Structural Basis for Near Infrared Absorption and Noncanonical Photoisomerization in Neorhodopsin

In retinal proteins, light absorption leads to a double bond isomerization of the chromophore, followed by conformational relaxations that drive functional protein rearrangements. The balance between photoisomerization and radiative or non-radiative decays of the excited state is adjusted to the demands of the respective photoreceptor function. The molecular determinants controlling the excited state processes remain poorly understood and are the focus of this combined crystallographic, spectroscopic, and theoretical work on the recently discovered neorhodopsin (NeoR). NeoR exhibits a highly red-shifted and fluorescent dark state and selectively photoisomerizes from all-trans to 7-cis. We show that the local electrostatic environment reduces the negative charge density near the Schiff base and suppresses torsional motion around the canonical C13=C14 isomerization site of microbial rhodopsins. Instead, the chromophore-binding pocket permits only low-efficiency C7=C8 isomerization, accompanied by polyene inversion, {beta}-ionone ring displacement, and Schiff base deprotonation. Consequently, unlike other retinal photoreceptors, NeoR undergoes structural changes localized near the {beta}-ionone ring.