Journal of Chemical Ecology

, Volume 42, Issue 1, pp 60–70 | Cite as

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

  • M. Reverter
  • T. Perez
  • A. V. Ereskovsky
  • B. Banaigs


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.


Aplysina sponges Secondary metabolites Bioactivity Temporal variation Intraspecific variations Reproductive cycle Dynamic chemical defense Dienone 



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, 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° awarded by Saint-Petersburg State University) and La Caixa Foundation Fellowship awarded to M.Reverter.

Supplementary material

10886_2015_664_MOESM1_ESM.docx (13 kb)
ESM 1 (DOCX 12 kb)


  1. 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 9:2423–2437PubMedCentralCrossRefPubMedGoogle Scholar
  2. Abdo DA, Motti CA, Battershill CN, Harvey ES (2007) Temperature and spatiotemporal variability of Salicylihalamide A in the sponge Haliclona sp. J Chem Ecol 33:1635–1645CrossRefPubMedGoogle Scholar
  3. 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 147:36–42CrossRefPubMedGoogle Scholar
  4. 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 168:187–196CrossRefGoogle Scholar
  5. Becerro MA, Turon X, Uriz MJ (1997) Multiple functions for secondary metabolites in encrusting marine invertebrates. J Chem Ecol 23:1527–1547CrossRefGoogle Scholar
  6. 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 87:431–441CrossRefGoogle Scholar
  7. 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. 1081–1085Google Scholar
  8. 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 223:1–18CrossRefGoogle Scholar
  9. Braekman J-C, Daloze D (2004) Chemical and biological aspects of sponge secondary metabolites. Phytochem Rev 3:275–283CrossRefGoogle Scholar
  10. 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 5:8282PubMedCentralCrossRefPubMedGoogle Scholar
  11. Carney JR, Rinehart KL (1995) Biosynthesis of brominated tyrosine metabolites by Aplysina fistularis. J Nat Prod 58:971–985CrossRefPubMedGoogle Scholar
  12. 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 57:705–712CrossRefGoogle Scholar
  13. 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 24:105–113CrossRefGoogle Scholar
  14. Cimincello P, Dell’Aversano C, Fattorusso E, Magno S (1996b) Chemistry of Verongida sponges VII-Bromocompounds from the Caribbean sponge Aplysina archeri. Tetrahedron 52:9863–9868CrossRefGoogle Scholar
  15. 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 53:6565–6572CrossRefGoogle Scholar
  16. 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 62:590–593CrossRefGoogle Scholar
  17. 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. 325–353CrossRefGoogle Scholar
  18. 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 11:489–503PubMedCentralCrossRefPubMedGoogle Scholar
  19. Ebel R, Brenzinger M, Kunze A, Gross HJ, Proksch P (1997) Wound activation of protoxins in marine sponge Aplysina aerophoba. J Chem Ecol 23:1451–1462CrossRefGoogle Scholar
  20. Engel S, Pawlik JR (2000) Allelopathic activities of sponge extracts. Mar Ecol Prog Ser 207:273–281CrossRefGoogle Scholar
  21. 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 30:327–336CrossRefGoogle Scholar
  22. 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 38:451–462CrossRefPubMedGoogle Scholar
  23. Hay ME (1996) Marine chemical ecology: What’s known and what’s next? J Exp Mar Biol Ecol 200:103–134CrossRefGoogle Scholar
  24. Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annu Rev Ecol Syst 19:111–145CrossRefGoogle Scholar
  25. 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 37:537–545CrossRefPubMedGoogle Scholar
  26. 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:e28059PubMedCentralCrossRefPubMedGoogle Scholar
  27. 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 7:289–304CrossRefGoogle Scholar
  28. 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 169:87–95CrossRefGoogle Scholar
  29. 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 243:309–312CrossRefGoogle Scholar
  30. 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 26:1123–1133CrossRefGoogle Scholar
  31. 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 25:250–260CrossRefPubMedGoogle Scholar
  32. 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 406:71–78CrossRefGoogle Scholar
