Sensing deep extreme environments: the receptor cell types, brain centers, and multi-layer neural packaging of hydrothermal vent endemic worms

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• 作者：Shuichi Shigeno (1)
  Atsushi Ogura (2)
  Tsukasa Mori (3)
  Haruhiko Toyohara (4)
  Takao Yoshida (1)
  Shinji Tsuchida (1)
  Katsunori Fujikura (1)
  
  1. Department for Marine Biodiversity Research ; Japan Agency for Marine-Earth Science and Technology ; 2-15 Natsushima-cho ; Yokosuka ; 237-0061 ; Kanagawa ; Japan
  2. Nagahama Institute of Bio-Science and Technology ; Institute of Bio-Science and Technology ; 1266 Tamura-Cho ; Nagahama ; 526-0829 ; Shiga ; Japan
  3. Nihon University ; 1866 Kameino ; Fujisawa ; 252-0880 ; Kanagawa ; Japan
  4. Division of Applied Biosciences ; Kyoto University ; Graduate School of Agriculture ; Laboratory of Marine Biological Function ; Kitashirakawa Oiwake-cho ; Sakyo-ku ; Kyoto ; 606-8602 ; Japan
  
• 关键词：Deep ; sea ; Sensory cells ; Brain ; Nervous system ; Glia ; Annelids ; Evolution
• 刊名：Frontiers in Zoology
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：11
• 期：1
• 全文大小：14,869 KB
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• 刊物主题：Zoology;
• 出版者：BioMed Central
• ISSN：1742-9994

文摘

Introduction Deep-sea alvinellid worm species endemic to hydrothermal vents, such as Alvinella and Paralvinella, are considered to be among the most thermotolerant animals known with their adaptability to toxic heavy metals, and tolerance of highly reductive and oxidative stressful environments. Despite the number of recent studies focused on their overall transcriptomic, proteomic, and metabolic stabilities, little is known regarding their sensory receptor cells and electrically active neuro-processing centers, and how these can tolerate and function in such harsh conditions. Results We examined the extra- and intracellular organizations of the epidermal ciliated sensory cells and their higher centers in the central nervous system through immunocytochemical, ultrastructural, and neurotracing analyses. We observed that these cells were rich in mitochondria and possessed many electron-dense granules, and identified specialized glial cells and serial myelin-like repeats in the head sensory systems of Paralvinella hessleri. Additionally, we identified the major epidermal sensory pathways, in which a pair of distinct mushroom bodies-like or small interneuron clusters was observed. These sensory learning and memory systems are commonly found in insects and annelids, but the alvinellid inputs are unlikely derived from the sensory ciliary cells of the dorsal head regions. Conclusions Our evidence provides insight into the cellular and system-wide adaptive structure used to sense, process, and combat the deep-sea hydrothermal vent environment. The alvinellid sensory cells exhibit characteristics of annelid ciliary types, and among the most unique features were the head sensory inputs and structure of the neural cell bodies of the brain, which were surrounded by multiple membranes. We speculated that such enhanced protection is required for the production of normal electrical signals, and to avoid the breakdown of the membrane surrounding metabolically fragile neurons from oxidative stress. Such pivotal acquisition is not broadly found in the all body parts, suggesting the head sensory inputs are specific, and these heterogenetic protection mechanisms may be present in alvinellid worms.