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藻类捕光天线系统:结构与功能的统一

甄张赫 李文军 林瀚智 秦松

甄张赫,李文军,林瀚智,等. 藻类捕光天线系统:结构与功能的统一[J]. 海洋学报,2021,43(2):126–138 doi: 10.12284/hyxb2021024
引用本文: 甄张赫,李文军,林瀚智,等. 藻类捕光天线系统:结构与功能的统一[J]. 海洋学报,2021,43(2):126–138 doi: 10.12284/hyxb2021024
Zhen Zhanghe,Li Wenjun,Lin Hanzhi, et al. Algal light-harvesting system: Linkage of structures and functions by using structural biology[J]. Haiyang Xuebao,2021, 43(2):126–138 doi: 10.12284/hyxb2021024
Citation: Zhen Zhanghe,Li Wenjun,Lin Hanzhi, et al. Algal light-harvesting system: Linkage of structures and functions by using structural biology[J]. Haiyang Xuebao,2021, 43(2):126–138 doi: 10.12284/hyxb2021024

藻类捕光天线系统:结构与功能的统一

doi: 10.12284/hyxb2021024
基金项目: 国家自然科学基金(419061094,2061134020);广东省科学院实施创新驱动发展能力建设专项(2020GDASYL-20200102015)。
详细信息
    作者简介:

    甄张赫(1992—),女,辽宁省盖平县人,博士研究生,主要从事藻类捕光蛋白结构及其功能机制研究。E-mail:zhzhen@yic.ac.cn

    通讯作者:

    秦松,研究员,主要从事分子藻类学与产品工程相关工作。E-mail:sqin@yic.ac.cn

  • 中图分类号: Q949.2

Algal light-harvesting system: Linkage of structures and functions by using structural biology

  • 摘要: 藻类是光合自养的水生孢子植物,为了适应水下弱光的特殊生境,藻类捕光天线历经亿万年的进化,形成了特殊的结构与功能。从发现藻类捕光天线的存在到至今的70多年间,其结构解析技术的发展共经历了4个阶段:首先是利用生化及普通光谱技术研究结构组成(1950−1980年);其次是利用X-ray晶体学技术研究局部精细结构(1980年至今);再次是利用电镜技术研究完整的粗略结构(1980−2010年);最后是近10年来利用冷冻电镜技术研究完整的精细结构(2010年至今)。目前以蓝藻、红藻、绿藻和硅藻为主的藻类捕光天线复合体完整的精细结构均已被解析,仅2019年就有10余种精细结构被发现。藻类捕光天线系统结构生物学的研究,不仅搭建了对结构与功能统一认识的桥梁,而且为深入揭示藻类光合作用高效能量传递机制奠定了坚实的结构基础。将藻类捕光天线系统结构和功能统一起来,进一步研究对光环境的适应性成为未来的重点,并将为藻类捕光天线蛋白在光电器件领域的应用提供充分的科学依据。
  • 图  1  捕光复合体粗略结构及精细结构对比

    A. 红藻(Porphyridium cruentum)PBS 电镜结构(粗略结构)(图片引自文献[24]);B. 红藻(P. purpureum)PBS 冷冻电镜精细结构(图片源于PDB库,PDB码为6KGX);C. 豌豆C2S2M2-type PSII-LHCII 电镜结构(粗略结构)(图片引自文献[79]);D. 绿藻(Chlamydomonas reinhardtii)C2S2M2N2-type PSII-LHCII 冷冻电镜精细结构(图片源于PDB库,PDB码为6KAF)

    Fig.  1  Comparison of contour and fine structures of algal light-harvesting complexes

    A. The rough structure of PBS from red alga Porphyridium cruentum by using electron microscope (picture quoted from reference [24]); B. the fine-structure of PBS from red alga P. purpureum by using cryo-electron microscope (PDB code is 6KGX); C. the electron microscope structure (rough structure) of C2S2M2-type PSII-LHCII from pea (picture quoted from reference [79]); D. the fine cryo-electron microscope structure of C2S2M2N2-type PSII-LHCII from Chlamydomonas reinhardtii (picture quoted from PDB library, PDB code is 6KAF)

    图  2  计算生物学分析蓝藻藻胆蛋白同源序列及结构[90]

