Light-harvesting by antenna-containing rhodopsins in pelagic Asgard archaea

Gali Tzlil, Maria del Carmen Marin, Yuma Matsuzaki, Probal Nag, Shota Itakura, Yosuke Mizuno, Shunya Murakoshi, Tatsuki Tanaka, Shirley Larom, Masae Konno, Rei Abe-Yoshizumi, Ana Molina-Marquez, Daniela Barcenas-Perez, Jose Cheel, Michal Koblizek, Rosa Leon, Kota Katayama, Hideki Kandori, Igor Schapiro, Wataru Shihoya, Osamu Nureki, Keiichi Inoue, Andrey Rozenberg, Ariel Chazan, Oded Beja
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Abstract

Aquatic bacterial rhodopsin proton pumps have been recently reported to utilize hydroxylated carotenoids1,2. Here, by combining a marine chromophore extract with purified archaeal rhodopsins identified in marine metagenomes, we report on light energy transfer from diverse hydroxylated carotenoids (lutein, diatoxanthin, and fucoxanthin) to heimdallarchaeial rhodopsins (HeimdallRs)3,4 from uncultured marine planktonic members of the 'Ca. Kariarchaeaceae' ('Ca. Asgardarchaeota')5. These light-harvesting antennas absorb in the blue-light range and transfer energy to the green-light absorbing retinal chromophore within HeimdallRs. Furthermore, antenna enhancement of proton pumping by HeimdallRs is also observed under white-light illumination along with a carotenoid-binding induced structural change in the protein. Our results indicate that the use of light-harvesting antennas in microbial rhodopsins is observed not only in bacteria but also in marine archaea.
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浮游阿斯加德古菌中含触角的罗多普勒蛋白的光收集作用
最近有报道称,水生细菌的视黄素质子泵可利用羟基类胡萝卜素1,2。在这里,通过将海洋发色团提取物与在海洋元基因组中鉴定出的纯化的古细菌视紫红质相结合,我们报告了光能从多种羟基类胡萝卜素(叶黄素、二硅氧黄质和岩藻黄质)向海姆达尔古细菌视紫红质(HeimdallRs)3,4 转移的情况,这些视紫红质来自未培养的海洋浮游生物 "Ca.这些光收集天线吸收蓝光,并将能量转移到 HeimdallRs 内吸收绿光的视网膜发色团上。此外,在白光照射下,还观察到 HeimdallRs 质子泵的天线增强作用以及类胡萝卜素结合引起的蛋白质结构变化。我们的研究结果表明,不仅在细菌中,在海洋古细菌中也能观察到微生物罗多普勒蛋白使用光收集天线的现象。
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