Tani Kazutoshi, Kanno Ryo, Nagashima Kenji V P, Kawakami Mai, Hiwatashi Naho, Nakata Kazuna, Nagashima Sakiko, Inoue Kazuhito, Takaichi Shinichi, Purba Endang R, Hall Malgorzata, Yu Long-Jiang, Madigan Michael T, Mizoguchi Akira, Humbel Bruno M, Kimura Yukihiro, Wang-Otomo Zheng-Yu
Center for Computational Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki, Japan.
Graduate School of Medicine, Mie University, Tsu, Japan.
Commun Biol. 2025 Jan 11;8(1):42. doi: 10.1038/s42003-024-07421-w.
Halorhodospira (Hlr.) halophila strain BN9622 is an extremely halophilic and alkaliphilic purple phototrophic bacterium and has been widely used as a model for exploring the osmoadaptive and photosynthetic strategies employed by phototrophic extreme halophiles that enable them to thrive in hypersaline environments. Here we present the cryo-EM structures of (1) a unique native Hlr. halophila triple-complex formed from light-harvesting (LH1), the reaction center (RC), and high-potential iron-sulfur protein (HiPIP) at 2.44 Å resolution, and (2) a HiPIP-free LH1-RC complex at 2.64 Å resolution. Differing from the LH1 in the Hlr. halophila LH1-LH2 co-complex where LH1 encircles LH2, the RC-associated LH1 complex consists of 16 (rather than 18) αβ-subunits circularly surrounding the RC. These distinct forms of LH1 indicate that the number of subunits in a Hlr. halophila LH1 complex is flexible and its size is a function of the photocomplex it encircles. Like LH1 in the LH1-LH2 co-complex, the RC-associated LH1 complex also contained two forms of αβ-polypeptides and both dimeric and monomeric molecules of bacteriochlorophyll a. The majority of the isolated Hlr. halophila LH1-RC complexes contained the electron donor HiPIP bound to the surface of the RC cytochrome subunit near the heme-1 group. The bound HiPIP consisted of an N-terminal functional domain and a long C-terminal extension firmly attached to the cytochrome subunit. Despite overall highly negative surface-charge distributions for both the cytochrome subunit and HiPIP, the interface between the two proteins was relatively uncharged and neutral, forming a pathway for electron tunneling. The structure of the Hlr. halophila LH1-RC-HiPIP complex provides insights into the mechanism of light energy acquisition coupled with a long-distance electron donating process toward the charge separation site in a multi-extremophilic phototroph.
嗜盐嗜盐红螺菌（Halorhodospira, Hlr.）菌株BN9622是一种极端嗜盐和嗜碱的紫色光合细菌，已被广泛用作模型，以探索光合极端嗜盐菌所采用的渗透适应和光合策略，这些策略使它们能够在高盐环境中茁壮成长。在此，我们展示了（1）一种独特的天然嗜盐嗜盐红螺菌三联体复合物的冷冻电镜结构，该复合物由光捕获（LH1）、反应中心（RC）和高电位铁硫蛋白（HiPIP）组成，分辨率为2.44 Å；以及（2）一种不含HiPIP的LH1-RC复合物，分辨率为2.64 Å。与嗜盐嗜盐红螺菌LH1-LH2共复合物中的LH1不同，其中LH1环绕着LH2，与RC相关的LH1复合物由16个（而非18个）αβ亚基组成，围绕着RC呈环状排列。这些不同形式的LH1表明，嗜盐嗜盐红螺菌LH1复合物中的亚基数量是灵活的，其大小是其所环绕的光复合物的函数。与LH1-LH2共复合物中的LH1一样，与RC相关的LH1复合物也包含两种形式的αβ多肽以及细菌叶绿素a的二聚体和单体分子。大多数分离出的嗜盐嗜盐红螺菌LH1-RC复合物含有与RC细胞色素亚基表面靠近血红素-1基团处结合的电子供体HiPIP。结合的HiPIP由一个N端功能域和一个牢固附着在细胞色素亚基上的长C端延伸组成。尽管细胞色素亚基和HiPIP的表面电荷分布总体上高度为负，但这两种蛋白质之间的界面相对不带电且呈中性，形成了电子隧穿的途径。嗜盐嗜盐红螺菌LH1-RC-HiPIP复合物的结构为多极端嗜盐光合生物中光能获取与向电荷分离位点的长距离电子供体过程耦合的机制提供了见解。
