Effects of depth and light on secondary metabolites and cyanobacterial symbionts of the sponge Dysidea granulosa

Abstract

The tropical sponge Dysidea granulosa contains a number of symbiotic heterotrophic bacteria and large quantities of the photosynthetic cyanobacterium Oscillatoria spongeliae, which are reported to be responsible for the production of ecologically active polybrominated diphenyl ethers (BDEs) in Dysidea spp. In order to better understand the relationship between these symbionts and the production of BDEs, we looked at the variation in secondary chemistry in 3 populations of D. granulosa and the relationship between cyanobacteria and secondary chemistry in the sponge, and experimentally assessed the role that depth and light play in this relationship by transplanting sponges in the field. At a population scale, the concentration of BDEs is positively correlated with the concentration of chlorophyll a (chl a), both varying significantly between populations. Yet, in sponges experimentally transplanted to a deeper site, the concentration of chl a decreased significantly while BDE concentration remained stable. We specifically tested the importance of light in determining levels of symbionts and BDEs by placing sponges under transparent, UV-opaque, and black Plexiglas plates. After 5 wk, levels of BDEs and chl a had decreased significantly, although these trends differed between light treatment, suggesting a lack of direct correlation between BDEs and cyanobacterial populations. This was also supported by a within-sponge analysis of chl a and BDEs, since high levels of compounds were found in the choanosome of the sponge, whereas chl a and cyanobacterial contents were minimal. Our data suggest that the relationship between the levels of BDEs in D. granulosa and its photosynthetic symbionts is more complex than expected. Variation in the levels of secondary metabolites and symbionts seems to be related at a population scale, but unrelated at an individual scale.

Chemical Defenses of Cryptic and Aposematic Gastropterid Molluscs Feeding on their Host Sponge Dysidea granulosa

“…D. granulosa is abundant up to a depth of 5-6 m in Gun Beach, a reef slope habitat with a series of 1-to 5-m-wide channels with vertical walls perpendicular to the shoreline and open to wave action and surge. On this location, D. granulosa has three polybrominated diphenyl ethers (BDEs) as major secondary metabolites (Becerro and Paul, 2004). On Gun Beach, the gastropterids S. psychedelicum and S. nigropunctatum are consistently found on D. granulosa, sometimes sharing the same specimen.…”

“…Samples were then extracted with 1:1 (v/v) DCM/MeOH. This extraction procedure differs slightly from that used by Becerro and Paul (2004) to extract BDEs from sponge samples, since we used DCM/MeOH instead of DCM as the extraction solvent. However, BDEs are exhaustively extracted by both solvent mixtures, and we did not find more polar secondary metabolites in the sponges or the gastropterids.…”

“…For quantification by GC-MS, we dissolved crude extracts in DCM (2 ml/mg) containing naphthalene (50 ug/ml) as internal standard (IS). Quantification was done with a Hewlett-Packard 5890 Series II GC fitted with an HP-5 capillary column (5% phenyl methyl crosslinked silicon siloxane, 30 m long, 0.25 mm i.d., 0.25 um film thickness) and coupled to a Hewlett-Packard 5972 MS. Gas chromatography was performed following methods of Becerro and Paul (2004). One ul of extract solution at a concentration of 0.5 mg/ml was injected.…”

“…We compared the concentration of compound 2 [3,5 dibromo-2-(2',4'-dibromophenoxy)phenol] in gastropterid body parts to the concentrations found by Becerro and Paul (2004) in the sponge ectosome and choanosme. Because we pooled the same gastropterid body parts from the same species, we have a single concentration value for each body part, i.e., we obtained an average value from our replicates but we lack variance data.…”

“…This strategy of sequestration, concentration, modification, and distribution of metabolites from the prey into the body of the predator is found widely in nudibranchs (Cimino and Ghiselin, 1999 and references therein), sacoglossans (Cimino and Ghiselin, 1998;Becerro et al, 2001), notaspideans (Teeyapant et al, 1993;Ebel et al, 1999;Becerro et al, 2003), and sea hares (Johnson and Willows, 1999). D. granulosa is a chemically defended sponge that produces a number of polybrominated diphenyl ethers (Becerro and Paul, 2004). Given the close and consistent association of both gastropterid species with D. granulosa and the widespread occurrence of compound sequestration and biomagnification observed in specialist predators, we set forth the hypothesis that, if they are true specialist predators, both S. nigropunctatum and S. psychedelicum will share secondary chemistry with their host sponge D. granulosa.…”