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Secondary Metabolome Variability and Inducible Chemical Defenses in the Mediterranean Sponge Aplysina cavernicola

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Abstract

Secondary metabolites play a crucial role in marine invertebrate chemical ecology. Thus, it is of great importance to understand factors regulating their production and sources of variability. This work aimed to study the variability of the bromotyrosine derivatives in the Mediterranean sponge Aplysina cavernicola, and also to better understand how biotic (reproductive state) and abiotic factors (seawater temperature) could partly explain this variability. Results showed that the A. cavernicola reproductive cycle has little effect on the variability of the sponges’ secondary metabolism, whereas water temperature has a significant influence on the production level of secondary metabolites. Temporal variability analysis of the sponge methanolic extracts showed that bioactivity variability was related to the presence of the minor secondary metabolite dienone, which accounted for 50 % of the bioactivity observed. Further bioassays coupled to HPLC extract fractionation confirmed that dienone was the only compound from Aplysina alkaloids to display a strong bioactivity. Both dienone production and bioactivity showed a notable increase in October 2008, after a late-summer warming episode, indicating that A. cavernicola might be able to induce chemical changes to cope with environmental stressors.

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References

  • Abbas S, Kelly M, Bowling J, Sims J, Waters A, Hamann M (2011) Advancement into the Arctic region for bioactive sponge secondary metabolites. Mar Drugs 9:2423–2437

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Abdo DA, Motti CA, Battershill CN, Harvey ES (2007) Temperature and spatiotemporal variability of Salicylihalamide A in the sponge Haliclona sp. J Chem Ecol 33:1635–1645

    Article  CAS  PubMed  Google Scholar 

  • Azevedo LG, Muccillo-Baisch AL, Filgueira M, Boyle RT, Ramos DF, Soares AD, Lerner C, Silva PA, Trindade GS (2008) Comparative cytotoxic and anti-tuberculosis activity of Aplysina caissara marine sponge crude extracts. Comp Biochem Physiol C Toxicol Pharmacol 147:36–42

    Article  PubMed  Google Scholar 

  • Becerro MA, Paul VJ, Starmer J (1998) Intracolonial variation in chemical defenses of the sponge Cacospongia sp. and its consequences on generalist fish predators and the specialist nudibranch predator Glossodoris pallida. Mar Ecol Prog Ser 168:187–196

    Article  Google Scholar 

  • Becerro MA, Turon X, Uriz MJ (1997) Multiple functions for secondary metabolites in encrusting marine invertebrates. J Chem Ecol 23:1527–1547

    Article  CAS  Google Scholar 

  • Bensoussan N, Romano J-C, Harmelin J-G, Garrabou J (2010) High resolution characterization of northwest Mediterranean coastal waters thermal regimes: to better understand responses of benthic communities to climate change. Est Coast Shelf Sci 87:431–441

    Article  Google Scholar 

  • Bergquist PR, Cook SC (2002) Order Verongida Bergquist, 1978. In: JNA H, Van SRWM (eds) Systema Porifera. A guide to the classification of sponges, vol 1. Kluwer Academic, Plenum Publishers, pp. 1081–1085

  • Betancourt-Lozano M, González-Farias FA, González-Acosta B, García-Gasca A (1998) Variation of antimicrobial activity of the sponge Aplysina fistularis (Pallas, 1766) and its relation to associated fauna. J Exp Mar Biol Ecol 223:1–18

    Article  Google Scholar 

  • Braekman J-C, Daloze D (2004) Chemical and biological aspects of sponge secondary metabolites. Phytochem Rev 3:275–283

    Article  CAS  Google Scholar 

  • Cachet N, Genta-Jouve G, Ivanisevic J, Chevaldonné P, Sinniger F, Culioli G, Pérez T, Thomas OP (2015) Metabolomic profiling reveals deep chemical divergence between two morphotypes of the zoanthid Parazoanthus axinellae. Sci Rep 5:8282

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carney JR, Rinehart KL (1995) Biosynthesis of brominated tyrosine metabolites by Aplysina fistularis. J Nat Prod 58:971–985

    Article  CAS  PubMed  Google Scholar 

  • Cimincello P, Dell’Aversano C, Fattorusso E, Magno S (1994) Chemistry of Verongida sponges I-Constituents of the Caribbean sponge Aplysina fistularis forma fulva. J Nat Prod 57:705–712

