Insights into the origins of fish hunting in venomous cone snails from studies of Conus tessulatus

Insights into the origins of fish hunting in venomous cone snails from studies of Conus tessulatus
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DOI:
10.1073/pnas.1424435112
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发表时间:
2015-04-21
影响因子:
11.1
通讯作者:
Olivera, Baldomero M.
Olivera, Baldomero M.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Aman, Joseph W.;Imperial, Julita S.;Olivera, Baldomero M.

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食肉捕食者的猎物转移是可以加速新生物多样性产生的事件。然而,很少有可能重建猎物偏好的变化是如何发生的。在这里,我们描述了一个进化的“确凿证据”,它阐明了海洋锥螺从捕食蠕虫到捕食鱼类的转变,导致了由大约100种食鱼圆锥螺组成的捕食鱼类谱系的适应性辐射。这个确凿的证据就是三角螺毒素TsVIA,一种来自圆锥蛇毒液的肽,可以延缓脊椎动物电压门控钠通道的失活。C. tessulatus是蠕虫捕食分支中的一个物种,它在系统发育上与捕食鱼的锥螺专家密切相关。在捕虫的锥螺的毒液中发现了一种能有效作用于脊椎动物钠离子通道的d-conotoxin,这表明一种密切相关的祖先毒素能够从捕虫过渡到捕鱼,因为delta-conotoxin在捕鱼者中高度保守,对其捕获猎物的机制至关重要;这个肽,delta-conotoxin TsVIA,与这些来自食鱼的锥蜗牛毒液的d-conotoxin具有惊人的序列相似性。对游离背根神经节(DRG)神经元的钙显像研究揭示了该肽可能的分子靶点(电压栅钠通道)和作用机制(抑制通道失活)。电生理学证实了这一结果。这项工作证明了如何阐明来自系统发育明确的谱系的毒素和受体之间的特定相互作用可以揭示重要进化转变背后的分子机制。
Prey shifts in carnivorous predators are events that can initiate the accelerated generation of new biodiversity. However, it is seldom possible to reconstruct how the change in prey preference occurred. Here we describe an evolutionary "smoking gun" that illuminates the transition from worm hunting to fish hunting among marine cone snails, resulting in the adaptive radiation of fish-hunting lineages comprising similar to 100 piscivorous Conus species. This smoking gun is delta-conotoxin TsVIA, a peptide from the venom of Conus tessulatus that delays inactivation of vertebrate voltage-gated sodium channels. C. tessulatus is a species in a worm-hunting clade, which is phylogenetically closely related to the fish-hunting cone snail specialists. The discovery of a d-conotoxin that potently acts on vertebrate sodium channels in the venom of a worm-hunting cone snail suggests that a closely related ancestral toxin enabled the transition from worm hunting to fish hunting, as delta-conotoxins are highly conserved among fish hunters and critical to their mechanism of prey capture; this peptide, delta-conotoxin TsVIA, has striking sequence similarity to these d-conotoxins from piscivorous cone snail venoms. Calcium-imaging studies on dissociated dorsal root ganglion (DRG) neurons revealed the peptide's putative molecular target (voltagegated sodium channels) and mechanism of action (inhibition of channel inactivation). The results were confirmed by electrophysiology. This work demonstrates how elucidating the specific interactions between toxins and receptors from phylogenetically well-defined lineages can uncover molecular mechanisms that underlie significant evolutionary transitions.