Rhodopsins are light-sensitive proteins that use light energy to perform various biological functions in bacterial and animal cells. The chromophore of Rhodopsins is the protonated Schiff base retinal (PSBR), which undergoes a primary photochemical isomerization reaction upon absorption of a photon. PSBR is in all-trans configuration in bacterial cells and isomerizes to the 13-cis form, while in animal cells it isomerizes from 11-cis to all-trans. The photoisomerization reaction of PSBR proceeds at a high rate within hundreds of femtoseconds, and such a high rate is provided in different ways in various Rhodopsins. Recently, we have shown that animal Rhodopsins use the intrinsic photophysical properties of their 11-cis chromophore, while bacterial Rhodopsins change both the speed and specificity of photoisomerization of their all-trans chromophore. Here, we study the role of the protein environment in the early-time excited-state dynamics of PSBR in microbial and animal Rhodopsins and provide a link to the specific photoisomerization mechanism. By using high-level extended multi-configuration quasi-degenerate perturbation theory (XMCQDPT2) combined with the effective fragment potential (EFP) method, we calculate the photoabsorption spectra of PSBR inside the active centers of bovine visual Rhodopsin and microbial Rhodopsin KR2 and compare them with those calculated in the gas phase. The analysis of the vibronic band shapes allows us to explore the early-time excited-state dynamics of PSBR in different environments and shows that the protein environment alters vibrational modes that are excited upon the S0-S1 transition, facilitating the specific photoisomerization. By performing molecular dynamics sampling, we also reveal structural heterogeneity of the retinal-binding pocket of microbial Rhodopsin KR2 and conclude that formation of a strong hydrogen bond between the retinal Schiff base and its counterion is essential for the ultrafast reaction dynamics. The pre-twisting of PSBR enhances the activity of both the localized stretching and hydrogen-out-of-plane (HOOP) modes upon photoexcitation. At the same time, other conformations of PSBR may give rise to long picosecond time components in the decay of the excited state in KR2. Our findings provide a direct link between the structure of the retinal-binding pocket and the reaction dynamics of PSBR inside the proteins.

Role of the protein environment in the early-time excited-state dynamics of protonated Schiff-base retinal in microbial and animal rhodopsins

ACS Spring Meeting 2021

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