    Article  Google Scholar 

  • Cimincello P, Dell’Aversano C, Fattorusso E, Magno S (1996a) Chemistry of Verongida sponges VI-Comparison of the secondary metabolic composition of Aplysina insularis and Aplysina fulva. Biochem Syst Ecol 24:105–113

    Article  Google Scholar 

  • Cimincello P, Dell’Aversano C, Fattorusso E, Magno S (1996b) Chemistry of Verongida sponges VII-Bromocompounds from the Caribbean sponge Aplysina archeri. Tetrahedron 52:9863–9868

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Cimincello P, Dell’Aversano C, Fattorusso E, Magno S, Pansini M (1999) Chemistry of Verongida sponges 9.1- Secondary metabolite composition of the Caribbean sponge Aplysina cauliformis. J Nat Prod 62:590–593

    Article  Google Scholar 

  • Cronin G (2001) Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defence theories. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton London New York Washington, pp. 325–353

    Chapter  Google Scholar 

  • De Caralt S, Bry D, Bontemps N, Turon X, Uriz MJ, Banaigs B (2013) Sources of secondary metabolite variation in Dysidea avara (Porifera: Demospongiae): the importance of having good neighbors. Mar Drugs 11:489–503

    Article  PubMed Central  PubMed  Google Scholar 

  • Ebel R, Brenzinger M, Kunze A, Gross HJ, Proksch P (1997) Wound activation of protoxins in marine sponge Aplysina aerophoba. J Chem Ecol 23:1451–1462

    Article  CAS  Google Scholar 

  • Engel S, Pawlik JR (2000) Allelopathic activities of sponge extracts. Mar Ecol Prog Ser 207:273–281

    Article  Google Scholar 

  • Ferretti C, Vacca S, de Ciucis C, Marengo B, Duckworth AR, Manconi R, Pronzato R, Domenicotti C (2009) Growth dynamics and bioactivity variation of the Mediterranean demosponges Agelas oroides (Agelasida, Agelasidae) and Petrosia ficiformis (Haplosclerida, Petrosiidae). Mar Ecol 30:327–336

    Article  Google Scholar 

  • Gochfeld DJ, Kamel HN, Olson JB, Thacker RW (2012) Trade-offs in defensive metabolite production but not ecological function in healthy and diseased sponges. J Chem Ecol 38:451–462

    Article  CAS  PubMed  Google Scholar 

  • Hay ME (1996) Marine chemical ecology: What’s known and what’s next? J Exp Mar Biol Ecol 200:103–134

    Article  CAS  Google Scholar 

  • Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annu Rev Ecol Syst 19:111–145

    Article  Google Scholar 

  • Ivanisevic J, Pérez T, Ereskovsky AV, Barnathan G, Thomas OP (2011a) Lysophospholipids in the Mediterranean sponge Oscarella tuberculata: seasonal variability and putative biological role. J Chem Ecol 37:537–545

    Article  CAS  PubMed  Google Scholar 

  • Ivanisevic J, Thomas OP, Pedel L, Pénez N, Ereskovsky AV, Culioli G, Pérez T (2011b) Biochemical trade-offs: evidence for ecologically linked secondary metabolism of the sponge Oscarella balibaloi. PLoS One 6:e28059

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ivanisevic J, Thomas OP, Lejeusne C, Chevaldonné P, Pérez T (2011c) Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges. Metabolomics 7:289–304

    Article  CAS  Google Scholar 

  • Kelman D, Kushmaro A, Loya Y, Kashman Y, Benayahu Y (1998) Antimicrobial activity of a Red Sea soft coral, Parerythropodium fulvum fulvum: reproductive and developmental considerations. Mar Ecol Prog Ser 169:87–95

    Article  Google Scholar 

  • Kelman D, Benayahu Y, Kashman Y (2000a) Chemical defence of the soft coral Parerythropodium fulvum fulvum (Forskål) in the Red Sea against generalist reef fish. J Exp Mar Biol Ecol 243:309–312

    Article  Google Scholar 

  • Kelman D, Benayahu Y, Kashman Y (2000b) Variation in secondary metabolite concentrations in yellow and grey morphs of the Red Sea soft coral Parerythropodium fulvum fulvum: possible ecological implications. J Chem Ecol 26:1123–1133

    Article  CAS  Google Scholar 

  • Lejeusne C, Chevaldonné P, Pergent-Martini C, Boudouresque CF, Pérez T (2010) Climate change effects on a miniature ocean: the highly diverse, higly impacted Mediterranean Sea. Trends Ecol Evol 25:250–260

