Computational and Spectroscopic Characterization of the Photocycle of an Artificial Rhodopsin

• Published in: The journal of physical chemistry letters 2020-06, Vol.11 (11), p.4245-4252
• Main Authors: Manathunga, Madushanka, Jenkins, Adam J, Orozco-Gonzalez, Yoelvis, Ghanbarpour, Alireza, Borhan, Babak, Geiger, James H, Larsen, Delmar S, Olivucci, Massimo
• Format: Article
• Language: English
• Subjects: Isomerism; Light; Quantum Theory; Receptors, Retinoic Acid; Rhodopsin - chemistry; Rhodopsin - radiation effects; Schiff Bases - chemistry; Spectrum Analysis - methods
• ISSN: 1948-7185; 1948-7185
• DOI: 10.1021/acs.jpclett.0c00751

The photocycle of a reversible photoisomerizing rhodopsin mimic (M2) is investigated. This system, based on the cellular retinoic acid binding protein, is structurally different from natural rhodopsin systems, but exhibits a similar isomerization upon light irradiation. More specifically, M2 displays a 15- to - conversion of retinal protonated Schiff base (rPSB) and - to 15- isomerization of unprotonated Schiff base (rUSB). Here we use hybrid quantum mechanics/molecular mechanics (QM/MM) tools coupled with transient absorption and cryokinetic UV-vis spectroscopies to investigate these isomerization processes. The results suggest that primary rPSB photoisomerization of M2 occurs around the C13═C14 double bond within 2 ps following an aborted-bicycle pedal (ABP) isomerization mechanism similar to natural microbial rhodopsins. The rUSB isomerization is much slower and occurs within 48 ps around the C15═N double bond. Our findings reveal the possibility to engineer naturally occurring mechanistic features into artificial rhodopsins and also constitute a step toward understanding the photoisomerization of UV pigments. We conclude by reinforcing the idea that the presence of the retinal chromophore inside a tight protein cavity is not mandatory to exhibit ABP mechanism.