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Sequestration and Possible Role of Dietary Alkaloids in the Sponge-Feeding Mollusk Tylodina perversa

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Molluscs

Part of the book series: Progress in Molecular and Subcellular Biology ((MMB,volume 43))

Abstract

Opisthobranchs of the genus Tylodina are found at exceedingly distant geographical regions in the marine environment but are always associated with sponges of the order Verongida (e.g., Aplysina species) which serve as prey for these gastropods. We investigated the chemical ecology of the Mediterranean species T. perversa that commonly feeds on A. aerophoba. The gastropod sequesters a set of sponge-derived brominated isoxazoline alkaloids which are accumulated in the mantle and egg masses and are furthermore exuded as part of the mucus when the animal is molested. Based on the documented feeding deterrent properties of the sponge alkaloids against fish, it is speculated that the sequestered sponge alkaloids serve also as a defense for T. perversa. Interestingly, specimens of T. perversa that were either collected while feeding on A. aerophoba or had been kept on these sponges under controlled conditions for several weeks almost always contained the brominated alkaloid aerothionin, which is not detected in A. aerophoba but occurs in the sibling species A. cavernicola instead. The latter sponge is also accepted as a food source by the gastropod, at least under experimental conditions. The possible origin of aerothionin in T. perversa is discussed.

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References

  • Aiello A, Fattorusso E, Menna M, Pansini M (1995) Chemistry of Verongida sponges 5. Brominated metabolites from the Caribbean sponge Pseudoceratina sp. Biochem Syst Ecol 23:377–381

    CAS  Google Scholar 

  • Albrizio S, Ciminiello P, Fattorusso E, Magno S, Pansini M (1994) Chemistry of Verongida sponges 1. Constituents of the Caribbean sponge Pseudoceratina crassa. Tetrahedron 50:783–788

    CAS  Google Scholar 

  • Andersen RJ, Faulkner DJ (1972) Antibiotic from marine organisms of the Gulf of California. Book of Abstracts of the Conference “Food and Drugs from the Sea”, Rhode Island, pp. 1111 – 1115.

    Google Scholar 

  • Avila C (1995) Natural products from opisthobranch molluscs: a biological review. Oceanogr Mar Biol Annu Rev 33:487–559

    Google Scholar 

  • Becerro MA, Turon X, Uriz MJ, Templado J (2003) Can a sponge feeder be a herbivore? Tylodina perversa (Gastropoda) feeding on Aplysina aerophoba (Demospongiae). Biol J Linn Soc 78:429–438

    Article  Google Scholar 

  • Ciminiello P, Costantino V, Fattorusso E, Magno S, Mangoni A, Pansini M (1994a) Chemistry of Verongida sponges 2. Constituents of the Caribbean sponge Aplysina fistularis forma fulva. J Nat Prod 57:705–712

    CAS  Google Scholar 

  • Ciminiello P, Fattorusso E, Magno S, Pansini M (1994b) Chemistry of Verongida sponges 3. Constituents of a Caribbean Verongula sp. J Nat Prod 57:1564–1569

    CAS  Google Scholar 

  • Ciminiello P, Fattorusso E, Magno S, Pansini M (1995) Chemistry of Verongida sponges 4. Comparison of the secondary metabolite composition of several specimens of Pseudoceratina crassa. J Nat Prod 58:689–696

    CAS  Google Scholar 

  • Ciminiello P, Fattorusso E, Magno S, Pansini M (1996a) Chemistry of Verongida sponges 6. Comparison of the secondary metabolic composition of Aplysina insularis and Aplysina fulva. Biochem Syst Ecol 24:105–107

    Google Scholar 

  • Ciminiello P, dell’Aversano C, Fattorusso E, Magno S, Carrano L, Pansini M (1996b) Chemistry of Verongida sponges 7. Bromocompounds from the Caribbean sponge Aplysina archeri. Tetrahedron 52:9863–9868

    CAS  Google Scholar 

  • Ciminiello P, Fattorusso E, Forino M, Magno S, Pansini M (1997) Chemistry of Verongida sponges 8. Bromocompounds from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. Tetrahedron 53:6565–6572

    CAS  Google Scholar 

  • Ciminiello P, dell’Aversano C, Fattorusso E, Magno S, Pansini M (1999) Chemistry of Verongida sponges 9. Secondary metabolite composition of the Caribbean sponge Aplysina cauliformis. J Nat Prod 62:590–593

    CAS  Google Scholar 

  • Ciminiello P, dell’Aversano C, Fattorusso E, Magno S, Pansini M (2000) Chemistry of Verongida sponges 10. Secondary metabolite composition of the Caribbean sponge Verongula gigantea. J Nat Prod 63:263–266

    CAS  Google Scholar 

  • Cimino G, Ghiselin MT (1999) Chemical defense and evolutionary trends in biosynthetic capacity among dorid nudibranchs (Mollusca: Gastropoda: Opisthobranchia). Chemoecology 9:187–207

