Natural Products Isolated From Species of Halgerda Bergh, 1880 (Mollusca: Nudibranchia) and Their Ecological and Evolutionary Implications

Abstract

Abstract-Chemical investigations of five species of molluscan nudibranchs, Halgerda, collected from Australia and Japan were carried out. We have identified a novel tryptophan derivative halgerdamine (1) along with the known compounds, trigonellin (3), esmodil (4), zooanemonin (5) and C2-&#224-D-mannosylpyranosyl-L-tryptophan (2) from H. aurantiomaculata. C2-&#224-D-mannosylpyranosyl-L-tryptophan (2) was thought to be a by-product of tryptophan metabolism exclusive to humans. The only other chordates reported to contain this compound are a number of ascidian species from New Caledonia and Australia including Atriolum robustum and Leptoclinides dubius. The occurrence of 2 in a mollusc has not been previously reported and this study is the first documented occurrence of 2 in an invertebrate. Structure elucidation of the halgerdamine (1) was achieved using high-field 2D NMR spectroscopy. No detectable secondary metabolites were observed in extracts from five of the six other species studied while H. gunnessi contained mixtures of acylated tetrasaccharides. The compounds isolated from species of Halgerda are very different from those found in the close sister taxon, Asteronotus. Specifically, species of Halgerda contain no terpenes, spirodysin or bromophenols as does Asteronotus. Further, in contrast to other members of the Nudibranchia such as Chromodoris and Phyllidia, in which compound yields are quite high, several cryptic species of Halgerda species lack secondary metabolites, while the two highly conspicuous species yield mildly cytotoxic MeOH extracts. Our findings support recent hypotheses regarding progressive evolution of opisthobranchs. In particular, opisthobranchs have evolved to exploit a wider range of food and metabolites than did their ancestors, a demonstration of physiological innovation. Some species of Halgerda may not be chemically protected either via de novo synthesis or by sequestering particularly toxic compounds