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Aquacultivated sea cucumbers often suffer from SKin Ulceration Diseases (SKUDs). SKUDs have been observed in six holothuroid species from nine countries. All SKUDs present a similar symptom—the skin ulceration—and can be induced by bacteria, viruses, or abiotic factors. We here provide an update on SKUDs in holothuroids and analyse the case of the SKUD observed in Holothuria scabra in Madagascar. Field observations revealed a seasonality of the disease (i.e. wintertime maximum peak). Morphological analyses of integument ulcers showed that sea cucumbers react by forming a collagen fibre plug. Metagenomic analyses revealed a higher proportion of Vibrionaceae (Gammaproteobacteria) in ulcers in comparison to the healthy integument of the same individuals. Experimental infection assays were performed with ulcer crude extracts and bacteria isolated from these extracts (e.g. Vibrio parahaemolyticus ) but did not significantly induce skin ulceration. Our results suggest that the disease is not induced by a pathogen or, at the very least, that the pathogen is not found within the ulcers as the disease is not transmissible by contact. An initial cause of the SKUD in Madagascar might be the repeated and prolonged exposures to cold temperatures. Opportunistic bacteria could settle in the dermis of ulcerated individuals and promote the ulcer extension. We propose a general nomenclature for SKUDs based on the acronym of the disease, the affected sea cucumber species (e.g. Hs for Holothuria scabra ), the concerned region using an ISO code 3166-2 (e.g. MG for Madagascar), the description date (e.g. 20 for the year 2020), and, when known, the inducing agent (first letter of the general taxon, b for bacteria, v for virus in currently known cases; a a if it is an abiotic inducing parameter; nothing if the inducing cause has not been precisely identified). The disease described in this work will be designated under the name SKUD Hs-MG-20.

Due to the dearth of molecular markers variable enough to distinguish species of black corals, species delimitation in Antipatharia is still mainly based on morphological traits. One of the few markers available, the internal transcribed spacer (ITS) region located in ribosomal DNA, has already been used several times to infer phylogenetic relationships among antipatharians. However, this region was never considered in population-scale studies of shallow-water black corals till now. Here, we sampled two phenotypic variants of 41 specimens of the shallow-water antipatharian Stichopathes cf. maldivensis along the SW of Madagascar. The sampling area represents 200 km of shore and encompasses the runoffs of three rivers. We used direct sequencing to determine the main ITS1 types present in the genomes of the collected specimens and retrieved sequences from GenBank for Indonesian specimens. Then, we constructed a haploweb to visualize possible species boundaries using the criterion of mutual allelic exclusivity. With this method, we confirm that the previously described phenotypic variants belong to a single species that apparently extends from Indonesia to Madagascar. Likewise, the three rivers that pour freshwater in southwestern Madagascar do not appear to act as a barrier for the larval dispersal of this species. This study highlights the usefulness of ITS markers within antipatharians at both species and population levels.

Saponins are plant and marine animal specific metabolites that are commonly considered as molecular vectors for chemical defenses against unicellular and pluricellular organisms. Their toxicity is attributed to their membranolytic properties. Modifying the molecular structures of saponins by quantitative and selective chemical reactions is increasingly considered to tune the biological properties of these molecules (i) to prepare congeners with specific activities for biomedical applications and (ii) to afford experimental data related to their structure–activity relationship. In the present study, we focused on the sulfated saponins contained in the viscera of Holothuria scabra, a sea cucumber present in the Indian Ocean and abundantly consumed on the Asian food market. Using mass spectrometry, we first qualitatively and quantitatively assessed the saponin content within the viscera of H. scabra. We detected 26 sulfated saponins presenting 5 different elemental compositions. Microwave activation under alkaline conditions in aqueous solutions was developed and optimized to quantitatively and specifically induce the desulfation of the natural saponins, by a specific loss of H2SO4. By comparing the hemolytic activities of the natural and desulfated extracts, we clearly identified the sulfate function as highly responsible for the saponin toxicity.

