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Sequestration of Dietary Alkaloids by the Spongivorous Marine Mollusc

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Sequestration of Dietary Alkaloids by the Spongivorous Marine Mollusc Sequestration of Dietary Alkaloids by the Spongivorous Marine Mollusc Tylodina perversa Carsten Thomsa, Rainer Ebela, Ute Hentschelb, and Peter Prokscha,* a Institut für Pharmazeutische Biologie, Universität Düsseldorf, Universitätsstraße 1, Geb. 26.23, D-40225 Düsseldorf, Germany. Fax: 0049-211-81-11923. E-mail: [email protected] b Institut für Molekulare Infektionsbiologie, Universität Würzburg, Röntgenring 11, D-97070 Würzburg, Germany *Author for correspondence and reprint request Z. Naturforsch. 58c, 426Ð432 (2003); received January 15/February 4, 2003 Specimens of the spongivorous Mediterranean opisthobranch Tylodina perversa that had been collected while feeding on Aplysina aerophoba were shown to sequester the brominated isoxazoline alkaloids of their prey. Alkaloids were stored in the hepatopancreas, mantle tis- sues, and egg masses in an organ-specific manner. Surprisingly, the known sponge alkaloid aerothionin which is found only in A. cavernicola but not in A. aerophoba was also among the metabolites identified in wild caught specimens of T. perversa as well as in opisthobranchs with a documented feeding history on A. aerophoba. Mollusc derived aerothionin is pos- tulated to be derived from a previous feeding encounter with A. cavernicola as T. perversa was found to freely feed on both Aplysina sponges in aquarium bioassays. The possible ecological significance of alkaloid sequestration by T. perversa is still unknown. Key words: Sponge-Opisthobranch Interactions, Marine Natural Products, Chemical Ecology Introduction Pansini, 1997). The sibling species A. cavernicola is pale yellow in appearance and dwells in under- Sponges of the genus Aplysina (syn. Verongia) water caves or at depths of up to 40 m and even harbor a wealth of structurally unique brominated below. Just like other Aplysina sponges Ð e.g. isoxazoline alkaloids (e.g. 1Ð4,Fig. 1) that are those occurring in the Caribbean sea (Pawlik et al., thought to be biogenetically derived from 3,5-di- 1995) Ð A. aerophoba and A. cavernicola are bromotyrosine (Tymiak and Rinehart, 1981). rarely attacked by predatory fish presumably due Whereas the spirocyclohexadienylisoxazoline moi- to the presence of the typical brominated Aplysina ety of most brominated alkaloids isolated from alkaloids. Nevertheless, the opisthobranch mollusc Aplysina sponges is structurally identical the re- Tylodina perversa is frequently found feeding on spective compounds differ by the nature of their A. aerophoba and is considered to be a specialized amine substituents linked to the carbonyl group predator on this sponge (Riedl, 1983) and perhaps adjacent to the isoxazoline ring (Fig. 1). Several also on A. cavernicola even though up to now it isoxazoline alkaloids from Aplysina sponges in- has not been reported from the latter from nature. cluding aerothionin (4), aerophobin-2 (2)orisofis- Morphologically defenseless opisthobranchs that tularin-3 (3)(Fig. 1) have recently been shown to are found in the oceans in a dazzling variety of act as strong feeding deterrents against marine shapes and colors are known to feed apparently fishes such as Blennius sphinx (Thoms, 2000) and unharmed on chemically defended sponges and are thought to play a crucial role in the chemical other marine invertebrates thereby accumulating defense of the sponges against predatory fish the chemical weaponry of their prey which in turn (Thoms et al., in preparation). is utilized for the chemical defense of the molluscs The Mediterranean sea hosts two Aplysina spe- e.g. against fishes (Faulkner and Ghiselin, 1983; cies: the sulphurous yellow A. aerophoba is a con- Paul and van Alstyne, 1988; Pawlik, 1988). T. per- spicuous sponge that lives exposed on hard bottom versa is no exception in this regard since it is like- substrata. It can be found at water depths as low wise morphologically defenseless (the rudimentary as 1 m and is among the most common sponges shell provides no efficient defense) and has been occurring in the Mediterranean sea (Riedl, 1983; shown to sequester brominated alkaloids from its 0939Ð5075/2003/0500Ð0426 $ 06.00 ” 2003 Verlag der Zeitschrift für Naturforschung, Tübingen · www.znaturforsch.com · D C. Thoms et al. · Sequestration of Alkaloids by the Mollusc Tylodina perversa 427 H CO 3 Br ence of T. perversa as judged by choice feeding Br experiments and on the organ specific accumula- H N tion of dietary alkaloids during long term feeding HO O H NH N 2 of T. perversa on the sponges A. aerophoba and N N O A. cavernicola under controlled conditions in sea 1 H CO 3 Br water tanks. Furthermore we provide evidence Br based on electron microscopic studies that the se- H N questration of sponge metabolites by T. perversa H CO HO O H NH 3 Br N 2 N N is not paralleled by an accumulation of sponge- Br associated bacteria that are harbored in high den- O 2 OH Br sity in both A. aerophoba and