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Toxin-like neuropeptides in the sea anemone Nematostella unravel recruitment from the nervous system to venom
bioRxiv - Evolutionary Biology Pub Date : 2020-05-30 , DOI: 10.1101/2020.05.28.121442
Maria Y. Sachkova , Morani Landau , Joachim M. Surm , Jason Macrander , Shir Singer , Adam M. Reitzel , Yehu Moran

The sea anemone Nematostella vectensis (Anthozoa, Cnidaria) is a powerful model system for characterizing the evolution of genes functioning in venom and nervous systems. Despite being an example for evolutionary novelty, the evolutionary origin of most toxins remains unknown. Here we report the first bona fide case of protein recruitment from the cnidarian nervous to venom system. The ShK-like1 peptide has ShKT cysteine motif, is lethal for fish larvae and packaged into nematocysts, the cnidarian venom-producing stinging capsules. Thus, ShK-like1 is a toxic venom component. Its paralog, ShK-like2, is a neuropeptide localized to neurons and is involved in development. Interestingly, both peptides exhibit similarities in their functional activities: both of them provoke contraction in Nematostella polyps and are toxic to fish. Because ShK-like2 but not ShK-like1 is conserved throughout sea anemone phylogeny, we conclude that the two paralogs originated due to a Nematostella-specific duplication of a ShK-like2 ancestor, a neuropeptide-encoding gene, followed by diversification and partial functional specialization. Strikingly, ShK-like2 is represented by two gene isoforms controlled by alternative promoters conferring regulatory flexibility throughout development. Additionally, we characterized the expression patterns of four other peptides with structural similarities to studied venom components, and revealed their unexpected neuronal localization. Thus, we employed genomics, transcriptomics and functional approaches to reveal one new venom component, five neuropeptides with two different cysteine motifs and an evolutionary pathway from nervous to venom system in Cnidaria.

中文翻译:

海葵Nematostella中的毒素样神经肽解毒,从神经系统到毒液。

海葵线虫Nematostella vectensis(Anthozoa,Cnidaria)是一个强大的模型系统,用于表征在毒液和神经系统中起作用的基因的进化。尽管是进化新颖的一个例子,但大多数毒素的进化起源仍然未知。在这里,我们报道了从CNIDIAN神经系统到毒液系统的第一个真正的蛋白质募集案例。ShK-like1肽具有ShKT半胱氨酸基序,对鱼幼虫具有致死性,并被包装成线虫囊,即产生刺鼻毒液的刺痛胶囊。因此,ShK-like1是有毒的毒液成分。它的旁系同源蛋白ShK-like2是一种定位于神经元的神经肽,参与发育。有趣的是,这两种肽在功能活性上都表现出相似性:它们都引起线虫结肠息肉收缩,并且对鱼类有毒。因为在整个海葵系统发育过程中,ShK-like2而不是ShK-like1是保守的,所以我们得出结论,这两个旁系同源体是由于NeKostostella特定地复制了ShK-like2祖先,一种神经肽编码基因,然后进行了多样化和部分功能专门化。令人惊讶的是,ShK-like2由两个基因的同工型所代表,这些同工型由其他启动子控制,可在整个开发过程中赋予调节灵活性。此外,我们表征了与研究毒液成分具有结构相似性的其他四种肽的表达模式,并揭示了其意外的神经元定位。因此,我们采用了基因组学,转录组学和功能方法来揭示一种新的毒液成分,
更新日期:2020-05-30
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