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Structural insights into light harvesting by antenna-containing rhodopsins in marine Asgard archaea

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Tzlil, Gali, Marín, María del Carmen, Matsuzaki, Yuma, Nag, Probal, Itakura, Shota, Mizuno, Yosuke, Murakoshi, Shunya, Tanaka, Tatsuki, Larom, Shirley, Konno, Masae, Abe-Yoshizumi, Rei, Molina-Márquez, Ana, Bárcenas-Pérez, Daniela, Cheel, José, Koblížek, Michal, León, Rosa, Katayama, Kota, Kandori, Hideki, Schapiro, Igor, Shihoya, Wataru, Nureki, Osamu, Inoue, Keiichi, Rozenberg, Andrey, Chazan, Ariel, Béjà, Oded·2025·Nature Microbiology
DOI 10.1038/s41564-025-02016-5PMC PMC12137139

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Abstract

Aquatic bacterial rhodopsin proton pumps harvest light energy for photoheterotrophic growth and are known to contain hydroxylated carotenoids that expand the wavelengths of light utilized, but these have not been characterized in marine archaea. Here, by combining a marine chromophore extract with purified archaeal rhodopsins identified in marine metagenomes, we show light energy transfer from diverse hydroxylated carotenoids to heimdallarchaeial rhodopsins (HeimdallRs) from uncultured marine planktonic members of 'Candidatus Kariarchaeaceae' ('Candidatus Asgardarchaeota'). These light-harvesting antennas absorb in the blue-light range and transfer energy to the green-light-absorbing retinal chromophore within HeimdallRs, enabling the use of light that is otherwise unavailable to the rhodopsin. Furthermore, we show elevated proton pumping by the antennas in HeimdallRs under white-light illumination, which better simulates the light conditions encountered by these archaea in their natural habitats. Our results indicate that light-harvesting antennas in microbial rhodopsins exist in families beyond xanthorhodopsins and proteorhodopsins and are present in both marine bacteria and archaea.

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Metadata

Authors
Tzlil, G., Marín, M. D. C., Matsuzaki, Y., Nag, P., Itakura, S., Mizuno, Y., Murakoshi, S., Tanaka, T., Larom, S., Konno, M., Abe-Yoshizumi, R., Molina-Márquez, A., Bárcenas-Pérez, D., Cheel, J., Koblížek, M., León, R., Katayama, K., Kandori, H., Schapiro, I., Shihoya, W., Nureki, O., Inoue, K., Rozenberg, A., Chazan, A., & Béjà, O.
Affiliations
  • Technion – Israel Institute of Technology (IL)
  • The University of Tokyo (JP)
  • Hebrew University of Jerusalem (IL)
  • Nagoya Institute of Technology (JP)
  • The Institute for Solid State Physics, The University of Tokyo (JP)
  • Universidad de Huelva (ES)
  • Czech Academy of Sciences (CZ)
Corresponding author
  • Shihoya, Wataru
  • Nureki, Osamu
  • Inoue, Keiichi
  • Rozenberg, Andrey
  • Chazan, Ariel
  • Béjà, Oded
ORCID
Venue
Nature Microbiology
Publisher
Springer Science and Business Media LLC
Published
2025-05-29
Volume
10
Issue
6
Pages
1484-1500
ISSN
2058-5276 (ISSN-L)
DOI
10.1038/s41564-025-02016-5
PMC
PMC12137139
OpenAlex
W4410867306
Cited by
9
References
2
Citations by year
2026: 3 · 2025: 6
FWCI
3.53
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Microbiology (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Repositorio Institucional de la Universidad de Huelva (Universidad de Huelva) (submittedVersion)
Funders
  • Israel Science Foundation (3131/20)
  • MEXT | Japan Society for the Promotion of Science (JPMXP1323015482)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Photoreceptor and optogenetics research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
Keywords
rhodopsin, light-harvesting antenna, Asgard archaea, chromophores, light energy transfer, proton translocation, marine plankton, photoheterotrophy, blue light absorption, retinal chromophore
MeSH terms
Archaea, Carotenoids, Energy Transfer, Light, Phylogeny, Rhodopsin, Seawater, Archaeal Proteins, Rhodopsins, Microbial, Light-Harvesting Protein Complexes, Metagenome, Aquatic Organisms

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