Sea Urchin Tube Feet Research Articles

Hyposalinity reduces coordination and adhesion of sea urchin tube feet.

Climate change will increase the frequency and intensity of low-salinity (hyposalinity) events in coastal marine habitats. Sea urchins are dominant herbivores in these habitats and are generally intolerant of salinity fluctuations. Their adhesive tube feet are essential for survival, effecting secure attachment and locomotion in high wave energy habitats, yet little is known about how hyposalinity impacts their function. We exposed green sea urchins (Strongylocentrotus droebachiensis) to salinities ranging from ambient (32‰) to severe (14‰) and assessed tube feet coordination (righting response, locomotion) and adhesion [disc tenacity (force per unit area)]. Righting response, locomotion and disc tenacity decreased in response to hyposalinity. Severe reductions in coordinated tube foot activities occurred at higher salinities than those that affected adhesion. The results of this study suggest moderate hyposalinities (24-28‰) have little effect on S. droebachiensis dislodgement risk and survival post-dislodgment, while severe hyposalinity (below 24‰) likely reduces movement and prevents recovery from dislodgment.

Plasticity in the purple sea urchin (Strongylocentrotus purpuratus): Tube feet regeneration and adhesive performance

Sea urchins are key members of hydrodynamically intense habitats, such as open coast intertidal and shallow reefs. Secure attachment to the substrata, by means of tube feet and spines, is essential for survival. Previous studies suggest that environmental variables (i.e. hydrodynamics, substrate) can influence the morphology and adhesive performance of tube feet. Catastrophic failure of tube feet occurs often due to strong hydrodynamic forces. The time and ability of amputated tube feet to return to pre-amputation adhesive performance, and the interaction with environmental factors are unknown. To assess the dynamics of adhesive performance and regeneration of tube feet, we 1) evaluated phenotypic plasticity of disc surface area of two urchin populations inhabiting sites with different lithologies (field - in-situ conditions) and, 2) assessed regeneration of their functionality (tube foot length, time of disc first appearance, disc surface area, and tenacity) after amputation (laboratory - ex-situ conditions). Results showed that in the field, tube feet are plastic in their phenotype: sea urchins from the two sites differed in their disc surface area. Plasticity was also observed in the laboratory, where urchins regenerate tube feet that are shorter in length and have smaller discs compared to pre-amputation measurements. Thus, sea urchin tube feet recovering from amputation events in the intertidal may differ in their initial morphology and in the recovery period after amputation. Moreover, tube feet that were never amputated also decreased their disc area, suggesting that plasticity occurs on tube feet of urchins maintained in laboratory conditions. In shallow temperate reef systems, urchins are ecosystem engineers that affect the abundance and distribution of many other organisms. The plastic nature of morphological and adhesive abilities of sea urchin tube feet influences their ability to survive and dominate wave-battered habitats.

Light-Dependent Electrical Activity in Sea Urchin Tube Feet Cells.

Sea urchins can detect and respond to light, and many species of sea urchins are negatively phototaxic. Light detection is hypothesized to occur via photoreceptors located on sea urchin tube feet, and opsins have been detected in tube feet, spines, and the test. However, the molecular mechanisms underlying light detection are, for the most part, unknown. Individual tube feet disc cells were isolated from purple sea urchins (Strongylocentrotus purpuratus), and the electrical responses of these cells to varying levels of illumination were quantified using the patch clamp technique. No currents were observed under bright illumination, whereas under dark conditions, large, slowly activating currents were consistently observed. Two types of cells were functionally identified based on their responses to darkness. Type I cells sustained currents indefinitely in the dark, whereas Type II cell currents spontaneously decayed after several seconds. The large currents observed were composed of the summation of many smaller events that were characterized by a rapid onset and an exponentially decaying component, which may be indicative of direct vesicular release from the tube feet disc cells in response to the dark conditions.

Effects of elevated carbon dioxide on contraction force and proteome composition of sea urchin tube feet

This study examined how contraction force and protein profiles of the tube feet of the sea urchin (Pseudocentrotus depressus) were affected when acclimated to 400 (control), 2000 and 10,000μatm CO2 for 48days. Acclimation to higher CO2 conditions significantly reduced contraction force of the tube feet. Two-dimensional gel electrophoresis showed that eight spots changed in protein volume: six up-regulated and two down-regulated. Using matrix-assisted laser desorption/ionization-quadrupole ion trap-time of flight mass spectrometry, three up-regulated spots (tubulin beta chain, tropomyosin fragment, and actin N-terminal fragment) and two down-regulated spots (actin C-terminal fragment and myosin light chain) were identified. One possible interpretation of the results is that elevated CO2 weakened contraction of the tube feet muscle through an alteration of proteome composition, mainly associated with post-translational processing/proteolysis of muscle-related proteins.

