Coral anthozoan-specific opsins employ a novel chloride counterion for spectral tuning

• DOI: 10.7554/elife.105451
• Publication Date: 2025-03-12T16:25:31Z
• Authors: Yusuke Sakai; Saumik Sen; Tomohiro Sugihara; Yukiya Kakeyama; Makoto Iwasaki; Gebhard FX Schertler; Xavier Deupi; Mitsumasa Koyanagi; Akihisa Terakita

Abstract Animal opsins are G protein coupled receptors that have evolved to sense light by covalently binding a retinal chromophore via a protonated (positively charged) Schiff base. A negatively charged amino acid in the opsin, acting as a counterion, stabilises the proton on the Schiff base, which is essential for sensitivity to visible light. In this study, we investigate the spectroscopic properties of a unique class of opsins from a reef-building coral belonging to the anthozoan-specific opsin II group (ASO-II opsins), which intriguingly lack a counterion residue at any of established sites. Our findings reveal that, unlike other known animal opsins, the protonated state of the Schiff base in visible light-sensitive ASO-II opsins is highly dependent on exogenously supplied chloride ions (Cl−). By using structural modelling and QM/MM calculations to interpret spectroscopy data, we conclude that, in the dark state, ASO-II opsins employ environmental Cl− as their native counterion, while a nearby polar residue, Glu292 in its protonated neutral form, facilitates Cl− binding. In contrast, Glu292 plays a crucial role in maintaining the protonation state of the Schiff base in the light-activated protein, serving as the counterion in the photoproduct. Furthermore, Glu292 is involved in G protein activation of the ASO-II opsin, suggesting that this novel counterion system coordinates multiple functional properties.