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

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.

The role of the home environment in neurocognitive development of children living in extreme poverty and with frequent illnesses: a cross-sectional study

“…Studies have consistently demonstrated an association between SES and child physical health. Children living in poverty are at a higher risk of low birth weight ( Rouse et al , 2015), child mortality ( Shigeno et al ., 2014) and poor nutritional status ( Braissant et al ., 2015; Liu et al , 2015). These children consequently suffer poorer neurodevelopmental outcomes than those who are from wealthier families ( Kordas et al ., 2009).…”

The neuroanatomy of the siboglinid Riftia pachyptila highlights sedentarian annelid nervous system evolution

“…In the vestimentiferan Oasisia , the amp and SLN were also detected as P-medN and vCS , respectively (Fig 5a in [23]). Mushroom bodies are found in many errant and in some sedentary annelids such as the serpulid Serpula , the alvinellid Paralvinella hessleri , and sabellids, including Chone and Euchone species [49,64,80,83]. As in P .…”

“…As in P . hessleri [83] and E . papillosa [49], the mushroom-like structures in Riftia do not occupy the typical dorso-lateral position in the brain, but instead extend anteriorly.…”

“…Interestingly, the chemosynthetic P . hessleri exhibits theses structures, which potentially play a specific chemosensory role in the vent environment [83].…”

The complete mitochondrial genome of Paralvinella hessleri: an endemic species of deep-sea hydrothermal vent

“…Similar to the famous 'Pompeii worm' Alvinella pompeijna and the 'Sulfur worm' Paralvinilla sulfincola, P. hessleri also colonizes mid to high temperature hydrothermal vent. It is considered to be among the most thermotolerant metazoan (Shigeno et al 2014). However, the molecular information of the P. hessleri (as well as most other alvinellid worms) is still extremely rare.…”