Mapping sea urchins tube feet proteome — A unique hydraulic mechano-sensory adhesive organ

Marine organisms secrete adhesives for substrate attachment that to be effective require functional assembly underwater and displacement of water, ions, and weakly bound polyions that are ubiquitous in seawater. Therefore, understanding the characteristics of these protein/carbohydrate-based marine adhesives is imperative to decipher marine adhesion and also, to accelerate the development of new biomimetic underwater adhesives and anti-fouling agents. The present study, aims at mapping the proteome of the sea urchin Paracentrotus lividus adhesive organs using a combination of complementary protein separation techniques (1-D-nanoLC and 2-DE), databases and search algorithms. This strategy resulted in the identification of 328 non-redundant proteins, constituting the first comprehensive list of sea urchin tube feet proteins. Given the known importance of phosphorylation and glycosylation in marine adhesion, the 2DE proteome was re-analyzed with specific fluorescent stains for these two PTMs, resulting in the identification of 69 non-redundant proteins. The obtained results demonstrate that tube feet are unique mechano-sensory adhesive organs and highlight putative adhesive proteins, that although requiring further confirmation, constitute a step forward in the quest to decipher sea urchins temporary adhesion.

<p><strong>Echinoderms don’t suck: evidence against the involvement of suction in tube foot attachment*</strong></p>

Suction has usually been regarded as the primary functional mean for attachment in sea star and sea urchin tube feet and this hypothesis has become widespread in the public knowledge. Yet, a few studies have suggested that adhesive secre­tions may also play a prominent role in tube foot attachment. Here we use a morphological and biomechanical approach to investigate the role of suction in asteroid and echinoid tube foot attachment. Microscopic observations of tube feet rapidly fixed while they were attached to a smooth substratum show that their distal surfaces are totally flat and lack a suction cavity. Detachment force and tenacity of a single tube foot appear to be independent of the pulling angle: i.e., the introduction of a shear component in the pulling force does not decrease attachment strength as would be expected for a sucker. Moreover, sea urchin tube feet attach as strongly to perforated surfaces, which preclude pressure reduction, as to their unperforated counterparts. Taken together, these results clearly show that echinoderm tube feet rely on adhesive secretions and not on suction.

Is the adhesive material secreted by sea urchin tube feet species‐specific?

Sea urchin adoral tube feet are highly specialized organs that have evolved to provide efficient attachment to the substratum. They consist of a disk and a stem that together form a functional unit. Tube foot disk tenacity (adhesive force per unit area) and stem mechanical properties (e.g., stiffness) vary between species but are apparently not correlated with sea urchin taxa or habitats. Moreover, ultrastructural studies of sea urchin disk epidermis pointed out differences in the internal organization of the adhesive secretory granules among species. This prompted us to look for interspecific variability in the composition of echinoid adhesive secretions, which could explain the observed variability in adhesive granule ultrastructure and disk tenacity. Antisera raised against the footprint material of Sphaerechinus granularis (S. granularis) were first used to locate the origin of adhesive footprint constituents in tube feet by taking advantage of the polyclonal character of the generated antibodies. Immunohistochemical assays showed that the antibodies specifically labeled the adhesive secretory cells of the disk epidermis in the tube feet of S. granularis. The antibodies were then used on tube foot histological sections from seven other sea urchin species to shed some light on the variability of their adhesive substances by looking for antibody cross-reactivity. Surprisingly, no labeling was observed in any of the species tested. These results indicate that unlike the adhesive secretions of asteroids, those of echinoids do not share common epitopes on their constituents and thus would be "species-specific." In sea urchins, variations in the composition of adhesive secretions could therefore explain interspecific differences in disk tenacity and in adhesive granule ultrastructure.

Unique system of photoreceptors in sea urchin tube feet

Different sea urchin species show a vast variety of responses to variations in light intensity; however, despite this behavioral evidence for photosensitivity, light sensing in these animals has remained an enigma. Genome information of the recently sequenced purple sea urchin (Strongylocentrotus purpuratus) allowed us to address this question from a previously unexplored molecular perspective by localizing expression of the rhabdomeric opsin Sp-opsin4 and Sp-pax6, two genes essential for photoreceptor function and development, respectively. Using a specifically designed antibody against Sp-Opsin4 and in situ hybridization for both genes, we detected expression in two distinct groups of photoreceptor cells (PRCs) located in the animal's numerous tube feet. Specific reactivity of the Sp-Opsin4 antibody with sea star optic cushions, which regulate phototaxis, suggests a similar visual function in sea urchins. Ultrastructural characterization of the sea urchin PRCs revealed them to be of a microvillar receptor type. Our data suggest that echinoderms, in contrast to chordates, deploy a microvillar, r-opsin-expressing PRC type for vision, a feature that has been so far documented only in protostome animals. Surprisingly, sea urchin PRCs lack any associated screening pigment. Indeed, one of the tube foot PRC clusters may account for directional vision by being shaded through the opaque calcite skeleton. The PRC axons connect to the animal internal nervous system, suggesting an integrative function beyond local short circuits. Because juveniles display no phototaxis until skeleton completion, we suggest a model in which the entire sea urchin, deploying its skeleton as PRC screening device, functions as a huge compound eye.

