Sensing deep extreme environments: the receptor cell types, brain centers, and multi-layer neural packaging of hydrothermal vent endemic worms
© Shigeno et al.; licensee BioMed Central Ltd. 2014
Received: 23 July 2014
Accepted: 23 October 2014
Published: 18 November 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.
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 ,. 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 ,. The emblematic characteristic of these alvinellids is thus their exceptional tolerance to high temperatures and the toxicity of acidic and reducing fluids -. Indeed, the alvinellid thermostabilization, detoxification, and anti-oxidative stress capacities have been attributed to a number of biochemical, physiological, and structural properties ,-, supported by deep sequencing analysis of the transcriptomic and proteomic level stability -.
Despite these extensive studies, little attention has been given to the sensory and nervous systems, particularly their behavioral ecology. Studies of sensory systems of animals endemic to hydrothermal vents are important for two main reasons. First, the sensory ecology of vent-endemic species is largely unknown, with the exception of some classic pioneering work on alvinellid larval settling , and crustacean vision and olfaction (e.g., -). Second, 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., ); therefore, the sensory receptors and neural tissues may possess specific tolerance mechanisms.
Classic anatomical studies have revealed that the overall body, tissue, and cellular organization of Alvinella pompejana exhibits a typical polychaete ground plan, without visual and gravity sense organs . The sensory receptor cells identified on the branchial crown and feeding appendages are ciliate cells, mitochondria-rich, and of the bipolar type with single long axon, often associated with supportive cells ,. Thus far the nuchal organs, usually a paired epidermal ciliary structure in most polychaetes , have not been found in the prostomium of alvinellids. The structure of the central nervous system has been extensively studied in polychaetes and other annelid taxa -, including a few chemosynthetic siboglinid species -; however, the ultrastructural organization of the brain and nerves, as well as regional specialization, including inter- and intra-lobe connective patterns, is largely unknown in the deepsea annelids, including terebelliform alvinellids.
Since the first discovery of alvinellids on the East Pacific Rise , 11 species have been described in the order Terebellida and family Alvinellidae, which comprises two genera, Alvinella and Paralvinella . Among the alvinellid species, we examined Paralvinella hessleri, which is abundant in the hydrothermal communities of active chimneys. These chimneys can be easily accessed with remotely operated vehicles in the fields of the Izu-Ogasawara Arc or the Okinawa Trough of Japan. Compared to the well-studied A. pompejana, P. hessleri is smaller in size (total 10 mm or less), thus more individuals can be maintained in restricted laboratory space, and examined with whole-mount, three-dimensional (3D) analysis without dissection. In this study, 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 (,; see also ; Shigeno et al., unpublished). Using this species, we sought to provide the first comprehensive maps of the distribution of ciliated sensory cells, neural projections in the higher brain centers, and newly identified cellular components, to explain mechanisms for tolerating the hydrothermal vent environment.
Alvinellid body plans
Classification of the sensory and motor ciliated cell types of Paralvinella hessleri
Projections in CNS
Specific characters ciliary length/width
chemical sensory cells
penetrative sensory cells
VNC, each segment
chemical sensory cells 1-12/0.3μm
forming lines on the dorsal head 4-13/0.2μm
neck ciliary bands?
round and short cilia 1-3/0.2μm
penetrative sensory cells
ventral area of notopods
roughly lined with pods 1-21/0.1-0.2μm(sharp)
lateral branch and whole bodies
typical motor cilia 1-12/0.2μm
motor ciliary cells
Ventral patch type
ventrally localized 1-11/0.2μm
sensory receptor cells?
The sensory receptor cell types
The sensilla type (Figure 3 G-I): These cells are ciliate sensory cells with a short distal process, also known as typical bipolar receptor cells . Three to five cilia penetrate the cuticle, and the sensory cells send long axons directly to the central nervous system. This cell type is broadly distributed on the head, branches, buccal tentacles, and the trunk. The three (the short, intermediate, and long) ciliary subtypes were detected. The short and intermediate types seem to be developing cell, but here we distinguished as a sensilla type due to their shapes, ciliary numbers, and thickness of cilia.
The line type (Figure 3 J): These are penetrative multiciliate cells, and the cilia and cell bodies exhibit bilateral longitudinal lines running inside of the dorsal grooves extending from the head end. The ciliary cells are superficially lined, but more detailed analysis identified subtle repeated gaps among these cells. The cilia are generally long and similar in length (10–12 μm).
