Intracellular sequestration requires specialized cellular and molecular mechanisms allowing a predator to retain and use specific organelles that once belonged to its prey. Little is known about how common cellular mechanisms, like phagocytosis, can be modified to selectively internalize and store foreign structures. One form of defensive sequestration involves animals that sequester stinging organelles (nematocysts) from their cnidarian prey. While it has been hypothesized that nematocysts are identified by specialized phagocytic cells for internalization and storage, little is known about the cellular and developmental mechanisms of this process in any metazoan lineage. This knowledge gap is mainly due to a lack of genetically tractable model systems among predators and their cnidarian prey. Here, we introduce the nudibranch Berghia stephanieae as a model system to investigate the cell, developmental, and physiological features of nematocyst sequestration selectivity. We first show that B. stephanieae, which feeds on Exaiptasia diaphana, selectively sequesters nematocysts over other E. diaphana tissues found in their digestive gland. Using confocal microscopy, we document that nematocyst sequestration begins shortly after feeding and prior to the formation of the appendages (cerata) where the organ responsible for sequestration (the cnidosac) resides in adults. This finding is inconsistent with previous studies that place the formation of the cnidosac after cerata emerge. Our results also show, via live imaging assays, that both nematocysts and dinoflagellates can enter the nascent cnidosac structure. This result indicates that selectivity for nematocysts occurs inside the cnidosac in B. stephanieae, likely in the cnidophage cells themselves. Our work highlights the utility of B. stephanieae for future research, because: (1) this species can be cultured in the laboratory, which provides access to all developmental stages, and (2) the transparency of early juveniles makes imaging techniques (and therefore cell and molecular assays) feasible. Our results pave the way for future studies using live imaging and targeted gene editing to identify the molecular mechanisms involved in nematocyst sequestration. Further studies of nematocyst sequestration in B. stephanieae will also allow us to investigate how common cellular mechanisms like phagocytosis can be modified to selectively internalize and store foreign structures.

中文翻译：

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裸鳃亚目贝吉亚的刺胞在发育过程中的移动和储存 (Valdés, 2005)

细胞内隔离需要专门的细胞和分子机制，使捕食者能够保留和使用曾经属于其猎物的特定细胞器。关于如何修改常见的细胞机制（如吞噬作用）以选择性地内化和储存外来结构，我们知之甚少。一种形式的防御性隔离涉及从刺胞动物猎物隔离刺痛细胞器（线虫囊）的动物。虽然已经假设刺丝囊被专门的吞噬细胞识别用于内化和储存，但对于任何后生动物谱系中这一过程的细胞和发育机制知之甚少。这种知识差距主要是由于捕食者及其刺胞动物猎物缺乏遗传易处理的模型系统。这里，我们介绍了裸鳃亚目Berghia stephanieae 作为模型系统来研究刺丝囊隔离选择性的细胞、发育和生理特征。我们首先表明以 Exaiptasia diaphana 为食的 B. stephanieae 选择性地隔离线虫囊，而不是在其消化腺中发现的其他 E. diaphana 组织。使用共聚焦显微镜，我们记录了线虫囊隔离在喂食后不久开始，并且在负责隔离的器官（刺胞囊）位于成人的附属物（cerata）形成之前开始。这一发现与之前的研究不一致，这些研究将刺胞动物的形成置于角虫出现后。我们的研究结果还表明，通过实时成像分析，线虫囊和甲藻都可以进入新生的刺胞结构。该结果表明，刺丝囊的选择性发生在 B. stephanieae 的刺胞内，可能在刺胞体细胞本身中。我们的工作突出了 B. stephanieae 在未来研究中的效用，因为：（1）该物种可以在实验室中培养，从而可以进入所有发育阶段，（2）早期幼体的透明度使得成像技术（因此细胞和分子测定）是可行的。我们的结果为未来使用实时成像和靶向基因编辑来识别刺胞囊隔离所涉及的分子机制的研究铺平了道路。进一步研究 B. stephanieae 中的线虫囊隔离也将使我们能够研究如何修改吞噬作用等常见细胞机制以选择性内化和储存外来结构。