Photoisomerization in rhodopsins: Shape-changing reactions of retinal at low temperatures

Abstract

Rhodopsins are photoreceptive membrane proteins containing 11-cis (animal rhodopsins) and all-trans (microbial rhodopsins) retinal chromophores. Animal rhodopsins act as G protein–coupled receptors, whereas microbial rhodopsins serve numerous roles and can act as light-driven ion pumps, photosensors, light-gated ion channels, and light-activated enzymes. Microbial rhodopsins play crucial roles in optogenetics. Isomerization is a shape-changing reaction that does not occur at low temperatures. In contrast, primary photo-intermediates are formed in rhodopsins even at 77 K. Therefore, the primary reactions in rhodopsins were debated in the 1970s, although isomerization was initially proposed. The ultrafast spectroscopy analysis of bovine rhodopsin containing an 11-cis-locked retinal chromophore revealed that the primary event in our vision is retinal photoisomerization. Moreover, molecular motions have been directly visualized by time-resolved x-ray crystallography. The unique ability of rhodopsins to undergo isomerization at 77 K was used to determine structural changes by low-temperature Fourier transform infrared spectroscopy, with detailed vibrational analysis providing structural information on animal and microbial rhodopsins, including protein-bound water. In contrast, unusual isomerization pathways (all-trans to 7-cis or 11-cis) and temperature effects (no reactions at <273 or <170 K) have been found for near-infrared light–absorbing microbial rhodopsins.