The animal-like cryptochrome of Chlamydomonas rein-hardtii (CraCRY) is a recently discovered photoreceptor that controls the transcriptional profile and sexual life cycle of this alga by both blue and red light. CraCRY has the uncommon feature of efficient formation and longevity of the semireduced neutral form of its FAD cofactor upon blue light illumination. Tyrosine Y-373 plays a crucial role by elongating , as fourth member, the electron transfer (ET) chain found in most other cryptochromes and DNA photolyases, which comprises a conserved tryptophan triad. Here, we report the full mechanism of light-induced FADH(center dot) formation in CraCRY using transient absorption spectroscopy from hundreds of femtoseconds to seconds. Electron transfer starts from ultrafast reduction of excited FAD to FAD(center dot-) by the proximal tryptophan (0.4 ps) and is followed by delocalized migration of the produced WH center dot+ radical along the tryptophan triad (similar to 4 and similar to 50 ps). Oxidation of Y-373 by coupled ET to WH center dot+ and deprotonation then proceeds in similar to 800 ps, without any significant kinetic isotope effect, nor a pH effect between pH 6.5 and 9.0. The FAD(center dot-)/Y-373(center dot) pair is formed with high quantum yield (similar to 60%); its intrinsic decay by recombination is slow (similar to 50 ms), favoring reduction of Y-37(3)center dot by extrinsic agents and protonation of FAD(center dot-) to form the long-lived, red-light absorbing FADH(center dot) species. Possible mechanisms of tyrosine oxidation by ultrafast proton-coupled ET in CraCRY, a process about 40 times faster than the archetypal tyrosine-Z oxidation in photosystem II, are discussed in detail.