Structural basis of sensory receptor evolution in octopus.

Structural basis of sensory receptor evolution in octopus.
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DOI:
10.1038/s41586-023-05822-1
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发表时间:
2023-04
期刊:
影响因子:
64.8
通讯作者:
Bellono, Nicholas W.
Bellono, Nicholas W.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Allard, Corey A. H.;Kang, Guipeun;Kim, Jeong Joo;Valencia-Montoya, Wendy A.;Hibbs, Ryan E.;Bellono, Nicholas W.

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化学触觉感受器(CR)是一种头足类特有的创新,可以让章鱼通过“触摸味觉”探索海底。CRs从烟碱乙酰胆碱受体分化出来,介导在海洋环境中不易扩散的不溶性分子的接触依赖性化学感觉。在这里,我们利用章鱼CRs探测感觉受体进化的结构基础。我们提出了冷冻电镜结构的章鱼CR和比较它与烟碱受体,以确定功能,使环境感觉与神经传递。进化、结构和生物物理分析表明,参与阳离子渗透和信号转导的通道结构是保守的。相反,正构配体结合位点受到多样化选择,从而介导新分子的检测。在冷冻电子显微镜结构中的偶然发现揭示了章鱼CR配体结合口袋是异常疏水的,使得能够感觉到油脂化合物与通过典型神经递质受体检测到的小极性分子。这些发现为理解原子水平上的进化适应与新生物行为的出现之间的联系提供了一个结构框架。
Chemotactile receptors (CRs) are a cephalopod-specific innovation that allow octopuses to explore the seafloor via ‘taste by touch’. CRs diverged from nicotinic acetylcholine receptors to mediate contact-dependent chemosensation of insoluble molecules that do not readily diffuse in marine environments. Here, we exploit octopus CRs to probe the structural basis of sensory receptor evolution. We present the cryo-electron microscopy structure of an octopus CR and compare it with nicotinic receptors to determine features that enable environmental sensation versus neurotransmission. Evolutionary, structural and biophysical analyses show that channel architecture involved in cation permeation and signal transduction is conserved. In contrast, the orthosteric ligand-binding site is subject to diversifying selection, thereby mediating the detection of new molecules. Serendipitous findings in the cryo-electron microscopy structure reveal that the octopus CR ligand-binding pocket is exceptionally hydrophobic, enabling sensation of greasy compounds versus the small polar molecules detected by canonical neurotransmitter receptors. These discoveries provide a structural framework for understanding connections between evolutionary adaptations at the atomic level and the emergence of new organismal behaviour.
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