    Article  CAS  Google Scholar 

  • Cimino G, Ghiselin MT (2001) Marine natural products chemistry as an evolutionary narrative. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC, Washington, DC, pp 115–156

    Google Scholar 

  • Cimino G, Sodano G (1994) Transfer of sponge secondary metabolites to predators. In: van Soest RWM, van Kempen TMG, Braekman JC (eds) Sponges in space and time. Balkema, Rotterdam, pp 459–472

    Google Scholar 

  • Cimino G, de Rosa S, de Stefano S, Spinella A, Sodano G (1984) The zoochrome of the sponge Verongia aerophoba (“Uranidine”). Tetrahedron Lett 25:2925–2928

    Article  CAS  Google Scholar 

  • Cimino G, Fontana A, Gimenez F, Marin A, Mollo E, Trivellone E, Zubia E (1993) Biotransformation of a dietary sesterterpenoid in the Mediterranean nudibranch Hypselodoris orsini. Experientia 49:582–586

    Article  CAS  Google Scholar 

  • Cimino G, Fontana A, Gavagnin M (1999) Marine opisthobranch mollusks: chemistry and ecology in sacoglossans and dorids. Curr Org Chem 3:327–372

    CAS  Google Scholar 

  • Di Marzo V, Vardaro RR, Depetrocellis L, Villani G, Minei R, Cimino G (1991) Cyercenes, novel pyrones from the Ascoglossan mollusk Cyerce critallina – tissue distribution, biosynthesis and possible involvement in defense and regenerative processes. Experientia 47:1221-1227

    Article  Google Scholar 

  • Di Marzo V, Marin A, Vardaro RR, Depetrocellis L, Villani G, Cimino G (1993) Histological and biochemical bases of defense mechanisms in 4 species of Polybranchioidea ascoglossan mollusks. Mar Biol 117:367–380

    Google Scholar 

  • Doneddu M, Manunza B (1995) La molluschi gasteropodi rinvenuti in associazione con Verongia aerophoba (Schmidt). Conchiglia 275:4–6

    Google Scholar 

  • Ebel R, Marin A, Proksch P (1999) Organ-specific distribution of dietary alkaloids in the marine opisthobranch Tylodina perversa. Biochem Syst Ecol 27:769–777

    Article  CAS  Google Scholar 

  • Fattorusso E, Forenza S, Minale L, Sodano G (1971) Isolation of 3,4-dihydroxyquinoline-2-carboxylic acid from the sponge Aplysina aerophoba. Gazz Chim Ital 101:104–105

    CAS  Google Scholar 

  • Faulkner DJ (1992) Chemical defenses of marine mollusks. In: Paul VJ (ed) Ecological roles of marine natural products. Comstock, Ithaca, pp 119–163

    Google Scholar 

  • Friedrich AB, Merkert H, Fendert T, Hacker J, Proksch P, Hentschel U (1999) Microbial diversity in the marine sponge Aplysina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridization (FISH). Mar Biol 134:461–470

    Article  Google Scholar 

  • Friedrich AB, Fischer I, Proksch P, Hacker J, Hentschel U (2001) Temporal variation of the microbial community associated with the Mediterranean sponge Aplysina aerophoba. FEMS Microbiol Ecol 38:105–113

    Article  CAS  Google Scholar 

  • Gabb WM (1865) Description of new species of marine shells from the coast of California. Proc Calif Acad Sci 3:182–190

    Google Scholar 

  • Gainey PA, Turk SM (1997) More records of Charonia lampas (L.), a recent record of Pteria hirundo (L.) and a marine slug Tylodina perversa Gmelin new to Britain. J Conchol 36:78–79

    Google Scholar 

  • Gavagnin M, Marin A, Mollo E, Crispino A, Villani G, Cimino G (1994) Secondary metabolites from Mediterranean Elysioidea – origin and biological role. Comp Biochem Physiol B Biochem Mol Biol 108:107–115

    Article  Google Scholar 

  • Gavagnin M, Mollo E, Montanaro D, Ortea J, Cimino G (2000) Chemical studies of Caribbean sacoglossans: dietary relationships with green algae and ecological implications. J Chem Ecol 26:1563–1578

    Article  CAS  Google Scholar 

  • Gmelin JRV (1791) Caroli A Linne systema naturae per regna tria naturae, vol 1, pt 6, cl 6. Vermes, Leipzig, pp 3021–3910

    Google Scholar 

  • Götting (1996) Mollusca. In: Westheide W, Rieger RM (eds) Einzeller und Wirbellose. Spektrum, Heidelberg, pp 276–330

    Google Scholar 

  • Heim I (2003) MSc thesis, University of Stuttgart, Stuttgart

    Google Scholar 

  • Hentschel U, Schmid M, Wagner M, Fieseler L, Gernert C, Hacker J (2001) Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS Microbiol Ecol 35:305–312

    Article  PubMed  CAS  Google Scholar 

  • Hesbacher S, Baur B, Baur A, Proksch P (1995) Sequestration of lichen compounds by three species of terrestrial snails. J Chem Ecol 21:233–246

