Phototrophy by antenna-containing rhodopsin pumps in aquatic environments

• Published in: Nature (London) 2023-03, Vol.615 (7952), p.535-540
• Main Authors: Chazan, Ariel, Das, Ishita, Fujiwara, Takayoshi, Murakoshi, Shunya, Rozenberg, Andrey, Molina-Márquez, Ana, Sano, Fumiya K., Tanaka, Tatsuki, Gómez-Villegas, Patricia, Larom, Shirley, Pushkarev, Alina, Malakar, Partha, Hasegawa, Masumi, Tsukamoto, Yuya, Ishizuka, Tomohiro, Konno, Masae, Nagata, Takashi, Mizuno, Yosuke, Katayama, Kota, Abe-Yoshizumi, Rei, Ruhman, Sanford, Inoue, Keiichi, Kandori, Hideki, León, Rosa, Shihoya, Wataru, Yoshizawa, Susumu, Sheves, Mordechai, Nureki, Osamu, Béjà, Oded
• Format: Article
• Language: English
• Subjects: 101/28; 631/158/855; 631/57/1464; Antennas; Aquatic environment; Aquatic Organisms - metabolism; Aquatic Organisms - radiation effects; Bacteria - metabolism; Bacteria - radiation effects; Carotenoids; Carotenoids - metabolism; Chromophores; Color; Cyanobacteria - metabolism; Cyanobacteria - radiation effects; Electromagnetic absorption; Energy; Energy harvesting; Energy transfer; Heterotrophic Processes - radiation effects; Humanities and Social Sciences; Ketocarotenoids; Lakes; Light; Lutein - metabolism; Lutein - radiation effects; Metagenome; Metagenomics; Microorganisms; multidisciplinary; Oceans; Oceans and Seas; Phototrophic Processes - radiation effects; Phototrophy; Proteins; Proton Pumps - metabolism; Proton Pumps - radiation effects; Protons; Retina; Rhodopsin; Rhodopsins, Microbial - metabolism; Rhodopsins, Microbial - radiation effects; Science; Science (multidisciplinary); Zeaxanthin; Zeaxanthins - metabolism; Zeaxanthins - radiation effects
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/s41586-023-05774-6

Energy transfer from light-harvesting ketocarotenoids to the light-driven proton pump xanthorhodopsins has been previously demonstrated in two unique cases: an extreme halophilic bacterium 1 and a terrestrial cyanobacterium 2 . Attempts to find carotenoids that bind and transfer energy to abundant rhodopsin proton pumps 3 from marine photoheterotrophs have thus far failed 4 – 6 . Here we detected light energy transfer from the widespread hydroxylated carotenoids zeaxanthin and lutein to the retinal moiety of xanthorhodopsins and proteorhodopsins using functional metagenomics combined with chromophore extraction from the environment. The light-harvesting carotenoids transfer up to 42% of the harvested energy in the violet- or blue-light range to the green-light absorbing retinal chromophore. Our data suggest that these antennas may have a substantial effect on rhodopsin phototrophy in the world’s lakes, seas and oceans. However, the functional implications of our findings are yet to be discovered. Light energy transfer from abundant hydroxylated carotenoids to the retinal moiety of widespread light-driven proton pumps is detected.