FAD$^{\bullet-}$ radical anion and is independently validated by blocking the electron transfer through site-selective tryptophan mutation. Our results only provide insight into the role of nonadiabatic couplings for the initial steps of cryptochrome photoactivation and suggest a general strategy for redox-state-specific monitoring of charge transfer dynamics by probing coherent vibrational motion.