    Article  CAS  Google Scholar 

  • Pansini M (1997) Effects of light on the morphology, distribution and ecology of some Mediterranean sponges. Biol Mar Mediterr 4:74–80

    Google Scholar 

  • Riedl H (1983) Fauna und Flora des Mittelmeeres. Parey, Hamburg Rützler K (1985) Associations between Caribbean sponges and photosynthetic organisms. In: Rützler K (ed) New perspectives in sponge biology. Smithsonian Institution, Washington, DC, pp 455–466

    Google Scholar 

  • Teeyapant R (1994) Brominated secondary metabolites of the marine sponge Verongia aerophoba Schmidt and the sponge feeding gastropod Tylodina perversa Gmelin: identification, biological activities and biotransformation. Ph.D. thesis, University of Würzburg, Würzburg

    Google Scholar 

  • Teeyapant R, Kreis P, Wray V, Witte L, Proksch P (1993) Brominated secondary compounds from the marine sponge Verongia aerophoba and the sponge feeding gastropod Tylodina perversa. Z Naturforsch 48c:640–644

    Google Scholar 

  • Thoms C (2004) Alkaloide in Schwämmen der Gattung Aplysina – chemische Ökologie und assoziierte Mikroorganismen. Ph.D. thesis, University of Düsseldorf, Düsseldorf

    Google Scholar 

  • Thoms C, Horn M, Wagner M, Hentschel U, Proksch P (2003a) Monitoring microbial diversity and natural product profiles of the sponge Aplysina cavernicola following transplantation. Mar Biol 142:685–692

    CAS  Google Scholar 

  • Thoms C, Ebel R, Hentschel U, Proksch P (2003b) Sequestration of dietary alkaloids by the spongivorous marine mollusc Tylodina perversa. Z Naturforsch 58c:426–432

    Google Scholar 

  • Thoms C, Wolff M, Padmakumar K, Ebel R, Proksch P (2004) Chemical defense of Mediterranean sponges Aplysina cavernicola and Aplysina aerophoba. Z Naturforsch 59c:113–122

    Google Scholar 

  • Tymiak AA, Rinehart KL Jr (1981) Biosynthesis of dibromotyrosine-derived antimicrobial compounds by the marine sponge Aplysina fistularis. J Am Chem Soc 103:6763–6765

    Article  CAS  Google Scholar 

  • Vacelet J (1959) Répartition générale des eponges cornees de la region de Marseille et de quelques stations méditerranées. Rec Trav Stn Mar Endoume 26:39–101

    Google Scholar 

  • Vacelet J (1971) Electron-microscopic study on association between blue-green-algae (Chroococcales) and sponge of genus Verongia. J Microsc 12:363–380

    Google Scholar 

  • Vardaro RR, Dimarzo V, Crispino A, Cimino G (1991) Cyercenes, novel polypropionate pyrones from the autotomizing Mediterranean mollusk Cyerce cristallina. Tetrahedron 47:5569–5576

    Article  CAS  Google Scholar 

  • Voultsiadou-Koukoura E (1987) Some remarks on the Mediterranean species of the genus Aplysina (Demospongia, Verongida). In: Vacelet J, Boury-Esnault N (eds) Taxonomy of Porifera. (NATO ASI Ecological Series G, vol 13) Springer, Berlin Heidelberg New York, pp 275–279

    Google Scholar 

  • Wilkinson CR, Vacelet J (1979) Transplantation of marine sponges to different conditions of light and current. J Exp Mar Biol Ecol 37:91–104

    Article  Google Scholar 

  • Willan RC (1984) A review of diets in the Notaspidea (Mollusca: Opisthobranchia). J Malacol Soc Aust 6:125–142

    Google Scholar 

  • Willan RC (1987) Phylogenetic systematics of the Notaspidea (Opisthobranchia) with reappraisal of families and genera. Am Malacol Bull 5:215–241

    Google Scholar 

  • Willan RC (1998) Order Notaspidea. In: Beesley PL, Ross GJB, Wells A (eds) Mollusca: the southern synthesis (Fauna of Australia, vol 5, part B) CSIRO, Melbourne, pp 977–980

    Google Scholar 

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Authors and Affiliations

  1. Institut für Pharmazeutische Biologie, Heinrich-Heine-Universität, Universitätsstr. 1, 40225, Düsseldorf, Germany

    Peter Proksch

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  1. C. Thoms
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  2. R. Ebel
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  3. Peter Proksch
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  1. Istituto di Chimica Biomolecolare, Consiglio Nazionale delle Ricerche, Via Campi Flegrei, 34, 80078, Pozzuoli (Naples), Italy

    Guido Cimino  & Margherita Gavagnin  & 

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Thoms, C., Ebel, R., Proksch, P. (2006). Sequestration and Possible Role of Dietary Alkaloids in the Sponge-Feeding Mollusk Tylodina perversa . In: Cimino, G., Gavagnin, M. (eds) Molluscs. Progress in Molecular and Subcellular Biology, vol 43. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-30880-5_12

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