Abstract
IntroductionDeep-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.ResultsWe 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-014-0082-9) contains supplementary material, which is available to authorized users.
Highlights
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
The detailed physiology of P. hessleri, including mechanisms of thermotolerance, were not examined, but our preliminary experiments showed that the thermotolerance of these species is similar to those of A. pompejana and Paralvinella sulfincola from the North Pacific; P. hessleri prefers temperatures between 40-50°C, and endure temperatures as high as 55°C ([15,36]; see [16]; Shigeno et al, unpublished)
The central nervous system is composed of the supraesophageal mass or brain, subesophageal mass, and the segmented ventral nerve cords (Figure 2C)
Summary
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. The alvinellid worms are annelids that are generally found on microbial mats closely inhabiting the smokers extruding from the active chimneys of deep-sea hydrothermal vents [1,2] The fauna inhabiting these hot spring fields are exposed to highly fluctuating physico-chemical conditions, high levels of heavy metals, sulfide, and carbon dioxide, and harmful compounds such as hydrogen peroxide and hydroxyl radicals [3,4]. The alvinellid thermostabilization, detoxification, and anti-oxidative stress capacities have been attributed to a number of biochemical, physiological, and structural properties [4,9,10,11,12,13], supported by deep sequencing analysis of the transcriptomic and proteomic level stability [14,15,16] Despite these extensive studies, little attention has been given to the sensory and nervous systems, their behavioral ecology. The neural cells are expected to be highly sensitive to toxic and redox fluids, since the neuronal cells primarily carry out electronic and active chemical signal transduction via synapses (e.g., [22]); the sensory receptors and neural tissues may possess specific tolerance mechanisms
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