The tuft type (Figure 3 K): The cells are multiciliate penetrative type, namely the cilia penetrate the cuticle. The ciliary shape is round and tuft-like. One major subtype is distributed only in the dorsal, lateral, but not in the ventral side of the head. The cilia are short and densely packed compared with those of the patch ciliary type. In contrast to the branch surfaces, many pores and granules are found in the epidermis of the head part (Figure 3F).
The bud type (Figure 3 L-N): These penetrative multiciliate cells are situated in their characteristic positions on the head and trunk. As in polychaetes, the bud may correspond to the papilla ,. The cilia are sharp and roughly arranged in a short line.
The patch type (Figure 3 O): This multiciliate cell type may have motor functions for producing directed water flow or removing waste matter from the body surface, but chemical or mechanical sensation also may be possible. The axonal projection is lacking and cells are tightly connected to the epidermal cells by the gap junction (not shown). These cells are most dense on the lateral sides of each branch, and are broadly distributed over the entire body. The cilia are not sharp as in the bud type and usually exhibiting loop-like form as a possible artifact (Figure 3O).
The ventral patch type at the trunk (Figure 2 B): The ciliary structure is almost identical to the patch ciliary type, with ciliary density and length as stated above. Yet the distribution of cells displays a stereotypic linear pattern, and repeated positions are only observed in the ventral and ventro-lateral sides of the trunk (see the trunk part).
The sensory cells were detected using at least three independent methods: scanning electron microscopy (SEM), transmission electron microscopy (TEM), and light microscopy using labeling for acetylated alpha-tubulin, a widely used cytoskeleton marker for cilia and neural axons (shown later). Phalloidin fluorescent staining was also helpful for detecting F-type actin in the ciliary cells and neurons in differential contrast to the tubulin labeling (not shown).
The myelin-like glial repeats in the head sensory neurons
The mushroom body-like higher brain centers
The mushroom bodies traditionally called corpora pedunculata have been extensively studied as higher chemosensory learning centers in arthropods and annelids ,. In P. hessleri, we found a candidate pair of mushroom body cell clusters in the typical position in the dorso-lateral sides of the brain (Figure 8A), which receive inputs from sensory cells in the dorsal head regions (see Figure 7C). The ultrastructural studies revealed that the small interneurons of the mushroom bodies are histologically distinct compared with the surrounding intermediate-size interneurons (Figure 8B). In the small interneurons, there are a few mitochondria and more than 40 to 80 electronically dense particles (ca. smaller than 100 nm in diameter) in a single ultrathin section (Figure 8C). More characteristically, we found a unique support system for the neural cell bodies covered with glial cells (Figure 8D), and granular-rich axonal bundles in the mushroom body region (Figure 8E), although such glial membranes were not widespread in the neuropils (Figure 8F, G). The spatial distribution of the glial cell bodies could not be precisely determined due to their complexity, but most of neuronal cell bodies are tightly covered with thick membrane comprised of two to three layered glial membranes (Figure 8H). Characteristic fine dense granules are also distributed in some axons and cell bodies (Figure 8E), and may be neurosecretory cells (as described in the brain of other polychaetes ,), but larger granules of a different type are also seen (Figure 8I).
The sensory systems of the head branchial crown and buccal tentacles
The branchial crown
Most of the sensory cells are the primary sensilla type (summarized in Table 1). In each branchial leaflet, there are numerous patch type cells along the lateral sides, and broadly distributed sensilla types (see Figure 3A). Whole-mount immunocytochemistry identifies the ciliary position as well as the axonal origins in the branches (Figure 9D, E; Additional file 3: Movie S3). Notably, we failed to detect the multilayer glial membranes that were found in the head axons in any branchial sensory cells (data not shown).
The buccal tentacles
The tubulin immunochemistry distinguished the ciliary sensory cell types, and showed that most of the sensory cells are sensilla and patch type cells (Figure 9F, G). As in the case of the branchial crown, the multilayer glial membranes surrounding the axons are not distinguished, as described in previous studies .
The trunk nervous system
Unique biological systems are often expected to be discovered in animals living in unusual environmental conditions. In order to contribute to the discussion of the sensory and neural systems animals from hydrothermal vent environments, we studied the cellular, intracellular, and histological structure in Paralvinella hessleri, a member of the vent-endemic alvinellids, using electron microscopy, immunohistochemistry, and neurotracing in combination with laser confocal microscopy.