    A为通过计算生物学比对蓝藻的藻胆蛋白同源序列,识别非同义替换升高的位点(后验概率大于80%);横轴为藻胆蛋白中的氨基酸排列位点;纵轴为后验概率;A、B、E、F、F’、G、H代表7个螺旋,X、Y代表每个亚基N段的螺旋发卡域;浅灰色为α亚基,暗灰色为β亚基;图内部的a−d分支分别为PEC、PC、PE和APC。B为蓝藻藻蓝蛋白三维结构;灰色球状填充为dN/dS(同义频率/非同义频率)替换比例升高的残基;螺旋状条带表示蛋白质的α亚基和β亚基;灰色杆状表示生色团

    Fig.  2  Computational biology analysis of cyanobacterial phycobiliprotein homologous sequence and structure [90]

    A represent alignment of cyanobacterial phycobiliprotein homologous sequences to identify sites with increased non-synonymous substitutions (posterior probabilities>80%); the horizontal axis is amino acid arrangement sites; the vertical axis is posterior probability; A, B, E, F, F’, G, and H represent seven helices, X and Y represent the spiral hairpin domain at the N-terminus of each subunit; the gray lines represent α subunit, the dark gray lines represent β subunit; a-d represent PEC, PC, PE and APC, respectively. B represent three-dimensional structure of cyanobacterial phycocyanin; gray spheres represent the residues with increased synonymous frequency/non-synonymous frequency substitution ratio; helixes represent α subunit and β subunit; gray lines represent chromophore

    图  3  FCP单体结构及其色素组成[36]

    硅藻(P. tricornutum)FCP单体的结构信息来自PDB数据库(http://www.rcsb.org/),PDB码为6A2W

    Fig.  3  Monomer structure and pigment composition of FCP [36]

    The structure of the FCP monomer from diatom P. tricornutum is provided by PDB database (http://www.rcsb.org/), PDB code is 6A2W

    图  4  藻胆体光保护结构模型

    a. 藻胆体的OCP依赖型NPQ机制模型,图片引自文献[103];b. 藻胆体状态转换模型,状态一为移动传能机制,状态二为能量溢出机制,红色箭头为能量传递路径

    Fig.  4  Photoprotective structural model of phycobilisomes

    a. The mechanism model of OCP-dependent NPQ in phycobilisomes, picture quoted from reference [103]; b. phycobilisome state transition model, state 1 represents mobile energy transfer mechanism, state 2 represents overflow mechanism, red arrow represents energy transfer path

    表  1  藻类捕光天线复合体粗略结构及精细结构

    Tab.  1  Contour model and fine structures of algal light-harvesting antenna complexes

    捕光天线类型粗略结构
    鉴定方法
    结构结果与功能的关系引用文献精细结构
    鉴定方法
    结构结果与功能的关系引用文献
    PBS生理生化+
    光谱技术
    蛋白凝胶电泳鉴定藻胆体由藻胆蛋白及各种连接多肽组成;光谱测量藻胆体光吸收范围为460~700 nm
    揭示捕光范围及可能的
    能量传递路径
    [29]X-ray藻胆蛋白脱辅基蛋白结构、结合色素类型及色素结合位点
    通过结合色素类型
    及结合方式预测
    能量传递路径
    [41]
    普通电镜PBS结构具有多样性,如半椭圆形、块状等结合藻类生境,对比多种PBS形状及
    粗略结构,可揭示PBS形状与周围
    光环境的适应规律
    [21]冷冻电镜PBS完整结构及细节结构,如各类连接蛋白组成的骨架形式;色素网络及色素结合位点揭示PBS组装机制及
    能量传递途径
    [42]
    LHC及其与光系统的复合物生理生化+
    光谱技术
    蛋白凝胶电泳鉴定LHC蛋白大小及部分超分子复合体含有LHC的数量;光谱测量LHC光吸收范围为350~700 nm


