Phototrophy by antenna-containing rhodopsin pumps in aquatic environments

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 r...

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Veröffentlicht in:Nature (London) 2023-03, Vol.615 (7952), p.535-540
Hauptverfasser: 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
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container_start_page 535
container_title Nature (London)
container_volume 615
creator 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
description 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.
doi_str_mv 10.1038/s41586-023-05774-6
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Yuya</au><au>Ishizuka, Tomohiro</au><au>Konno, Masae</au><au>Nagata, Takashi</au><au>Mizuno, Yosuke</au><au>Katayama, Kota</au><au>Abe-Yoshizumi, Rei</au><au>Ruhman, Sanford</au><au>Inoue, Keiichi</au><au>Kandori, Hideki</au><au>León, Rosa</au><au>Shihoya, Wataru</au><au>Yoshizawa, Susumu</au><au>Sheves, Mordechai</au><au>Nureki, Osamu</au><au>Béjà, Oded</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Phototrophy by antenna-containing rhodopsin pumps in aquatic environments</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2023-03-16</date><risdate>2023</risdate><volume>615</volume><issue>7952</issue><spage>535</spage><epage>540</epage><pages>535-540</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><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 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.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>36859551</pmid><doi>10.1038/s41586-023-05774-6</doi><tpages>6</tpages><orcidid>https://orcid.org/0000-0001-6481-7448</orcidid><orcidid>https://orcid.org/0000-0001-6629-0192</orcidid><orcidid>https://orcid.org/0000-0002-9952-4685</orcidid><orcidid>https://orcid.org/0000-0002-6898-4347</orcidid><orcidid>https://orcid.org/0000-0002-5048-8169</orcidid><orcidid>https://orcid.org/0000-0002-4922-1344</orcidid><orcidid>https://orcid.org/0000-0001-8498-4374</orcidid><orcidid>https://orcid.org/0000-0003-1813-7008</orcidid><orcidid>https://orcid.org/0000-0002-0605-1816</orcidid><orcidid>https://orcid.org/0000-0002-5536-9193</orcidid><orcidid>https://orcid.org/0000-0003-4813-5740</orcidid><orcidid>https://orcid.org/0000-0002-0511-8724</orcidid><orcidid>https://orcid.org/0000-0001-5379-2951</orcidid><orcidid>https://orcid.org/0000-0002-4874-0679</orcidid><orcidid>https://orcid.org/0000-0001-9534-2297</orcidid><orcidid>https://orcid.org/0000-0001-9667-6010</orcidid></addata></record>
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identifier ISSN: 0028-0836
ispartof Nature (London), 2023-03, Vol.615 (7952), p.535-540
issn 0028-0836
1476-4687
language eng
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source MEDLINE; SpringerLink Journals; Nature Journals Online
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
title Phototrophy by antenna-containing rhodopsin pumps in aquatic environments
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