Sea urchin tube feet are photosensory organs that express a rhabdomeric-like opsin and PAX6

All echinoderms have unique hydraulic structures called tube feet, known for their roles in light sensitivity, respiration, chemoreception and locomotion. In the green sea urchin, the most distal portion of these tube feet contain five ossicles arranged as a light collector with its concave surface facing towards the ambient light. These ossicles are perforated and lined with pigment cells that express a PAX6 protein that is universally involved in the development of eyes and sensory organs in other bilaterians. Polymerase chain reaction (PCR)-based sequencing and real time quantitative PCR (qPCR) also demonstrate the presence and differential expression of a rhabdomeric-like opsin within these tube feet. Morphologically, nerves that could serve to transmit information to the test innervate the tube feet, and the differential expression of opsin transcripts in the tube feet is inversely, and significantly, related to the amount of light that tube feet are exposed to depending on their location on the test. The expression of these genes, the differential expression of opsin based on light exposure and the unique morphological features at the distal portion of the tube foot strongly support the hypothesis that in addition to previously identified functional roles of tube feet they are also photosensory organs that detect and respond to changes in the underwater light field.

Neural control of muscle relaxation in echinoderms.

Smooth muscle relaxation in vertebrates is regulated by a variety of neuronal signalling molecules, including neuropeptides and nitric oxide (NO). The physiology of muscle relaxation in echinoderms is of particular interest because these animals are evolutionarily more closely related to the vertebrates than to the majority of invertebrate phyla. However, whilst in vertebrates there is a clear structural and functional distinction between visceral smooth muscle and skeletal striated muscle, this does not apply to echinoderms, in which the majority of muscles, whether associated with the body wall skeleton and its appendages or with visceral organs, are made up of non-striated fibres. The mechanisms by which the nervous system controls muscle relaxation in echinoderms were, until recently, unknown. Using the cardiac stomach of the starfish Asterias rubens as a model, it has been established that the NO-cGMP signalling pathway mediates relaxation. NO also causes relaxation of sea urchin tube feet, and NO may therefore function as a 'universal' muscle relaxant in echinoderms. The first neuropeptides to be identified in echinoderms were two related peptides isolated from Asterias rubens known as SALMFamide-1 (S1) and SALMFamide-2 (S2). Both S1 and S2 cause relaxation of the starfish cardiac stomach, but with S2 being approximately ten times more potent than S1. SALMFamide neuropeptides have also been isolated from sea cucumbers, in which they cause relaxation of both gut and body wall muscle. Therefore, like NO, SALMFamides may also function as 'universal' muscle relaxants in echinoderms. The mechanisms by which SALMFamides cause relaxation of echinoderm muscle are not known, but several candidate signal transduction pathways are discussed here. The SALMFamides do not, however, appear to act by promoting release of NO, and muscle relaxation in echinoderms is therefore probably regulated by at least two neuronal signalling systems acting in parallel. Recently, other neuropeptides that influence muscle tone have been isolated from the sea cucumber Stichopus japonicus using body wall muscle as a bioassay, but at present SALMFamide peptides are the only ones that have been found to have a direct relaxing action on echinoderm muscle. One of the Stichopus japonicus peptides (holothurin 1), however, causes a reduction in the magnitude of electrically evoked muscle contraction in Stichopus japonicus and also causes 'softening' of the body wall dermis, a 'mutable connective tissue'. It seems most likely that this effect of holothurin 1 on body wall dermis is mediated by constituent muscle cells, and the concept of 'mutable connective tissue' in echinoderms may therefore need to be re-evaluated to incorporate the involvement of muscle, as proposed recently for the spine ligament in sea urchins.

Alterations in cholinergic signaling modulate contraction of isolated sea urchin tube feet: potential role of nitric oxide.

Alterations in cholinergic signaling modulate contraction of isolated sea urchin tube feet: potential role of nitric oxide.

Excitatory actions of GABA and of acetylcholine in sea urchin tube feet

1. 1. The musculature of isolated tube feet of several species of sea urchins was found to contract in response to GABA and to acetylcholine (ACh). The action of GABA but not that of ACh is blocked by bicuculline and picrotoxin. 2. 2. The action of GABA but not that of ACh requires the presence of Na +; it is reduced when the external Cl concentration is diminished. 3. 3. The following cholinomimetics were found to be effective: acetyl-β-methylcholine, carbamylcholine, butyrylcholine and nicotine. The contractile effect of these agents, but also that of GABA was prevented by the cholinolytics atropine, banthine, decamethonium, flaxedil, hexamethonium and mytolon. 4. 4. The action of ACh and of acetyl-β-methylcholine, but also that of GABA, was greatly enhanced by anticholinesterases (eserine, neostigmine). 5. 5. Both ACh and GABA were detected in tube foot extracts. ACh is specifically localized in those parts that contain nerve tissue, with concentrations up to 75 μg/g wet wt. 6. 6. It is concluded that GABA causes excitation of cholinergic motoneurones and does not affect the muscle fibers directly. The cholinoreceptors of the muscle fibers have both muscarinic and nicotinic properties.