    Article  PubMed  Google Scholar 

  • Leong W, Pawlik JR (2010) Evidence of a resource trade-off between growth and chemical defenses among Caribbean coral reef sponges. Mar Ecol Prog Ser 406:71–78

    Article  Google Scholar 

  • Lipowicz B, Hanekop N, Schmitt L, Proksch P (2013) An aeroplysinin-1 specific nitrile hydratase isolated from the marine sponge Aplysina cavernicola. Mar Drugs 11:3046–3067

    Article  PubMed Central  PubMed  Google Scholar 

  • Lira NS, Montes RC, Tavares JF, da Silva MS, da Cunha EVL, de Athayde-Filho PF, Rodrigues LC, da Silva Dias C, Barbosa-Filho JM (2011) Brominated compounds from marine sponges of the genus Aplysina and a compilation of their 13C NMR spectral data. Mar Drugs 9:2316–2368

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • López-Legentil S, Bontemps-Subielos N, Turon X, Banaigs B (2006) Temporal variation in the production of four secondary metabolites in a colonial ascidian. J Chem Ecol 32:2079–2084

    Article  PubMed  Google Scholar 

  • López-Legentil S, Bontemps-Subielos N, Turon X, Banaigs B (2007) Secondary metabolite and inorganic contents in Cystodytes sp. (Ascidiacea): temporal patterns and association with reproduction and growth. Mar Biol 151:293–299

    Article  Google Scholar 

  • Maida M, Carroll AR, Coll JC (1993) Variability of terpene content in the soft coral Sinularia flexibilis (Coelenterata: Octocorallia), and its ecological implications. J Chem Ecol 19:2285–2296

    Article  CAS  PubMed  Google Scholar 

  • Martí R, Fontana A, Uriz M-J, Cimino G (2003) Quantitative assessment of natural toxicity in sponges: toxicity bioassay versus compound quantification. J Chem Ecol 29:1307–1318

    Article  PubMed  Google Scholar 

  • Matlock DB, Ginsburg DW, Paul VJ (1999) Spatial variability in secondary metabolite production by the tropical red alga Portieria hornemannii. Hydrobiologia 398(399):267–273

    Google Scholar 

  • Page M, West L, Northcote P, Battershill C, Kelly M (2005) Spatial and temporal variability of cytotoxic metabolites in populations of the New Zealand sponge Mycale hentscheli. J Chem Ecol 31:1161–1174

    Article  CAS  PubMed  Google Scholar 

  • Paul VJ, Arthur KE, Ritson-Williams R, Ross C, Sharp K (2007) Chemical defenses: from compounds to communities. Biol Bull 213:226–251

    Article  CAS  PubMed  Google Scholar 

  • Paul VJ, Van Alstyne KL (1992) Activation of chemical defenses in the tropical green algae Halimeda spp. J Exp Mar Biol Ecol 160:191–203

    Article  CAS  Google Scholar 

  • Pawlik JR, Chanas B, Toonen RJ, Fenical W (1995) Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency. Mar Ecol Prog Ser 127:183–194

    Article  CAS  Google Scholar 

  • Pérez T, Vacelet J (2014) Effect of climatic and anthropogenic disturbances on sponges fisheries. In: Goffredo S, Dubinsky Z (eds) The Mediterranean Sea: Its history and present challenges, pp. 577–587

    Chapter  Google Scholar 

  • Plouguerne E, Ioannou E, Georgantea P, Vagias C, Roussis V, Hellio C, Kraffe E, Stiger-Pouvreau V (2010) Anti-microfouling activity of lipidic metabolites from the invasive brown alga Sargassum muticum (Yendo) Fensholt. Mar Biotechnol 12:52–61

    Article  CAS  PubMed  Google Scholar 

  • Porter JW, Targett NM (1988) Allelochemical Interactions between Sponges and Corals. Biol Bull 175:230–239

    Article  Google Scholar 

  • Puyana M, Fenical W, Pawlik JR (2003) Are there activated chemical defenses in sponges of the genus Aplysina from the Caribbean? Mar Ecol Prog Ser 246:127–135

    Article  CAS  Google Scholar 

  • Puglisi MP, Paul VJ, Slattery M (2000) Biogeographic comparisons of chemical and structural defenses of the Pacific gorgonians Annella mollis and A. reticulata. Mar Ecol Prog Ser 207:263–272

