Convergent evolution of tertiary structure in rhodopsin visual proteins from vertebrates and box jellyfish.
Convergent evolution of tertiary structure in rhodopsin visual proteins from vertebrates and box jellyfish.
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DOI：
10.1073/pnas.1721333115
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发表时间：
2018-06-12
影响因子：
11.1
通讯作者：
Lucas RJ
中科院分区：
文献类型：
--
作者：
Gerrard E;Mutt E;Nagata T;Koyanagi M;Flock T;Lesca E;Schertler GFX;Terakita A;Deupi X;Lucas RJ
复杂的光感受器在径向对称和双侧对称的动物中独立进化，但对径向对称动物中转导光信息的蛋白质（视蛋白）知之甚少。我们利用同源建模和异源作用光谱研究了视觉能力强的箱形水母（Carybdea rastonii）晶状体眼的视蛋白（JellyOp）的结构。我们发现动物视蛋白的一个关键结构特征——反作用——在JellyOp中从一个独特的位置（跨膜束中的E94）维持可见光敏感性。这种独特的反离子位置，仅在动物视蛋白中发现的第三个，密切反映了脊椎动物视觉蛋白的位置，这被认为是脊椎动物实现高保真光接收的独特适应。箱形水母和脊椎动物的进化间隔了大约5亿年，但它们的晶体眼睛结构相似，都是利用视紫红质来维持视力的。所有视蛋白都有一个带负电的残基-反-以维持可见光敏感性并促进视黄醛发色团的光异构化。在脊椎动物视紫红质中，反离子位置的分子进化——从第二个细胞外环的高度保守的远端位置（E181）到第三个跨膜螺旋的近端位置（E113）——被确定为高保真度光接受的关键驱动因素。在这里，我们使用计算生物学和异源作用光谱来确定箱形水母高级视觉装置的出现是否也伴随着视蛋白三级结构的变化。我们发现箱形水母（JellyOp）晶状体眼的视蛋白中的反离子也移动到TM2跨膜束e94内的一个独特的近端位置。此外，我们发现这个希夫碱/反离子系统包括一个额外的正电荷r186，它与E94共同进化，在JellyOp的发色团结合口袋中分离E94和E181。通过设计这种口袋中和R186和E94，或者将E94与脊椎动物的反离子e113交换，我们可以分别重建无脊椎动物和脊椎动物反离子系统的版本，在动物视蛋白的这个区域支持相对相似的整体结构。总之，我们的数据建立了动物视蛋白中唯一的第三个反离子位点，并揭示了具有先进视觉系统的远亲物种视蛋白三级结构的趋同进化。
Complex photoreceptors have independently evolved in animals with radial and bilateral symmetry, but little is known about the proteins that transduce light information (opsins) in radially symmetrical animals. We use homology modeling and heterologous action spectroscopy to study the structure of an opsin (JellyOp) from the lens eye of the visually competent box jellyfish, Carybdea rastonii. We find that a key structural feature of animal opsins—the counterion—maintains visible-light sensitivity in JellyOp from a unique location, E94 in the transmembrane bundle. This unique position for the counterion, the third only discovered in animal opsins, closely mirrors the location in vertebrate visual proteins, which was thought to be a unique adaptation in vertebrates to achieve higher fidelity photoreception. Box jellyfish and vertebrates are separated by >500 million years of evolution yet have structurally analogous lens eyes that employ rhodopsin photopigments for vision. All opsins possess a negatively charged residue—the counterion—to maintain visible-light sensitivity and facilitate photoisomerization of their retinaldehyde chromophore. In vertebrate rhodopsins, the molecular evolution of the counterion position—from a highly conserved distal location in the second extracellular loop (E181) to a proximal location in the third transmembrane helix (E113)—is established as a key driver of higher fidelity photoreception. Here, we use computational biology and heterologous action spectroscopy to determine whether the appearance of the advanced visual apparatus in box jellyfish was also accompanied by changes in the opsin tertiary structure. We found that the counterion in an opsin from the lens eye of the box jellyfish Carybdea rastonii (JellyOp) has also moved to a unique proximal location within the transmembrane bundle—E94 in TM2. Furthermore, we reveal that this Schiff base/counterion system includes an additional positive charge—R186—that has coevolved with E94 to functionally separate E94 and E181 in the chromophore-binding pocket of JellyOp. By engineering this pocket—neutralizing R186 and E94, or swapping E94 with the vertebrate counterion E113—we can recreate versions of the invertebrate and vertebrate counterion systems, respectively, supporting a relatively similar overall architecture in this region of animal opsins. In summary, our data establish the third only counterion site in animal opsins and reveal convergent evolution of tertiary structure in opsins from distantly related species with advanced visual systems.
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影响因子：
3.7
作者：
Bailes HJ;Zhuang LY;Lucas RJ
通讯作者：
Lucas RJ
影响因子：
5.5
作者：
Best, Robert B.;Zhu, Xiao;Shim, Jihyun;Lopes, Pedro E. M.;Mittal, Jeetain;Feig, Michael;MacKerell, Alexander D., Jr.
通讯作者：
MacKerell, Alexander D., Jr.
影响因子：
10.7
作者：
Hanson-Smith V;Kolaczkowski B;Thornton JW
通讯作者：
Thornton JW
影响因子：
5.4
作者：
Bailes HJ;Milosavljevic N;Zhuang LY;Gerrard EJ;Nishiguchi T;Ozawa T;Lucas RJ
通讯作者：
Lucas RJ
影响因子：
64.8
作者：
Nilsson, DE;Gislén, L;Garm, A
通讯作者：
Garm, A