Phototrophy by antenna-containing rhodopsin pumps in aquatic environments

Ariel Chazan, Ishita Das, Takayoshi Fujiwara, Shunya Murakoshi, Andrey Rozenberg, Ana Molina-Márquez, Fumiya K. Sano, Tatsuki Tanaka, Patricia Gómez-Villegas, Shirley Larom, Alina Pushkarev, Partha Malakar, Masumi Hasegawa, Yuya Tsukamoto, Tomohiro Ishizuka, Masae Konno, Takashi Nagata, Yosuke Mizuno, Kota Katayama, Rei Abe-Yoshizumi, Sanford Ruhman, Keiichi Inoue, Hideki Kandori, Rosa León, Wataru Shihoya (), Susumu Yoshizawa (), Mordechai Sheves (), Osamu Nureki () and Oded Béjà ()
Additional contact information
Ariel Chazan: Technion-Israel Institute of Technology
Ishita Das: Weizmann Institute of Science
Takayoshi Fujiwara: The University of Tokyo
Shunya Murakoshi: The University of Tokyo
Andrey Rozenberg: Technion-Israel Institute of Technology
Ana Molina-Márquez: University of Huelva
Fumiya K. Sano: The University of Tokyo
Tatsuki Tanaka: The University of Tokyo
Patricia Gómez-Villegas: University of Huelva
Shirley Larom: Technion-Israel Institute of Technology
Alina Pushkarev: Technion-Israel Institute of Technology
Partha Malakar: The Hebrew University of Jerusalem
Masumi Hasegawa: The University of Tokyo
Yuya Tsukamoto: The University of Tokyo
Tomohiro Ishizuka: The University of Tokyo
Masae Konno: The University of Tokyo
Takashi Nagata: The University of Tokyo
Yosuke Mizuno: Nagoya Institute of Technology
Kota Katayama: Nagoya Institute of Technology
Rei Abe-Yoshizumi: Nagoya Institute of Technology
Sanford Ruhman: The Hebrew University of Jerusalem
Keiichi Inoue: The University of Tokyo
Hideki Kandori: Nagoya Institute of Technology
Rosa León: University of Huelva
Wataru Shihoya: The University of Tokyo
Susumu Yoshizawa: The University of Tokyo
Mordechai Sheves: Weizmann Institute of Science
Osamu Nureki: The University of Tokyo
Oded Béjà: Technion-Israel Institute of Technology

Nature, 2023, vol. 615, issue 7952, 535-540

Abstract: Abstract Energy transfer from light-harvesting ketocarotenoids to the light-driven proton pump xanthorhodopsins has been previously demonstrated in two unique cases: an extreme halophilic bacterium1 and a terrestrial cyanobacterium2. Attempts to find carotenoids that bind and transfer energy to abundant rhodopsin proton pumps3 from marine photoheterotrophs have thus far failed4–6. 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.

Date: 2023
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DOI: 10.1038/s41586-023-05774-6

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