The sensory receptor cell types
The glial membrane supporters
The types of glial systems identified in P. hessleri have not been described in any animals, except for a scale-worm also endemic to hydrothermal vents (Shigeno et al., submitted). The neural cells of many animals are more or less protected by glia, and the specialized myelinating glia for the long axons are found in many vertebrates, crustaceans, and annelids . In the case of well-studied earthworms, the median and lateral giant axons of the ventral nerve cords are encompassed by concentrically wrapped lamellar sheets of insulating plasma membrane . In this study, the glial system found in the alvinellid worms is considerably different. First, the myelin structure is present in the head sensory input systems and not found in the ventral nerve cords. Second, in addition to the axonal bundles, the cell bodies of the brain themselves are covered with multilamellar sheets.
The glial cells in vertebrates and some invertebrates serve diverse functions, including as a nutrition source, and for immunity, peptide signaling, neural development, as a resistor in fine electronic signal modifiers. They also provide protection by filtering or blocking toxic substances, including oxidative stressors and heavy metals, through maintenance of the chemical environment used to conduct electrical impulses -. If the cells are myelinating, the conduction speed of electrical impulses increases, thus providing an adaptive advantage for rapid behavioral responses to stimuli from alarm cues . In the environment of hydrothermal vent fields, it is likely that specific glial protectors are required, since the environment is rich in heavy metals, hydrogen sulfide, and other toxic chemicals and metabolites produced by high temperature and pressure.
In addition, moderately hypoxic conditions are ubiquitous close to the vent field; therefore, some mechanism of protection is required to prevent the breakdown of glial membranes. This breakdown leads to irreversible cell death due to the production of reactive oxygen substances via hypoxia, which is well-studied in mammalian brains affected by ischemic stroke and integrity loss of the blood–brain barrier -. The actual functions of glial cells in alvinellids remain largely speculative, and it is not known how many glial cell types are present in these worms; however, our findings provide the first evidence for the role of such specialized glial systems in the hydrothermal endemic animals. Our findings also showed that not all of the sensory and neural cells are covered with multi-glial membranes, perhaps due to the presence of an alternative protector, such as the thick, non-pored collagenous walls in the epithelium of branches (summarized in Figure 11). This discovery suggests that unexpected biochemical heterogeneity and protection mechanisms may be present in the internal body spaces of these worms.
Specialization of the central nervous system
The mushroom body-like structure
One of the most distinguished areas in the polychaete brains is the corpora pedunculata, also known as mushroom bodies, a pair of neuropils with associated small somata called globuli cells. These may function in the chemosensory learning and memory centers found in many polychaetes ,, but are reduced  or not developed in sessile species, including the calcareous tubeworm Serpula . However, this does not mean that all sessile species lack mushroom bodies and globuli cells. In this study, we observed a pair of interneuron clusters in the anterolateral sides of the brain, indicating that these clusters might be positionally and functionally compared to the annelid mushroom bodies as homologous structures for the higher-order processing centers . Alternatively, higher-order neurons are often developed as distinct interneurons for a type of chemosensory system such as in the brains of aplacophoran molluscs ,. This indicates that the interneuron pools of alvinellids may have developed independently to act as specialized sensory receptors unique to hydrothermal vents.
One could assume that the highly developed branchial crown functions as a sensory organ due to the direct exposure of the bacteria-covered tubes to hot vent fluids. In this study, most sensory cells in the branches were of the ciliate type, and long axons extend into the subesophageal mass or the ventral nerve cords where there were no clearly identifiable lobes or neuropil compartments. Additionally, the buccal tentacles may possibly be used for the bacterial feeding (Shigeno, unpublished data), and have two sensory ciliated cell types and specific neuropil compartments that were not observed in the brain. If specialization of the neuropil compartments of chemosensory or gustatory centers are related to their chemical receptor diversity, as in the case of the glomeruli centers in annelid brains , we may expect that the sensing capacity of the branchial crown and buccal tentacles of the alvinellid worms is less specialized, and chemicals detected are not processed as environmental information. Whether or not the chemical receptors of alvinellids are specialized remains to be determined, and continued molecular studies of ionotropic, gustatory, and olfactory receptors are needed to better understand the chemosensory systems of animals endemic to hydrothermal vents.
Comparative evolutionary frameworks
As in free-living marine ragworms and sessile calcareous tubeworms, the sensory information collected by alvinellid sensory cells is processed by the mushroom bodies or comparable higher-order sensory centers, or the brain centers or the ventral nerve cords, as illustrated in Figure 11. This scheme for the sensory input and output signaling emphasizes the specific characteristics of alvinellid sensory processing systems.
