The heart of a dragon: 3D anatomical reconstruction of the 'scaly-foot gastropod' (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system.

The heart of a dragon: 3D anatomical reconstruction of the 'scaly-foot gastropod' (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system.
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DOI:
10.1186/s12983-015-0105-1
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发表时间:
2015
影响因子:
2.8
通讯作者:
Sigwart JD
Sigwart JD
中科院分区:
生物学2区
文献类型:
--
作者:
Chen C;Copley JT;Linse K;Rogers AD;Sigwart JD

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产于印度洋深海热液喷口生态系统的“鳞足腹足类”(ChrySomallon squamiferum Chen等,2015)是一种活跃的活动腹足类,生活在当地高密度环境中,其独特之处在于其脚部外表面覆盖着真皮鳞片。这些被硫化铁包裹的硅质岩,以及它对内共生细菌的营养依赖,都被认为是对硫化氢流动中极端环境的适应。通过解剖和内部解剖的3D断层重建,我们提出了“鳞足腹足类”适应极端环境生活的其他证据。我们对幼年和成年标本的解剖学研究表明,这种动物有一个巨大的无神经节神经系统,一个简单而简化的消化系统,而且这种动物是同时两性的。我们的研究表明,鳞叶金丝藻在幼虫后的整个生命周期中都依赖内共生细菌。特别令人感兴趣的是循环系统:叶甲鱼有一个非常大的线虫,由充满血腔的广泛血窦支撑。线虫为宿主提供氧气,但循环系统扩大,超出了其他类似的喷口腹足类的范围。在尾节的后方是一颗非常大且发育良好的心脏。根据耳廓和脑室的体积,心脏复合体约占身体体积的4%。这个比例巨大的心脏主要通过尾骨吸血,并供应高度血管化的食管腺。因此,我们推测,复杂的心血管系统很可能进化为在缺氧环境中氧化内共生体和/或向内共生体供应硫化氢。这项研究举例说明了如何通过对内部解剖学的详细研究来提高对生物体自体学的理解。这种腹足类是一种大型的活跃物种,在其热液喷口生态系统中非常丰富。然而,它的所有显著特征--保护性皮肤硬结、循环系统、高繁殖力--都可以被视为有利于其内共生微生物的适应。我们对这些结果的解释是,由于在极端的化学合成环境中解决能量需求的专业化,这种戏剧性的龙一样的物种已经成为其细菌的载体。本文的在线版本(doi:10.1186/s12983-0150105-1)包含补充材料,授权用户可以使用。
The ‘scaly-foot gastropod’ (Chrysomallon squamiferum Chen et al., 2015) from deep-sea hydrothermal vent ecosystems of the Indian Ocean is an active mobile gastropod occurring in locally high densities, and it is distinctive for the dermal scales covering the exterior surface of its foot. These iron-sulfide coated sclerites, and its nutritional dependence on endosymbiotic bacteria, are both noted as adaptations to the extreme environment in the flow of hydrogen sulfide. We present evidence for other adaptations of the ‘scaly-foot gastropod’ to life in an extreme environment, investigated through dissection and 3D tomographic reconstruction of the internal anatomy. Our anatomical investigations of juvenile and adult specimens reveal a large unganglionated nervous system, a simple and reduced digestive system, and that the animal is a simultaneous hermaphrodite. We show that Chrysomallon squamiferum relies on endosymbiotic bacteria throughout post-larval life. Of particular interest is the circulatory system: Chrysomallon has a very large ctenidium supported by extensive blood sinuses filled with haemocoel. The ctenidium provides oxygen for the host but the circulatory system is enlarged beyond the scope of other similar vent gastropods. At the posterior of the ctenidium is a remarkably large and well-developed heart. Based on the volume of the auricle and ventricle, the heart complex represents approximately 4 % of the body volume. This proportionally giant heart primarily sucks blood through the ctenidium and supplies the highly vascularised oesophageal gland. Thus we infer the elaborate cardiovascular system most likely evolved to oxygenate the endosymbionts in an oxygen poor environment and/or to supply hydrogen sulfide to the endosymbionts. This study exemplifies how understanding the autecology of an organism can be enhanced by detailed investigation of internal anatomy. This gastropod is a large and active species that is abundant in its hydrothermal vent field ecosystem. Yet all of its remarkable features—protective dermal sclerites, circulatory system, high fecundity—can be viewed as adaptations beneficial to its endosymbiont microbes. We interpret these results to show that, as a result of specialisation to resolve energetic needs in an extreme chemosynthetic environment, this dramatic dragon-like species has become a carrying vessel for its bacteria. The online version of this article (doi:10.1186/s12983-015-0105-1) contains supplementary material, which is available to authorized users.
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