Structural basis for blue-green light harvesting and energy dissipation in diatoms
Structural basis for blue-green light harvesting and energy dissipation in diatoms
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DOI：
10.1126/science.aav0365
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发表时间：
2019-02-08
期刊：
影响因子：
56.9
通讯作者：
Shen, Jian-Ren
中科院分区：
文献类型：
--
作者：
Wang, Wenda;Yu, Long-Jiang;Shen, Jian-Ren
光合生物含有捕光天线系统，以收集驱动光化学反应所需的光能。硅藻是在世界各地的淡水和海洋中发现的一组真核藻类，通过将大量二氧化碳固定为有机碳，帮助形成海洋初级生产力的基础。硅藻很好地适应了这种环境，因为它们含有具有特殊捕光和光保护能力的捕光天线，称为岩藻黄素（Fx）和叶绿素（Chl）a/c结合蛋白（FCPs）。FCPs含有色素Chl c和Fx，使其能够吸收水下蓝绿色区域的光，但仅含有Chl a/B的生物无法有效利用。这些色素还赋予FCP一个强大的能量淬灭系统，使其在海洋表层（一个光照不断变化的环境）中茁壮成长。RATIONALEFCP蛋白属于跨膜捕光复合物（LHC）蛋白超家族，与绿色谱系生物的主要Lhca（LHCI）和Lhcb（LHCII）亚基序列相似性较低。来自高等植物的LHCI和LHCII的结构，以及来自红蜘蛛的LHCI的结构，先前揭示了这些天线蛋白中色素的结合位点。这一信息尚未为FCP所知，这限制了对蓝绿色区域中的光吸收以及能量转移和耗散的机制的理解。我们解决了来自羽状的三角褐指藻（Phaeodactylum tricornutumat）的二聚体FCP的X射线晶体结构，分辨率为1.8- 1.5。FCP被纯化为二聚体，结构表明两个单体通过其跨膜C螺旋之间的相互作用保持在一起。这不同于在绿色谱系生物的主要LHCII中发现的三聚体的主要组织。每个FCP单体结合9个Chls和7个Fxs; Chls的数量远小于典型的14个Chls，而Fxs的数量大于LHCI和LHCII中发现的3至4个类胡萝卜素，导致FCP中的Fx/Chl比LHCI和LHCII中的高得多。其中两个Chl c位于跨膜螺旋A和B的两侧，分别与附近的两个Chl a和一个Fx紧密相互作用。这表明Chl c不仅与Chl a而且与Fx的快速能量耦合。每个Fx被一个或多个Chls包围，这表明它们之间的有效能量转移以及在强光条件下通过丰富的Fx有效耗散多余能量。每种Fx的两个末端基团的结合环境在蛋白质支架内显示出不同的亲和性，表明它们对蓝绿光的优选吸收区域存在差异。一个diadinoxanthin（Ddx）分子被分配到一个位置靠近单体-单体界面，因为它的弱电子密度，这表明它容易从脱辅基蛋白和可能参与的Ddx-deepoxy循环，功能在energy dissipation. CONCLUSION的FCP结构揭示了一个网络的叶绿素a/c和FXS，使有效的蓝绿色光捕获和能量耗散在硅藻。通过理论计算和时间分辨光谱方法，揭示了每种色素的配体结构和结合环境，从而可以详细研究这组天线中各个色素的吸收特性、能量传递途径和动力学以及多余能量耗散机制。
INTRODUCTIONPhotosynthetic organisms contain light-harvesting antenna systems to gather light energy required for driving photochemical reactions. Diatoms are a group of eukaryotic algae found in fresh water and oceans throughout the world that help form the basis of ocean primary productivity by fixing massive amounts of carbon dioxide into organic carbon. Diatoms are well adapted to this environment in that they contain light-harvesting antennas with exceptional light harvesting and photoprotection capabilities, called fucoxanthin (Fx) and chlorophyll (Chl) a/c-binding proteins (FCPs). FCPs contain the pigments Chl c and Fx, which enable them to absorb light in the blue-green region that is available under water but not effectively used by organisms that contain exclusively Chl a/b. These pigments also confer on FCPs a robust energy-quenching system necessary to thrive in the surface layer of the ocean, an environment with constantly changing light.RATIONALEFCP proteins belong to the superfamily of transmembrane light-harvesting complex (LHC) proteins with low sequence similarity to the main Lhca (LHCI) and Lhcb (LHCII) subunits of the green lineage organisms. The structures of LHCI and LHCII from higher plants, and the structure of LHCI from a red alga, previously revealed the binding sites for pigments in these antenna proteins. This information was not yet known for FCPs, which limited understanding of the mechanism of light absorption in the blue-green region and energy transfer and dissipation.RESULTSWe solved the x-ray crystal structure of a dimeric FCP from a pennate diatomPhaeodactylum tricornutumat 1.8-Å resolution. The FCP was purified as a dimer, and the structure showed that two monomers are held together by interactions between their transmembrane C helices. This differs from the predominant organization of trimers found in the major LHCII of the green-lineage organisms. Each FCP monomer binds nine Chls and seven Fxs; the number of Chls is much less than the typical 14 Chls, whereas that of Fxs is greater than the three to four carotenoids found in LHCI and LHCII, resulting in a much higher Fx/Chl ratio in FCP than those in LHCI and LHCII. Among the Chls, two are Chl c located at two sides of the transmembrane helices A and B, and they are in close interaction with two nearby Chls a and one Fx, respectively. This indicates fast energy coupling of Chl c not only with Chl a but also with Fx. Each Fx is surrounded by one or more Chls, suggesting efficient energy transfer between them and also efficient dissipation of excess energy under high light conditions through the abundant Fxs. The binding environment of the two end groups of each Fx showed different hydrophilicities within the protein scaffold, suggesting differences in their preferred absorption region of the blue-green light. One diadinoxanthin (Ddx) molecule is assigned to a position close to the monomer-monomer interface because of its weak electron density, suggesting its easy dissociation from the apoprotein and possible involvement in the Ddx-deepoxidation cycle that functions in energy dissipation.CONCLUSIONThe FCP structure revealed a network of Chls a/c and Fxs that enables efficient blue-green light harvesting and energy dissipation in diatoms. The ligand structure and binding environment of each pigment revealed in this study will enable detailed studies on the absorption properties of the individual pigments, energy transfer pathways and dynamics, and excess energy dissipation mechanisms in this group of antennas, by both theoretical calculations and time-resolved spectroscopic approaches.Structure of a FCPThe …