Role of secondary metabolites and pigments in the epidermal tissues, ripe ovaries, viscera, gut contents and diet of the sea cucumber Holothuria atra

Abstract

The epidermal tissues, ovaries, viscera, gut contents, and the diet of Holothuria atra (Jaeger), collected from the Great Barrier Reef (GBR), Australia, just prior to spawning, contained carotenoid pigments, mycosporine-like amino acids (MAAs) and three other metabolites in varying proportions. Mycosporine-glycine (mycosporine-gly), palythine, asterina-330, shinorine, mycosporine-2-gly, porphyra-334, and palythinol were present in the epidermal tissues. Mycosporine-gly was the major MAA in the epidermal tissues, gut contents and the diet, and the only MAA present in the ripe ovaries and the viscera. Gadusol, a metabolite with antioxidant properties, which co-occurs with MAAs, and in certain instances with trace amounts of 6-deoxygadusol in unfertilised and fertilised eggs and developing larvae of some marine invertebrates and vertebrates, was absent from H. atra. However, 6-deoxygadusol, with similar physical and chemical properties to gadusol, and the proposed biosynthetic precursor of MAAs, was present, but only in the ovaries. This is first report of the presence of this proposed biogenetic precursor of MAAs in significant amounts in a marine invertebrate. Approximately 90% of the total carotenoids of the epidermal tissues, ovaries and viscera of H. atra are highly oxidised, the main component being astaxanthin followed by canthaxanthin. These were the major carotenoids present in the ovaries and the total carotenoid content was highest in the ovaries. β-carotene, a common egg carotenoid, was present in trace quantities in the ovaries but, along with the xanthophylls lutein and zeaxanthin, it occurred in significant amounts in the gut contents and the diet of H. atra. Carotenoid patterns in the epidermal tissues and viscera were strikingly similar, containing β-carotene, canthaxanthin, astaxanthin, zeaxanthin, lutein, phoenicoxanthin and echinenone. The alkaloids homarine and isomeric trigonelline, (structurally unrelated to MAAs) and 6-deoxygadusol were present only in the ovaries and the viscera. It is suggested that these metabolites and pigments are either involved with photoprotection or reproduction, or associated with both processes. The origin, biogenetic relationships and the roles of these metabolites and pigments in H. atra are discussed.