A. cavernicola HO O H N O (Friedrich et al., 1999; Friedrich et al., 2001; N O O N Hentschel et al., 2001; Hentschel et al., 2002; Br N H CO O 3 Br 3 H OH Thoms et al., 2003). OH Br Br O Materials and Methods Br HO O H OCH N N 3 N N H O OH Live specimens of the gastropod T. perversa O 4 were collected along with their prey sponge Aply- Br sina aerophoba in April 2002 off the coast of Br OCH Banyuls-sur-Mer, France. Specimens of the sponge OH O 3 OH OH Aplysina cavernicola were collected off the coast OH of Marseille, France. Three gastropods (group 1) N were immediately dissected into mantle, hepato- H N COOH OH 6 pancreas, alimentary duct, and reproductive or- 5 gans after collection. Six individuals were kept in Fig. 1. Structures of alkaloids: aplysinamisin-1 (1), aero- a sea water tank containing specimens of A. aero- phobin-2 (2), isofistularin-3 (3), aerothionin (4), uranid- ine (5), and A. cavernicola pigment (6) phoba and were allowed to feed ad libitum. After two weeks feeding on A. aerophoba under con- trolled conditions three gastropods were transfer- sponge prey (Teeyapant et al., 1993; Ebel et al., red to a tank containing specimens of the related 1999). sponge species A. cavernicola (group 3) and main- The majority of reports on the sequestration of tained there for two weeks (until the first signs of prey-derived secondary metabolites by opistho- decay at the prey sponge were observed) while the branch molluscs originates from analysis of speci- three remaining individuals were kept on A. aero- mens caught in the wild with a poorly documented phoba for another three weeks, yielding a total of feeding history (e.g. Faulkner and Ghiselin, 1983; five weeks (group 2). After these periods all gas- Pawlik et al., 1988). The full host range of prey tropods were dissected as described above. species amenable to respective opisthobranch spe- Egg masses that had been produced by molluscs cies, the organ-specific qualitative and quantitative of groups 2 and 3 during captivity and egg masses distribution of sequestered dietary secondary me- that had been removed from freshly collected gas- tabolites in the molluscs vs. those in their prey as tropods while feeding on A. aerophoba in the wild well as the metabolic fate of sequestered metabo- were lyophilized for subsequent extraction and lites are often unknown. Knowledge of the dif- HPLC analysis. Fresh egg ribbons were also pre- ferent factors that influence accumulation and re- served for electron microscopical analysis immedi- tention of putative defensive natural products, ately after collection as described below. however, is crucial for an assessment of the eco- Samples of the sponges (A. aerophoba and logical consequences of natural product sequestra- A. cavernicola) used for the feeding experiments tion by opisthobranch molluscs. In this study we were taken at the beginning and in the course of report on an investigation of the feeding prefer- the feeding experiments and analyzed by HPLC. 428 C. Thoms et al. · Sequestration of Alkaloids by the Mollusc Tylodina perversa For HPLC analysis lyophilized samples of man- in 1:1 (v/v) propylene oxide/Epon 812 (Serva) the tle, hepatopancreas, and egg ribbons of the gastro- samples were embedded in Epon 812 at a temper- pods as well as lyophilized samples of the Aplysina ature of 60 ∞C. The embedded samples were sub- sponges were ground, extracted with methanol sequently sectioned with an ultramicrotome (OM and subsequently injected into an HPLC system U3, C. Reichert, Austria) and examined by trans- coupled to a photodiode-array detector (Dionex, mission electron microscopy (Zeiss EM 10, Zeiss, Germany). Routine detection was at 254 nm. The Germany). separation column (125 ¥ 4mmi.d.) was prefilled Feeding experiments with T. perversa employing with Eurosphere C-18 (5 µm) (Knauer, Germany). Aplysina and Axinella sponges were performed in Compounds were identified by their online UV six separate water tanks (size: 20 ¥ 20 ¥ 10 cm), spectra and by direct comparison with previously containing one specimen each of the sponges isolated standards (Ebel et al., 1997). Each com- Aplysina aerophoba, A. cavernicola and either pound in the samples analyzed was quantified Axinella damicornis or A. polypoides (all of them using calibration curves obtained for the respec- approximately 10 cm in diameter) and one individ- tive isolated natural products. ual of T. perversa. All the sponge species used for Electron microscopy was performed employing the experiment had a similar yellow color. The tissue samples of mantle, hepatopancreas and re- gastropod was placed at a starting point at about productive organs of gastropods of group 1 as well 15 cm equal distance from the three sponges. As as with freshly collected egg masses. The samples soon as it had selected one of the respective were cut into small slices with an ethanol-sterilized sponges the result was protocolled. For repetition scalpel, rinsed three times in sterile sea water, experiments the positions of the sponges in the fixed in 2.5% glutaraldehyde, and stored at 4∞ C.
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