Triterpene glycosides defend the Caribbean reef sponge Erylus formosus from predatory fishes

Abstract

The reef sponge Erylus formosus (Demospongiae: Geodiidae) from the Bahamas and southern Florida contains a suite of triterpene glycosides that, at a natural volumetric concentration, deters predation by the fish Thalassoma bifasciatum in laboratory assays, and a natural assemblage of reef fishes in field assays. Antifeedant metabolites were isolated by bioassay-guided fractionation of extracts of E. formosus using standard chromatographic methods and identified by nuclear magnetic resonance (NMR) spectroscopy and mass spectrometry. Included in the deterrent mixture from E. formosus collected in the Bahamas and Florida were at least 6 related triterpene glycosides possessing identical aglycones but with different sugar residues. Two additional compounds with a penasterol triterpene core (formoside, and an N-acetyl galactosamine derivative, formoside B) were found in specimens from the Bahamas but not Florida. Formoside, while being the major deterrent metabolite of E. formosus from the Bahamas, is less potent than the other triterpene glycosides on a weight per volume basis. As a mixture, the triterpene glycosides protect E. formosus from predatory reef fishes, but when these compounds were separated into fractions some failed to deter feeding at natural concentrations. As compounds of this type are beginning to be recognized as prevalent sponge metabolites, we suggest that terpene glycosides may have important ecological functions, just as a defensive role has been ascribed to similar compounds in sea stars, sea cucumbers, and terrestrial plants.

Chemical mediation of interactions among marine organisms

“…264 In a subsequent study, cholesterol 66, 22-dehydrocholesterol 67, 22-dehydro-7)3-hydroxycholesterol 68, and 24-methylenecholesterol 69 were isolated as the active metabolites from Alcyonium paessleri while homarine 70 and trigonelline 71 were isolated as the active metabolites from Gersemia antarctica. 212 Ecologically relevant concentrations of these metabolites were found in the seawater surrounding the soft corals posing a potential barrier to predators. Extracts of the surrounding seawater also inhibited the growth of three sympatric microbes.…”

Identification of RL-TGR, a coreceptor involved in aversive chemical signaling

“…As shown in Fig. 1F, using RT-PCR with primers designed to amplify a segment within the putative ORF of the functional clone, we also detected a transcript in RNA from heads of the bluehead wrasse (Thalassoma bifasciatum), a marine fish that co-occurs with the sponge E. formosus, a source of formoside (20). Comparison of the DNA sequence from the RT-PCR products from bluehead wrasse and the corresponding region of clone A9-f4-230 indicated 100% identity between these two divergent fishes (Fig.…”

“…Furthermore, Xenopus oocytes expressing a zebrafish cDNA library, the cystic fibrosis transmembrane conductance regulator (CFTR), and the beta-2 adrenergic receptor (β 2 AR) exhibited a receptor-mediated electrophysiological response to formoside, a triterpene glycoside deterrent found in the sponge Erylus formosus (19,20). Using CFTR chloride channels to monitor activation of β 2 AR, we found that the kinetics of the formoside-mediated response in oocytes expressing the cDNA library suggest that the zebrafish genome encodes a protein whose activation by formoside causes a G protein-signaling cascade culminating in activation of CFTR.…”

Effects of Holothuroid Ichtyotoxic Saponins on the Gills of Free-Living Fishes and Symbiotic Pearlfishes

“…Since these contributions, saponins have been isolated from numerous species of Aspidochirotida and Dendrochirotida and also from sea stars (Mackie and Turner, 1970;Kitagawa and Kobayashi, 1977;Demeyer et al, 2014). More recently, they have also been noted in sponges (Thompson et al, 1985;Kubanek et al, 2000) and in chrysomelid beetles (Plasman et al, 2000a, b). Saponins have been reported to possess a wide range of biological activities including hemolytic, antitumoral, anti-inflammatory, antifungal, anti-bacterial, cytostatic, and ichthyotoxic properties (Kalinin et al, 1996a(Kalinin et al, , b, 2008Prokofeva et al, 2003;Bordbar et al, 2011).…”