First, the axonal projections of the line type sensory cells or the nuchal organ of P. hessleri extend directly into the subesophageal ganglia. This situation is dissimilar to that of the calcareous tubeworm Serpula, where the nuchal pathways extend into the brain (Figure 11; ). Additionally, the nuchal organ related centers of alvinellids are less specialized than those of the bloodworm Glycera rouxii, which has distinct centers known as annexed ganglia and associated giant cells , suggesting that the alvinellid cilliary cells might have a simple receptor capacity. Second, the signals from the branchial crown of P. hessleri are processed only in the subesophageal ganglia, whereas the sensory cells of the branchial crown in calcareous tubeworms project into both the brain and subesophageal ganglia . Third, the mushroom bodies are composed of small interneurons and as in the ragworms, are located at the antero-dorsal sides of the brain ; however, the alvinellid mushroom bodies receive inputs from the broadly distributed single sensory cell types of the head (see Figure 11). In addition, the alvinellid sensory inputs to the brain through the mushroom bodies are similar to those of free-living ragworms in the genus Neanthes . We therefore propose that the input systems from the eyes, antenna, cirrus, and pulps of the ragworms, which are not developed in the alvinellid head parts, could be compared to those of the type 1 and type 2 sensory cells. We further suggest that alvinellids utilize two distinct sub-systems for sensory signaling: (1) the brain, which serves as a primary sensory processing system, and (2) several “short-cut” pathways from the head and branchial sensory cells to the subesophageal and ventral nerve cords, presumably for the simple and rapid transduction of environmental sensory signals to the trunk motor control networks or any adaptive organs, which regulate homeostasis through the endocrine and circulatory systems in the trunk region.
Materials and methods
More than three hundred individuals of adults or juveniles of alvinellids, Paralvinella hessleri , Polychaeta, Sedentaria, and Alvinellidae, were collected aboard the research vessel “Natsushima” during research cruise NT12-10 (31°53.049′ N, 139°58.104′ E, 907 m depth, off Myojin-sho submarine caldera, onboard ID 1374–9; or 32°06.214′ N, 139°52.05′ E, 1294 m depth, off Myojin Knoll, onboard ID 1377–4), in the Izu-Ogasawara Arc, Japan. Samples were collected on the 25th or 29th of April 2012 with Hyper-Dolphin 3000 remotely operated vehicles (HPD#1374 or #1377). Worms were collected using a suction sampler from the surface of the white microbial mat with worm’s nests attached to the chimney walls. The individuals used in this study were fresh and active animals, which were selected by eye for collection. Following the ROV field surveys, the live animals were maintained in non-aerated cold deep-sea water collected in the same canisters, and specimens were stored at 4–8°C for a few days.
Histology and immunocytochemistry
The specimens were fixed on board with 4% paraformaldehyde in phosphate buffered saline (PBS); alternatively, the suction sampler and canister were filled with deep-sea water (4°C) for 12 hours, then were washed in PBS, and transferred to 80% methanol or ethanol for long term storage at –30°C or –80°C. Immunostaining of the whole-mounts followed a standard protocol (n >30). The whole-mounts were treated with Proteinase K (5 μg/ml in PBS) for 5 min at 37°C. A mouse monoclonal anti-acetylated alpha-tubulin antibody (6-11B-1 clone) isolated following immunization with sea urchin flagella proteins (acTUBA, Sigma Chemical, T6793, 1:3000) in PBST (PBS with 1% Tween 20 and 1% BSA), or rabbit polyclonal anti-serotonin (5-hydroxytryptamine, 5-HT, 1:500) antibody (Sigma, S5545, 1:500) was used to detect 5-HT positive selected neurons. These primary antibodies have been widely employed in invertebrate neuroanatomy (e.g., ). A CF™ 488A goat anti-mouse IgG or CF™ 594 goat anti-rabbit IgG antibody (Biotium Incorporated, 1:400) was used as a secondary antibody. DAPI (4′-6-Diamidino-2-phenylindole; Sigma, 0.1μg/ml), SYTO®13, a green-fluorescent nucleic acid stain dye (Invitrogen, 1:5000), and rhodamine-conjugated Concanavalin A (ConA, Vector Laboratories, 1:1000) and CF™ 594 phalloidin (Cytoskeleton Incorporated, 1:600) were used for counterstaining of the nuclei, the cell membrane, or F-actin rich muscle fibers, respectively. Samples were examined using confocal laser scanning microscopy as described below. Some paraformaldehyde fixed samples were embedded in paraffin and cut with a rotatory microtome to a 5–10 μm thickness. These sections were stained in Mayer’s hematoxylin and eosin solution.
