Mechanism of coral light-sensing proteins elucidated by Osaka Metropolitan University

A joint research group consisting of Dr. Yusuke Sakai (doctoral researcher at the time of the study), Professor Akihisa Terakita, and Professor Mitsumasa Koyanagi from the Graduate School of Science at Osaka Metropolitan University, Dr. Xavier Deupi from the PSI Center for Life Sciences in Switzerland, and their colleagues discovered that opsins, which are light-sensitive proteins in reef-building corals, have a different mechanism from known animal opsins, with positively charged Schiff bases being stabilized by chloride ions. Their research was published online in eLife.

Opsins, proteins that sense light, detect light by binding with retinal, a small molecule. Normally, when retinal binds through a Schiff base, it responds strongly to UV but shows little response to the visible light that humans can see. Previous research has shown that for opsins to respond sensitively to visible light, hydrogen ions (protons) need to be added to the Schiff base. For the protonated Schiff base to be stable, amino acids with counterions (negative charge) must be present in the surrounding area. Past studies have shown that amino acids functioning as counterions exist in any of three different locations within the protein. This is considered to play important roles and have effects on opsin function and evolution.

In recent years, a different type of opsin from those previously known was discovered in animals belonging to the anthozoan class, such as corals and sea anemones, and was classified into a new opsin group called ASO-II. It was found that ASO-II group opsins lack negatively charged amino acid residues at any of the three amino acid positions previously confirmed to function as counterions.

The research group used ASO-II group opsins contained in "Acropora tenuis," a species of reef-building coral, to investigate in detail which amino acids serve as counterions for receiving visible light. They conducted experiments replacing amino acids and further analysis by simulating molecular structure and movements.

As a result, they found that these coral-derived ASO-II group opsins use chloride ions rather than amino acids as counterions. This is the first confirmed case of inorganic ions functioning as counterions in opsins, representing a breakthrough that brings new perspectives to understanding opsin evolution and diversification.

Furthermore, they revealed that the stabilization of the protonated Schiff base by chloride ions is weaker than stabilization by amino acid residues. Therefore, they found that opsins have the property of reversibly switching between states sensitive to visible light (protonated form) and states sensitive to UV (deprotonated form) in response to changes in hydrogen ion concentration (pH).

This pH dependence may have important implications for actual coral ecology. Corals that form coral reefs maintain a symbiotic relationship with algae called zooxanthellae within their cells, utilizing glucose and other nutrients produced by the photosynthesis of the zooxanthellae as nutritional sources. During this photosynthetic process, the pH inside and outside coral cells often shifts toward alkalinity, and these pH fluctuations are thought to directly affect the function of these opsins. It was suggested that when the pH increases, the proportion of protonated Schiff bases decreases, leading to the reduced sensitivity of opsins to visible light while relatively increasing sensitivity to UV.

Sakai commented: "The characteristics of opsins possessed by corals, which are famous for forming beautiful coral reefs, were extremely unique. I am very pleased that this research has expanded the diversity (possibilities) of opsins. The world of coral opsins and the coral photophysiology and ecology revealed through them surely holds many more possibilities."

Journal Information
Publication: eLife
Title: Coral anthozoan-specific opsins employ a novel chloride counterion for spectral tuning
DOI: 10.7554/eLife.105451.3