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Chemical and structural analysis of a photoactive vertebrate cryptochrome from pigeon

B. Zoltowski,Y. Chelliah,A. Wickramaratne,Lauren E. Jarocha,Nischal Karki,Wei Xu,H. Mouritsen,P. Hore,R. Hibbs,C. Green,J. Takahashi

Published 2019 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance Seasonal migration is dependent on an organism being able to sense and reorient to the Earth’s magnetic field. Cryptochromes (CRYs) have been implicated as light-driven sensors of the Earth’s magnetic field; however, contradictions between in vitro photochemistry and in vivo behavioral studies limit validation of CRYs as magnetosensors. To reconcile these discrepancies, we conducted detailed photochemical and structural studies of a CRY from Columbia livia (pigeon). We present the structure of a photoactive vertebrate CRY that reveals a pathway conserved in migratory organisms that facilitates its function as a magnetosensor. Computational and biochemical studies implicate the blue-light sensor cryptochrome (CRY) as an endogenous light-dependent magnetosensor enabling migratory birds to navigate using the Earth’s magnetic field. Validation of such a mechanism has been hampered by the absence of structures of vertebrate CRYs that have functional photochemistry. Here we present crystal structures of Columba livia (pigeon) CRY4 that reveal evolutionarily conserved modifications to a sequence of Trp residues (Trp-triad) required for CRY photoreduction. In ClCRY4, the Trp-triad chain is extended to include a fourth Trp (W369) and a Tyr (Y319) residue at the protein surface that imparts an unusually high quantum yield of photoreduction. These results are consistent with observations of night migratory behavior in animals at low light levels and could have implications for photochemical pathways allowing magnetosensing.

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