Decrypting the Nonadiabatic Photoinduced Electron Transfer Mechanism in Light-Sensing Cryptochrome

Area of Science:

• Biochemistry
• Photobiology
• Structural Biology

Background:

• Cryptochromes are blue light photoreceptors vital for circadian rhythms, phototropism, and magnetoreception in diverse organisms.
• Light-induced signaling involves photoexcitation of the flavin adenine dinucleotide (FAD) cofactor and subsequent electron transfer (ET) through a tryptophan chain.

Purpose of the Study:

• To elucidate the unclear initial photoinduced electron transfer from tryptophan to FAD in cryptochromes.
• To investigate the roles of nonadiabatic pathways and the protein environment on ET kinetics and quantum efficiency.

Main Methods:

• Extensive nonadiabatic and adiabatic dynamics simulations were performed.
• On-the-fly multireference ab initio electronic structure calculations were utilized for *Arabidopsis thaliana* cryptochrome 1 (*At*CRY1).

Main Results:

• A novel mechanism involving rapid nonradiative decay from higher-lying singlet states leading to charge separation was identified.
• A slower adiabatic ET on the S₁ state, hindered by a newly found low-energy S₁ local excitation minimum, was observed.
• The protein environment was found to stabilize tryptophan orientations, facilitating subsequent ET steps.

Conclusions:

• The study reveals a dual mechanism for photoinduced electron transfer in cryptochromes, involving both rapid nonradiative decay and slower adiabatic ET.
• Protein environment plays a crucial role in modulating ET efficiency and cryptochrome function.
• These findings advance the understanding of structure-function relationships in photoreceptors.