The counterion–retinylidene Schiff base interaction of an invertebrate rhodopsin rearranges upon light activation

• Published in: Communications biology Vol. 2; no. 1; p. 180
• Main Authors: Nagata, Takashi, Koyanagi, Mitsumasa, Tsukamoto, Hisao, Mutt, Eshita, Schertler, Gebhard F. X., Deupi, Xavier, Terakita, Akihisa
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 13.05.2019; Nature Publishing Group
• Subjects: 631/45/612/194; 631/57/2272; 82/80; Amino Acid Substitution; Amino acids; Animals; Arthropod Proteins - chemistry; Arthropod Proteins - genetics; Arthropod Proteins - radiation effects; Biology; Biomedical and Life Sciences; Chromophores; Circadian rhythms; Hydrogen Bonding; Invertebrates; Life Sciences; Light; Models, Molecular; Molecular modelling; Mutagenesis, Site-Directed; Photochemical Processes; Protein Stability; Retina; Rhodopsin; Rhodopsin - chemistry; Rhodopsin - genetics; Rhodopsin - radiation effects; Schiff Bases - chemistry; Schiff Bases - radiation effects; Spiders - chemistry; Spiders - genetics; Ultraviolet radiation; G protein-coupled receptors; Molecular biophysics
• ISSN: 2399-3642; 2399-3642
• DOI: 10.1038/s42003-019-0409-3

Animals sense light using photosensitive proteins—rhodopsins—containing a chromophore—retinal—that intrinsically absorbs in the ultraviolet. Visible light-sensitivity depends primarily on protonation of the retinylidene Schiff base (SB), which requires a negatively-charged amino acid residue—counterion—for stabilization. Little is known about how the most common counterion among varied rhodopsins, Glu181, functions. Here, we demonstrate that in a spider visual rhodopsin, orthologue of mammal melanopsins relevant to circadian rhythms, the Glu181 counterion functions likely by forming a hydrogen-bonding network, where Ser186 is a key mediator of the Glu181–SB interaction. We also suggest that upon light activation, the Glu181–SB interaction rearranges while Ser186 changes its contribution. This is in contrast to how the counterion of vertebrate visual rhodopsins, Glu113, functions, which forms a salt bridge with the SB. Our results shed light on the molecular mechanisms of visible light-sensitivity relevant to invertebrate vision and vertebrate non-visual photoreception. Takashi Nagata et al. use UV-visible spectroscopic analysis to show that Ser186 increases the retinylidene Schiff base (SB) pKa of a spider rhodopsin in the inactive state but not after light activation. The change in contribution of Ser186 to the SB pKa suggests that the counterion (Glu181)–SB interaction rearranges upon light activation.