Marine organisms have developed a high diversity of chemical defences in order to avoid predators and parasites. In sea cucumbers, saponins function as repellents and many species produce these cytotoxic secondary metabolites. Nonetheless, they are colonized by numerous symbiotic organisms amongst which the Harlequin crab, Lissocarcinus orbicularis , is one of the most familiar in the Indo-Pacific Ocean. We here identify for the first time the nature of the molecules secreted by sea cucumbers and attracting the symbionts: saponins are the kairomones recognized by the crabs and insuring the symbiosis. The success of this symbiosis would be due to the ability that crabs showed during evolution to bypass the sea cucumber chemical defences, their repellents becoming powerful attractants. This study therefore highlights the complexity of chemical communication in the marine environment.

Saponins are plant secondary metabolites. There are associated with defensive roles due to their cytotoxicity and are active against microorganisms. Saponins are frequently targeted to develop efficient drugs. Plant biomass containing saponins deserves sustained interest to develop high-added value applications. A key issue when considering the use of saponins for human healthcare is their toxicity that must be modulated before envisaging any biomedical application. This can only go through understanding the saponin-membrane interactions. Quinoa is abundantly consumed worldwide, but the quinoa husk is discarded due to its astringent taste associated with its saponin content. Here, we focus on the saponins of the quinoa husk extract (QE). We qualitatively and quantitively characterized the QE saponins using mass spectrometry. They are bidesmosidic molecules, with two oligosaccharidic chains appended on the aglycone with two different linkages; a glycosidic bond and an ester function. The latter can be hydrolyzed to prepare monodesmosidic molecules. The microwave-assisted hydrolysis reaction was optimized to produce monodesmosidic saponins. The membranolytic activity of the saponins was assayed based on their hemolytic activity that was shown to be drastically increased upon hydrolysis. In silico investigations confirmed that the monodesmosidic saponins interact preferentially with a model phospholipid bilayer, explaining the measured increased hemolytic activity.

Quinones are one of the major pigment groups that provide such bright colors to feather stars (Echinodermata, Crinoidea). These secondary metabolites also act as defensive molecules rendering crinoids unpalatable and repellent to other organisms. However, feather stars are usually associated with numerous symbiotic organisms, amongst which the ectocommensal snapping shrimp Synalpheus stimpsonii . We investigated the chemical stimulus allowing host selection in S. stimpsonii through the combination of behavioral tests, chemical extractions, and mass spectrometry analyses. The individuals of S. stimpsonii used in the experiments were sampled around the Great Reef of Toliara (Madagascar) where they are found in association with two crinoid species: Comanthus wahlbergii and Phanogenia distincta . The chemical attractiveness of the two crinoid hosts and a non-host species, Cenometra bella , was tested in an olfactometer. The three crinoids produced attractive kairomones allowing the snapping shrimp to recognize them. Mass spectrometry analyses on purified extracts of P. distincta revealed the presence of three different anthraquinones (rhodoptilometrin, comantherin, and a new crinoid anthraquinone). Compared to the existing literature, this anthraquinonic cocktail is specific to P. distincta . When these extracts were injected in the olfactometer, they triggered similar attracting behavior suggesting that crinoid anthraquinones are kairomones allowing host selection for S. stimpsonii . This hypothesis is also supported by the fact that shrimps were chemically attracted by pure commercial anthraquinones. In addition to their traditional defensive role (allomones), anthraquinones would, therefore, also function as kairomones, maintaining the symbiosis between S. stimpsonii and its crinoid hosts.

Sea cucumbers are marine deuterostomes possessing a complex innate immune system composed of a wide diversity of immune cells—coelomocytes—making them compelling models for exploring the evolution of immunity. This study investigates the functional specialisation of coelomocytes within the two main echinoderm body fluids, namely, the perivisceral fluid (PF) from the perivisceral cavity and the hydrovascular fluid (HF) from the hydrovascular–ambulacral system. Given their distribution restricted to the HF, haemocyte-like cells (HELs) are particularly investigated. In echinoderms, haemocytes have been described as reddish cells containing haemoglobin and thus presenting a function in oxygen transport. Using an integrative approach that combines cell morphological analyses, pigment profiling, and multi-omics technologies, we demonstrate in the sea cucumber Holothuria forskali that HELs harbour exceptionally high concentrations of carotenoids, primarily canthaxanthin and astaxanthin, potent antioxidant molecules responsible for their pigmentation. Transcriptomics and proteomics analyses reveal that HELs express candidate genes involved in the carotenoid metabolism pathway as well as catalase, an antioxidant enzyme. Additionally, spectral flow cytometry assays reveal that HELs do not produce reactive oxygen species (ROS) in contrast to most coelomocyte types, reinforcing the hypothesis of their antioxidant function. HELs also contribute to the formation of large red bodies (i.e., coelomocyte aggregates) and increase in concentration following lipopolysaccharide injections, indicating an active role in immunity. Given these results, we hypothesise that these cells act after the culmination of the immune response, forming an antioxidant shell around the cellular aggregates to mitigate oxidative stress from ROS produced while encapsulating pathogens, thus protecting the host tissues. The discovery of carotenoid-carrying coelomocytes constitutes the first report of pigmented coelomocytes in sea cucumbers (except respiratory pigments), challenging the long-standing assumption that these cells contain haemoglobin. Therefore, we propose renaming haemocytes into carotenocytes, at least in this species. However, we believe that this newly described coelomocyte type has been misidentified as haemoglobin-containing cells in many previous studies and may be present in many other holothuroid species. Our findings thus establish a new paradigm in the study of coelomocytes in echinoderms, as well as in the function of the hydrovascular system, which is unique to this phylum.

