Highly sensitive light-driven proton pump in Prometheoarchaea discovered by research group from University of Tokyo, Nagoya Institute of Technology

A research group led by Associate Professor Keiichi Inoue and Project Researcher Masae Konno from the Institute for Solid State Physics, the University of Tokyo, Professor Osamu Nureki, Assistant Professor Wataru Shihoya (at the time of the research, currently Associate Professor at Keio University), Project Assistant Professor Tatsuki Tanaka, and Graduate Students Yuma Matsuzaki and Shunya Murakoshi from the Graduate School of Science, the University of Tokyo, and Distinguished Professor Hideki Kandori, Associate Professor Kota Katayama, Researcher Rei Yoshizumi, Graduate Student (at the time of the research) Shota Itakura, and Graduate Student Yosuke Mizuno from Nagoya Institute of Technology revealed that Heimdallarchaeota (one of the Prometheoarchaea), one of the extant species closest to the common ancestor of eukaryotes, possess a protein called Heimdallrhodopsin. This protein captures solar energy with high efficiency using carotenoid pigments, use it to transport protons (hydrogen ions), and convert the energy into chemical energy.

Through spectroscopic measurements using advanced laser technology, the group revealed for the first time in the world that the carotenoid pigments in Heimdallrhodopsin capture light as light antennas and use that energy for proton transport. They also succeeded in capturing its unique structure, suitable for binding various carotenoid pigments, through X-ray crystallographic analysis. The fact that Heimdallarchaeota captures light with high efficiency and use it for their own growth was completely unknown until now, revealing an unprecedented new aspect. Furthermore, since Heimdallrhodopsin uses carotenoids such as lutein that also exist in the human body, this protein is expected to be useful as a new biomolecular tool for developing highly sensitive vision regeneration and light-based treatment technologies for neurological diseases. The group's research was published in Nature Microbiology.

Microbial rhodopsins are proteins that capture sunlight using retinal, an analog of vitamin A, and use that energy to transport protons from inside the cell to outside. This creates a proton concentration gradient between the inside and outside of the cell, which drives processes such as the synthesis of adenosine triphosphate (ATP), the cell's energy currency. It is already known that microbial rhodopsins are possessed by bacteria and archaea that inhabit diverse environments such as oceans, rivers, lakes, lagoons, and soil. Recent research has revealed that especially in the ocean, enormous amounts of solar energy comparable to photosynthesis by algae are being used for microbial survival through microbial rhodopsins.

Meanwhile, among archaea, Heimdallarchaeota is considered to be the extant species most closely related to the ancient archaea that became the common ancestor of eukaryotes, including humans, and is one of the Prometheoarchaea that has attracted attention as an extremely important species for understanding the evolution of life. However, due to difficulties in isolating cells, most of the ecology of Heimdallarchaeota remains unknown, which poses a major problem in understanding the process leading to eukaryotes.

The research group discovered that some Heimdallarchaeota, which were previously thought to inhabit mud at the bottom of oceans and lakes, actually live floating in seawater in ocean regions around the world where sunlight is abundantly available, and furthermore possess a previously unknown type of microbial rhodopsin (Heimdallrhodopsin).

Therefore, they artificially produced large amounts of the protein using E. coli and examined the properties of Heimdallrhodopsin. They revealed that it binds carotenoid pigments such as lutein, which is abundant in the eyes and skin of animals (including humans), and fucoxanthin, which algae including kelp and wakame use as light antennas to efficiently collect light in photosynthesis.

Furthermore, they found that when the bound carotenoid pigments absorb blue light with short wavelengths and high energy, they immediately transfer that energy to the nearby retinal pigment, driving the proton transport reaction as if the retinal pigment itself had absorbed light. From this, it is thought that Heimdallarchaeota evolved to utilize sunlight more skillfully than other Prometheoarchaea by evolving Heimdallrhodopsin, which uniquely uses various carotenoid pigments as light antennas. Additionally, spectroscopic measurements using lasers and infrared light revealed that when carotenoid pigments are bound, the structure of Heimdallrhodopsin changes, making it easier to transport protons—an unprecedented form of transport efficiency improvement.

Through X-ray crystallographic analysis, the group successfully revealed the three-dimensional structure of Heimdallrhodopsin at the atomic level. As a result, it became clear that Heimdallrhodopsin has a unique surface topography suitable for binding various carotenoid pigments. Computer simulations revealed how various carotenoid pigments bind to Heimdallrhodopsin. From the structure obtained, the group elucidated the mechanism by which energy is transferred through direct contact between the retinal pigment and carotenoids.

Journal Information
Publication: Nature Microbiology
Title: Structural insights into light harvesting by antenna-containing rhodopsins in marine Asgard archaea
DOI: 10.1038/s41564-025-02016-5