Electron microscopy ultrastructural analysis
The electron microscopy analyses were conducted according to previously described methods , with some modifications. The whole-mount or dissected specimens (n >10) were fixed in a solution of 2.5% glutaraldehyde in cold deep-sea water for at least one week. After extensive washes with 0.22 mm-filtered seawater, samples were postfixed with 2% osmium tetroxide in filtered seawater for two hours at 4°C. For field-emission scanning microscopy (FE-SEM), samples were stained with 1% aqueous tannic acid (pH 6.8) for one hour and treated with 1% aqueous osmium tetroxide for one hour at 4°C. Samples were dehydrated in a graded ethanol series, critical point-dried (JCPD-5; JEOL Ltd., Tokyo, Japan), coated using an osmium plasma coater (POC-3; Meiwa Shoji Co., Osaka, Japan), and observed under an FE-SEM (JSM-6700F; JEOL Ltd., Tokyo, Japan). For transmission electron microscopy (TEM), the postfixed animals were rinsed with distilled water, and stained with 1% aqueous uranyl acetate for two hours at 4°C. The samples were then rinsed, dehydrated, and embedded in Epon 812 resin (TAAB, Aldermaston, UK). Ultrathin sections were obtained with an ultramicrotome (thickness 60nm; Reichert Ultracut S; Leica, Wetzlar, Germany), and the sections were double stained with uranyl acetate and lead citrate for observation under the TEM (Tecnai 20; FEI company, Tokyo, Japan) operated at 120 kV. The photos were taken with resolution 2048 – 2115 pixel.
The lipophilic dye tracers NeuroVue® maroon or red (Polysciences Incorporated, Warrington, PA, USA) were used for neuronal tract tracing according to the manufacturer’s protocol, with some modifications. The dyes transfer into plasma membranes in formaldehyde fixed tissues and diffuses laterally within the membrane, finally labeling the cell bodies, axons, and allowing visualization of neuronal processes. More than twenty worms were fixed in 4% paraformaldehyde in cold deep-sea water overnight, and washed in PBS without any polysorbate detergents and alcohol. The fine pieces of coated dye filters were directly applied to the head part with the fine tips of capillary tubes, and they were stored in 0.1% paraformaldehyde in PBS, and at 37°C for one to three weeks. The dye tracers transferred into the epidermal tissues and diffused in the neuronal membranes, allowing visualization of the selected or accidentally labeled cell bodies and long axonal arborization. ConA and Alexa Fluor® 350 or 594 were used as a versatile lectin probe for the membrane counterstaining to illuminate dye-traced cells. The whole-mount samples were stained with other dyes and viewed using confocal microscopy as described below.
Samples were examined as whole-mounts or sections using the confocal laser scanning microscope Fluoview, FV500 ver4.3c (Olympus, Lake Success, NY, USA) with the fluorescent microscope IX-71 automated inverted microscope platform (Olympus). Laser power was employed with UV, Argon, and HeNe, and the appropriate filter set was selected according to the fluorescent markers. The pseudo-colors were used to enhance the structural images according to the manufacturer’s protocol. Additional processing of images for contrast, brightness, and color balance was performed as needed with Adobe Photoshop CS5 (Adobe Systems Incorporated, San Jose, CA, USA). Schematic diagrams were created with Adobe Illustrator CS5 (Adobe Systems Incorporated).
The terms used for the alvinellid sensory cells and nervous systems are based on the definitions given by previous studies ,,, unless otherwise specified. Richter et al.  was also used as a nomenclatural reference for invertebrate neuroanatomical terms. Desbruyeres et al.  was used for alvinellid anatomical terms.
SS designed the study, conducted the experimental studies, and wrote the manuscript draft. TY, SM, HT, and ST contributed substantially to the collection of deep-sea animal samples on board, and helped write the manuscript. TM, AO, and KF contributed to the data interpretation and to writing the manuscript. All authors read and approved the final manuscript.
The authors would like to thank the captain and crew of R/V “Natsushima” and the operation teams of the ROV “Hyper Dolphin 3000”. We are grateful to research scientists on board during cruise NT12-10 for their kind assistance in obtaining the study materials. We particularly thank Koji Inoue, Masatomi Hosoi, Retori Hiraoka, and the Chief Scientist of this cruise, Motohiro Shimanaga. For the electron microscopy studies, we thank Katsuyuki Uematsu and Akihiro Tame. We also thank an anonymous reviewer for reading the manuscript and providing critical comments. Grant sponsor: Japanese Society for the Promotion of Science (No. 90360560) and Japan Agency for Marine-Earth Science and Technology Internal Research & Development Award to SS.
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