    揭示捕光范围[43]X-ray脱辅基蛋白结构、结合色素类型及色素结合位点
    揭示内部能量
    传递路径
    [36]
    普通电镜超分子复合体可能的组成成分,例如观察不同藻类的PSII-LHCII复合体中LHC的排列方式及数量通过LHC与光合反应中心的结合
    方式推测可能的能量传递方式
    [44]冷冻电镜复合体完整精细结构能量传递途径及
    光保护机制
    [45]
      注:图片1引自文献[29]。图片1:SDS-聚丙烯酰胺凝胶电泳-Synechococcus PCC 6701的PBS多肽。图片2:隐藻(Chroomonas sp. CCMP270)捕光天线PC645晶体结构,结构下载于PDB(http://www.rcsb.org/),PDB码:4LMS,分辨率为1.35 Å。图片3和图片4引自文献[43]。图片3:褐藻Fx and Chl a/c bindingprotein A (FCPA)提取图;A:Triton-X-100样品提取处理;B:蔗糖梯度(0.2~0.5 mol/L蔗糖)样品分离。图片4:褐藻FCPA吸收光谱(波长450 nm处的上方线)及荧光发射光谱(波长450 nm处的下方线)的对比图。图片5:硅藻捕光天线FCP晶体结构,结构下载于PDB(http://www.rcsb.org/),PDB码为6A2W,分辨率为1.8 Å。
    下载: 导出CSV

    表  2  藻类捕光天线复合体晶体结构解析进展

    Tab.  2  Progress in crystal structure analysis of algal light-harvesting antenna complexes

    藻类PSII主要捕光天线PSI主要捕光天线结合色素文献
    蓝藻PBS: APC*, PC*, PE*, PEC (phycoerythrocyanin)*IsiA (Iron-stress-induced protein)PCB, PEB, PUB, PVB, Chl a[26, 46-48]
    红藻PBS: APC*, PC*, PE*LHCR: LhcrPCB, PEB, PUB, Chl a[5, 21, 49-51]
    绿藻LHCII: Lhcb1-3, CP24, CP26, CP29*LHCI*: LhcaChl a, Chl b[52-54]
    隐藻Cr(Cryptophytes)-PBP (phycobiliprotein): Cr-PC*/Cr-PE*; LHC: Lhcr, Lhcz同PSIIPCB, PEB, MBV(mesobiliverdin), DBV(dihydrobiliverdin), bilin 584, bilin 618, Chl a, Chl c, alloxanthin[55]
    硅藻FCP*: Lhcf, Lhcx同PSIIChl a, Chl c, Fx, Dt, Dd[56-58]
    褐藻FCP: Lhcf, Lhcr, Lhcx, Lhcz同PSIIChl a, Chl c, Fx,violaxanthin, zeaxanthin, Dt, Dd[43, 58-59]
    甲藻PCP*;LHC: Lhcr, Lhcf, Lhcx同PSIIChl a, Chl c, Fx, violaxanthin[60-61]
    黄藻XLH (Xanthophyceae light-harvesting complex) IIXLHIChl a, Chl c, Dd, Dt[62]
    金藻LHCLHCChl a, Chl c, Fx, violaxanthin[63-64]
    裸藻LHCLHCChl a, Chl b, neoxanthin, Dt, Dd, β-carotene[65-67]
    轮藻LHCLHCChl a, Chl b, α-carotene, β-carotene, γ-carotene, lutein, eaxanthin, neoxanthin, zeaxanthin, violaxanthin,[65-67]
      注:*代表已有高分辨晶体结构。
    下载: 导出CSV

    表  3  电镜技术解析藻类捕光复合体结构的研究进展

    Tab.  3  Advance in electron microscope analysis of algal light-harvesting complexes

    藻类捕光天线复合体电镜冷冻电镜解析分辨率(冷冻电镜)引用文献
    蓝藻IsiA-PSI3.5 Å[76, 80]
    PBS13 Å[25]
    PBSrod-PSI[81]
    PBS-PSII[82-83]
    红藻PSI-LHCI3.82 Å[74]
    PBS3.5 Å, 2.82 Å[22, 42]
    绿藻PSI-LHCI3.49 Å, 2.9 Å[75, 84]
    PSII-LHCII3.2 Å[85]
    C2S2-type PSII-LHCII2.7 Å[45]
    C2S2M2-type PSII-LHCII3.2 Å[86]
    C2S2M2N2-type PSII LHCII3.7 Å[74]
    C2S2M2L2-type PSII LHCII3.4 Å[45]
    PSI-LHCI-LHCII[44]
    硅藻PSI-FCPI[87-88]
    PSII-FCPII3.02 Å, 3.8 Å[78, 89]
    隐藻PSI-LHCI[72]
    黄藻XLH[71]
      注:*代表已有高分辨晶体结构,√代表已用该技术进行了结构解析,−代表无分辨率报道。
    下载: 导出CSV
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  • 收稿日期:  2020-05-23
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