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.

Centre Algatech Institute of Microbiology Czech Academy of Sciences Třeboň Czech Republic

Department of Biological Sciences Graduate School of Science The University of Tokyo Tokyo Japan

Department of Life Science and Applied Chemistry Nagoya Institute of Technology Nagoya Japan

Department of Physics Technische Universität Dortmund Germany

Faculty of Biology Technion Israel Institute of Technology Haifa Israel

Faculty of Science University of South Bohemia České Budějovice Czech Republic

Fritz Haber Center for Molecular Dynamics Research Institute of Chemistry The Hebrew University of Jerusalem Jerusalem Israel

Institute of Environmental Engineering ETH Zurich Switzerland

Laboratory of Biochemistry and Molecular Biology Faculty of Experimental Sciences Marine International Campus of Excellence University of Huelva Huelva Spain

OptoBioTechnology Research Center Nagoya Institute of Technology Nagoya Japan

Physical and Analytical Chemistry Department University of Jaén Jaén Spain

Research Center Chemical Sciences and Sustainability University Alliance Ruhr Bochum Germany

The Institute for Solid State Physics The University of Tokyo Kashiwa Japan

The Nancy and Stephen Grand Technion Energy Program Technion Israel Institute of Technology Haifa Israel

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