Shigeno Shuichi, Ogura Atsushi, Mori Tsukasa, Toyohara Haruhiko, Yoshida Takao, Tsuchida Shinji, Fujikura Katsunori
Department for Marine Biodiversity Research, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, 237-0061, Kanagawa Japan.
Nagahama Institute of Bio-Science and Technology, Institute of Bio-Science and Technology, 1266 Tamura-Cho, Nagahama, 526-0829, Shiga Japan.
Front Zool. 2014 Nov 18;11(1):82. doi: 10.1186/s12983-014-0082-9. eCollection 2014.
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.
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.
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.
深海热液喷口特有的阿尔文虫科蠕虫物种，如阿尔文虫属和拟阿尔文虫属，被认为是已知最耐热的动物之一，它们能适应有毒重金属，并耐受高度还原和氧化应激环境。尽管最近有许多研究关注它们的整体转录组、蛋白质组和代谢稳定性，但对于它们的感觉受体细胞和电活性神经处理中心，以及这些细胞如何在如此恶劣的条件下耐受并发挥功能，人们了解甚少。
我们通过免疫细胞化学、超微结构和神经追踪分析，研究了表皮纤毛感觉细胞及其在中枢神经系统中的高级中枢的细胞外和细胞内组织结构。我们观察到这些细胞富含线粒体并拥有许多电子致密颗粒，并在赫氏拟阿尔文虫的头部感觉系统中鉴定出特化的神经胶质细胞和连续的髓鞘样重复结构。此外，我们确定了主要的表皮感觉通路，其中观察到一对不同的蘑菇体样或小中间神经元簇。这些感觉学习和记忆系统常见于昆虫和环节动物，但阿尔文虫科的输入不太可能来自头部背侧区域的感觉纤毛细胞。
我们的证据揭示了用于感知、处理和应对深海热液喷口环境的细胞和全系统适应性结构。阿尔文虫科的感觉细胞表现出环节动物纤毛类型的特征，其中最独特的特征是头部感觉输入和大脑神经细胞体的结构，它们被多层膜包围。我们推测，这种增强的保护对于产生正常的电信号以及避免代谢脆弱的神经元周围的膜因氧化应激而破裂是必需的。这种关键的特征并非在所有身体部位都广泛存在，这表明头部感觉输入是特定的，并且这些异源保护机制可能存在于阿尔文虫科蠕虫中。
