Dataset Information

A Distinct Saponin Profile Drives an Olfactory-Mediated Aggregation in the Aquacultivated Sea Cucumber Holothuria scabra.

ABSTRACT: 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.

SUBMITTER: Claereboudt EJS

PROVIDER: S-EPMC10053547 | biostudies-literature | 2023 Mar

REPOSITORIES: biostudies-literature

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A Distinct Saponin Profile Drives an Olfactory-Mediated Aggregation in the Aquacultivated Sea Cucumber <i>Holothuria scabra</i>.

Claereboudt Emily J S EJS Claereboudt Michel R MR Savarino Philippe P Caulier Guillaume G Gaumez Loic L Deleu Magali M Gerbaux Pascal P Eeckhaut Igor I

Marine drugs 20230316 3

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 <i>Holothuria scabra</i> both as adults in large sea-based pen ...[more]

PMID: 36976233

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Project description:The Aerobic Scope (AS), which reflects the functional capacity for biological fitness, is a highly relevant proxy to determine thermal tolerance in various taxa. Despite the importance of this method, its implementation is often hindered, due to lacking techniques to accurately measure standard- (SMR) and maximal- (MMR) metabolic rates, especially in sluggish marine invertebrates with low oxygen consumption rates, such as sea cucumbers. In this study the AS concept was modified to define a Temperature-induced Aerobic Scope (TAS), based on metabolic rate changes due to temperature adjustments rather than traditionally used physical activity patterns. Consequentially, temperature dependent peak and bottom O2 consumption rates, defined as Temperature-induced Maximal- (TMMR) and Standard Metabolic Rates (TSMR), respectively, served as MMR and SMR alternatives for the sea cucumber Holothuria scabra. TMMR and TSMR were induced through acute temperature change (2°C per hour; 17-41°C) until critical warm (WTcrit) and cold (CTcrit) temperatures were reached, respectively. In addition, Hsp70 gene expression linked to respiration rates served as synergistic markers to confirm critical threshold temperatures. O2 consumption of H. scabra peaked distinctly at WTcrit of 38°C (TMMR = 33.2 ± 4.7 μgO2 g-1 h-1). A clear metabolic bottom line was reached at CTcrit of 22°C (TSMR = 2.2 ± 1.4 μgO2 g-1 h-1). Within the thermal window of 22-38°C H. scabra sustained positive aerobic capacity, with assumed optimal performance range between 29-31.5°C (13.85-18.7 μgO2 g-1 h-1). Between 39-41°C H. scabra decreased respiration progressively, while gene expression levels of Hsp70 increased significantly at 41°C, indicating prioritization of heat shock response (HSR) and homeostatic disruption. At the cold end (17-22°C) homeostatic disruption was visible through incrementally increasing energetic expenses to fuel basal maintenance costs, but no Hsp70 overexpression occurred. TMMR, TSMR and TAS proved to be reliable metrics, similar to the traditional energetic key parameters MMR, SMR and AS, to determine a specific aerobic performance window for the sluggish bottom dwelling species H. scabra. In addition, the linkage between respiration physiology and molecular defense mechanisms showed valuable analytical synergies in terms of mechanistic prioritization as response to thermal stress. Overall, this study will help to define lethal temperatures for aquaculture and to predict the effects of environmental stress, such as ocean warming, in H. scabra.

Project description:The sea cucumber Holothuria scabra is an economically valuable marine species which is distributed throughout the Asia-Pacific region. With the natural population declining due to over fishing, aquaculture of this species is deemed necessary. Hence, it is essential to understand the mechanisms regulating the reproduction in order to increase their populations. Sex steroids, including estrogens, androgens and progestogens, play an important role in reproduction in most vertebrates and several invertebrates. It has been proposed that sea cucumbers have the same sex steroids as vertebrates but the steroidogenic pathway in the sea cucumbers is still unclear. In this study, we demonstrated by using liquid chromatography-tandem mass spectrometry (LC-MS/MS) that sex steroids (estradiol, progesterone, and testosterone) were present in H. scabra neural and gonadal tissues. In silico searches of available sea cucumber transcriptome data identified 26 steroidogenesis-related genes. Comparative analysis of encoded proteins for the steroidogenic acute regulatory protein (HscStAR), CYP P450 10, 17 and 3A (HscCYP10, HscCYP17, HscCYP3A) and hydroxysteroid dehydrogenases (Hsc3β-HSD, Hsc17β-HSD) with other species was performed to confirm their evolutionary conservation. Gene expression analyses revealed widespread tissue expression. Real-time PCR analysis revealed that HscStAR, HscCYP10, Hsc3β-HSD, and Hsc17β-HSD gene expressions were similar to those in ovaries and testes, which increased during the gonad maturation. HscCYP17 mRNA was increased during ovarian development and its expression declined at late stages in females but continued high level in males. The expression of the HscCYP3A was high at the early stages of ovarian development, but not at other later stages in ovaries, however it remained low in testes. Moreover, a role for steroids in reproduction was confirmed following the effect of sex steroids on vitellogenin (Vtg) expression in ovary explant culture, showing upregulation of Vtg level. Collectively, this study has confirmed the existence of steroids in an echinoderm, as well as characterizing key genes associated with the steroidogenic pathway. We propose that sex steroids might also be associated with the reproduction of H. scabra, and the identification of biosynthetic genes enables future functional studies to be performed.

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Dataset Information

A Distinct Saponin Profile Drives an Olfactory-Mediated Aggregation in the Aquacultivated Sea Cucumber Holothuria scabra.

Publications

A Distinct Saponin Profile Drives an Olfactory-Mediated Aggregation in the Aquacultivated Sea Cucumber <i>Holothuria scabra</i>.

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