In marine environments, host selection, defining how symbiotic organisms recognize and interact with their hosts, is often mediated by olfactory communication. Although adult symbionts may select their hosts detecting chemosensory cues, no information is available concerning the recruitment of symbiotic larvae which is a crucial step to sustain symbioses over generations. This study investigates the olfactory recognition of seastar hosts by adult Zenopontonia soror shrimps and the recruitment of their larvae. We examine the semiochemicals that influence host selection using chemical extractions, behavioural experiments in olfactometers, and mass spectrometry analyses. After describing the symbiotic population and the embryonic development of shrimps, our results demonstrate that asterosaponins, which are traditionally considered as chemical defences in seastars, are species-specific and play a role in attracting the symbiotic shrimps. Adult shrimps were found to be attracted only by their original host species Culcita novaeguineae , while larvae were attracted by different species of seastars. This study provides the first chemical identification of an olfactory cue used by larvae of symbiotic organisms to locate their host for recruitment. These findings highlight the importance of chemical communication in the mediation of symbiotic associations, which has broader significant implications for understanding the ecological dynamics of marine ecosystems.

Intraspecific chemical communication between echinoderms has often been limited to prespawning aggregation. However, sea cucumber farmers have long observed year-round adult aggregation as a potential source of disease propagation and the suboptimal use of available sea pen acreage and food resources. In this study, through spatial distribution statistics, we demonstrated the significant aggregation of the aquacultivated sea cucumber Holothuria scabra both as adults in large sea-based pens and as juveniles in laboratory-based aquaria, proving that aggregation in these animals is not only observed during spawning. The role of chemical communication in aggregation was investigated using olfactory experimental assays. Our study established that the sediment that H. scabra feeds on as well as the water preconditioned by conspecifics induced positive chemotaxis in juvenile individuals. More specifically, through comparative mass spectrometry, a distinct triterpenoid saponin profile/mixture was identified to be a pheromone allowing sea cucumber intraspecific recognition and aggregation. This “attractive” profile was characterized as containing disaccharide saponins. This “attractive” aggregation-inducing saponin profile was, however, not conserved in starved individuals that were no longer attractive to other conspecifics. In summary, this study sheds new light on the pheromones in echinoderms. It highlights the complexity of the chemical signals detected by sea cucumbers and suggests a role of saponins well beyond that of a simple toxin.

Echinoderms form a remarkable phylum of marine invertebrates that present specific chemical signatures unique in the animal kingdom. It is particularly the case for essential triterpenoids that evolved separately in each of the five echinoderm classes. Indeed, while most animals have Δ5-sterols, sea cucumbers (Holothuroidea) and sea stars (Asteroidea) also possess Δ7 and Δ9(11)-sterols, a characteristic not shared with brittle stars (Ophiuroidea), sea urchins (Echinoidea), and crinoids (Crinoidea). These particular Δ7 and Δ9(11) sterols emerged as a self-protection against membranolytic saponins that only sea cucumbers and sea stars produce as a defense mechanism. The diversity of saponins is large; several hundred molecules have been described in the two classes of these saponins (i.e., triterpenoid or steroid saponins). This review aims to highlight the diversity of triterpenoids in echinoderms by focusing on sterols and triterpenoid glycosides, but more importantly to provide an updated view of the biosynthesis of these molecules in echinoderms.