    Article  Google Scholar 

  • Rhoades DF (1979) Evolution of plant chemical defence against herbivores. In: Rosenthal GA (ed) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp. 3–54

    Google Scholar 

  • Sacristan-Soriano O, Banaigs B, Becerro MA (2011) Relevant spatial scales of chemical variation in Aplysina aerophoba. Mar Drugs 9:2499–2513

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sacristán-Soriano O, Banaigs B, Becerro MA (2012) Temporal trends in the secondary metabolite production of the sponge Aplysina aerophoba. Mar Drugs 10:677–693

    Article  PubMed Central  PubMed  Google Scholar 

  • Scalera LL, Sciscioli M, Matarrese A, Giove C (1971) Observazioni sui cicli sessuali di alcune keratosa (Porifera) e loro interesse negli studie filogenetici. Atti de la Società Peloritana delle Scienze, Fisiche, Matematiche e Naturali 17:33–52

    Google Scholar 

  • Skogsmyr I, Fagerström T (1992) The cost of anti-herbivory defence: an evaluation of some ecological and physiological factors. Oikos 64:451–457

    Article  Google Scholar 

  • Tan LT, Goh BPL, Tripathi A, Lim MG, Dickinson GH, Lee SSC, Teo SLM (2010) Natural antifoulants from the marine cyanobacterium Lyngbya majuscula. Biofouling 26:685–695

    Article  CAS  PubMed  Google Scholar 

  • Teeyapant R, Woerdenbag HJ, Kreis P, Hacker J, Wray V, Witte L, Proksch P (1993) Antibiotic and cytotoxic activity of brominated compounds from the marine sponge Verongia aerophoba. Z Naturforsch, C J Biosci 48:939–945

    CAS  Google Scholar 

  • Thompson JE (1984) Chemical ecology and the structure of sponge dominated assemblages. University of California, Ph.D Dissertation

    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, C, J Biosci 59:113–122

    CAS  PubMed  Google Scholar 

  • Thoms C, Ebel R, Proksch P (2006) Activated chemical defense in Aplysina sponges revisited. J Chem Ecol 32:97–123

    Article  CAS  PubMed  Google Scholar 

  • Turon RM (2009) Chemical bioactivity of sponges along an environmental gradient in a Mediterranean cave. Sci Mar 73:387–397

    Article  CAS  Google Scholar 

  • Uriz MJ, Turon X, Becerro MA, Galera J (1996) Feeding deterrence in sponges. The role of toxicity, physical defenses, energetic contents, and life-history stage. J Exp Mar Biol Ecol 205:187–204

    Article  Google Scholar 

  • Vacelet J (1959) Répartition générale des éponges et systématique des éponges cornées de la région de Marseille et de quelques stations méditerranéennes. Recueil des travaux de la Station Marine d’Endoume 16:39–101

    Google Scholar 

  • Weiss B, Ebel R, Elbrächter M, Kirchner M, Proksch P (1996) Defense metabolites from the marine sponge Verongia aerophoba. Biochem Syst Ecol 24:1–12

    Article  CAS  Google Scholar 

  • Wright JT, de Nys R, Steinberg PD (2000) Geographic variation in halogenated furanones from the red alga Delisea pulchra and associated hervibores and epiphytes. Mar Ecol Prog Ser 207:227–241

    Article  CAS  Google Scholar 

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Acknowledgments

Authors thank Alan Brazo for help in the analytical HPLC analyses. Chomatrographic, spectrometric, and structural analyses were performed using facilities of the Biodiversité et Biotechnologies Marines platform at the University of Perpignan (Bio2Mar, http://bio2mar.obs-banyuls.fr/fr/index.html). The sampling was performed thanks to the diving facilities of the Station Marine d’Endoume (OSU Institut Pytheas). This work was founded partly by the Agence Nationale de la Recherche (France; ECIMAR project, ANR-06-BDIV-001-04), the European Marie Curie mobility program (MIF1-CT-2006-040065-980066, research grant n° 1.38.209.2014 awarded by Saint-Petersburg State University) and La Caixa Foundation Fellowship awarded to M.Reverter.

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Reverter, M., Perez, T., Ereskovsky, A.V. et al. Secondary Metabolome Variability and Inducible Chemical Defenses in the Mediterranean Sponge Aplysina cavernicola . J Chem Ecol 42, 60–70 (2016). https://doi.org/10.1007/s10886-015-0664-9

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