The role of the hyaline spheres in sea cucumber metamorphosis: lipid storage via transport cells in the blastocoel

Abstract

Background For echinoderms with feeding larvae, metamorphic and post-settlement success may be highly dependent on larval nutrition and the accumulation of energetic lipids from the diet. In contrast to the sea urchins, starfish and brittle stars within the Phylum Echinodermata, sea cucumber metamorphosis does not involve formation of a juvenile rudiment, but instead there is a rearrangement of the entire larval body. Successful metamorphosis in sea cucumbers is often associated with the presence in the late auricularia stage of an evolutionary novelty, the hyaline spheres (HS), which form in the base of the larval arms. Known since the 1850s the function of these HS has remained enigmatic—suggestions include assistance with flotation, as an organizer for ciliary band formation during metamorphosis and as a nutrient store for metamorphosis. Results Here using multiple methodologies (lipid mapping, resin-section light microscopy, lipid and fatty acid analyses) we show definitively that the HS are used to store neutral lipids that fuel the process of metamorphosis in Australostichopus mollis . Neutral lipids derived from the phytoplankton diet are transported by secondary mesenchyme cells (“lipid transporting cells”, LTC), likely as free fatty acids or lipoproteins, from the walls of the stomach and intestine through the blastocoel to the HS; here, they are converted to triacylglycerol with a higher saturated fatty acid content. During metamorphosis the HS decreased in size as the triacylglycerol was consumed and LTC again transported neutral lipids within the blastocoel. Conclusion The HS in A. mollis functions as a nutrient storage structure that separates lipid stores from the major morphogenic events that occur during the metamorphic transition from auricularia–doliolaria–pentactula (settled juvenile). The discovery of LTC within the blastocoel of sea cucumbers has implications for other invertebrate larvae with a gel-filled blastocoel and for our understanding of lipid use during metamorphosis in marine invertebrates.

Controlled spawning and rearing of the sea cucumber, Parastichopus tremulus

“…Thus, there seems to be no benefit to metamorphosis from a prolonged larval stage if no hyaline spheres develop, as these are suggested as a nutrient store during metamorphosis (Peters-Didier & Sewell, 2019).…”

“…Observations on development rate and survival in different temperatures showed a faster development with increasing temperature in the auricularia larvae. The formation of hyaline spheres in auricularia indicates larval competence and subsequent performance (Duy et al, 2016; Peters‐Didier & Sewell, 2019). All late auricularia, with more or less well‐developed hyaline spheres, were found in the 13 and 16°C treatments.…”

Physicochemical Properties and Liposomal Formulations of Hydrolysate Fractions of Four Sea Cucumbers (Holothuroidea: Echinodermata) from the Northwestern Algerian Coast

“…In sea cucumbers, the neutral lipids obtained from phytoplanktonic sources are stored during the feeding period. When larvae are not able to obtain external nutriment sources, neutral lipids are degraded and used to fuel the rest of their metamorphosis during the larval development [57]. Phospholipids and glycolipids are the main component of algal lipids and in Posidonia oceanica leaves [58,59], which are one of the food sources for sea cucumbers [60,61].…”

Supply and larval traits at metamorphosis of a coastal marine invertebrate with a bi-phasic life cycle under contrasting oceanographic conditions

“…Larval fitness of marine invertebrates is influenced by maternal effects and environmental conditions experienced during larval life that will ultimately influence size at metamorphosis, planktonic larval duration (PLD), and early settlement performance (Calado and Leal, 2015). Temperature and food availability are usually identified as the most relevant factors shaping larval performance and survival (Giménez, 2010;Peters-Didier and Sewell, 2019;Rey et al, 2016;Torres et al, 2016).…”

“…Additionally, temporal variability in food supply or quality at different larval development stages (early versus late) may lead to different physiological responses in body size and reserves (Giménez, 2010;Peters-Didier and Sewell, 2019;Phillips, 2006) at recruitment, influencing early post-settlement performance and consequently, population dynamics.…”