  33. Lipowicz B, Hanekop N, Schmitt L, Proksch P (2013) An aeroplysinin-1 specific nitrile hydratase isolated from the marine sponge Aplysina cavernicola. Mar Drugs 11:3046–3067PubMedCentralCrossRefPubMedGoogle Scholar
  34. 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 9:2316–2368PubMedCentralCrossRefPubMedGoogle Scholar
  35. 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 32:2079–2084CrossRefPubMedGoogle Scholar
  36. 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 151:293–299CrossRefGoogle Scholar
  37. 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 19:2285–2296CrossRefPubMedGoogle Scholar
  38. 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 29:1307–1318CrossRefPubMedGoogle Scholar
  39. Matlock DB, Ginsburg DW, Paul VJ (1999) Spatial variability in secondary metabolite production by the tropical red alga Portieria hornemannii. Hydrobiologia 398(399):267–273Google Scholar
  40. 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 31:1161–1174CrossRefPubMedGoogle Scholar
  41. Paul VJ, Arthur KE, Ritson-Williams R, Ross C, Sharp K (2007) Chemical defenses: from compounds to communities. Biol Bull 213:226–251CrossRefPubMedGoogle Scholar
  42. Paul VJ, Van Alstyne KL (1992) Activation of chemical defenses in the tropical green algae Halimeda spp. J Exp Mar Biol Ecol 160:191–203CrossRefGoogle Scholar
  43. Pawlik JR, Chanas B, Toonen RJ, Fenical W (1995) Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency. Mar Ecol Prog Ser 127:183–194CrossRefGoogle Scholar
  44. 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. 577–587CrossRefGoogle Scholar
  45. 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 12:52–61CrossRefPubMedGoogle Scholar
  46. Porter JW, Targett NM (1988) Allelochemical Interactions between Sponges and Corals. Biol Bull 175:230–239CrossRefGoogle Scholar
  47. 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 246:127–135CrossRefGoogle Scholar
  48. 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 207:263–272CrossRefGoogle Scholar
  49. 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. 3–54Google Scholar
  50. Sacristan-Soriano O, Banaigs B, Becerro MA (2011) Relevant spatial scales of chemical variation in Aplysina aerophoba. Mar Drugs 9:2499–2513PubMedCentralCrossRefPubMedGoogle Scholar
  51. Sacristán-Soriano O, Banaigs B, Becerro MA (2012) Temporal trends in the secondary metabolite production of the sponge Aplysina aerophoba. Mar Drugs 10:677–693PubMedCentralCrossRefPubMedGoogle Scholar
  52. 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 17:33–52Google Scholar
  53. Skogsmyr I, Fagerström T (1992) The cost of anti-herbivory defence: an evaluation of some ecological and physiological factors. Oikos 64:451–457CrossRefGoogle Scholar
  54. Tan LT, Goh BPL, Tripathi A, Lim MG, Dickinson GH, Lee SSC, Teo SLM (2010) Natural antifoulants from the marine cyanobacterium Lyngbya majuscula. Biofouling 26:685–695CrossRefPubMedGoogle Scholar
  55. 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 48:939–945Google Scholar
  56. Thompson JE (1984) Chemical ecology and the structure of sponge dominated assemblages. University of California, Ph.D DissertationGoogle Scholar
  57. 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 59:113–122PubMedGoogle Scholar
  58. Thoms C, Ebel R, Proksch P (2006) Activated chemical defense in Aplysina sponges revisited. J Chem Ecol 32:97–123CrossRefPubMedGoogle Scholar
  59. Turon RM (2009) Chemical bioactivity of sponges along an environmental gradient in a Mediterranean cave. Sci Mar 73:387–397CrossRefGoogle Scholar
  60. 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 205:187–204CrossRefGoogle Scholar
  61. 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 16:39–101Google Scholar
  62. Weiss B, Ebel R, Elbrächter M, Kirchner M, Proksch P (1996) Defense metabolites from the marine sponge Verongia aerophoba. Biochem Syst Ecol 24:1–12CrossRefGoogle Scholar
  63. 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 207:227–241CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • M. Reverter
    • 1
  • T. Perez
    • 2
  • A. V. Ereskovsky
    • 2
    • 3
  • B. Banaigs
    • 1
  1. 1.CRIOBE, USR 3278 - CNRS/EPHE/UPVDUniversité de Perpignan Via DomitiaPerpignanFrance
  2. 2.Institut Méditerranéen de Biodiversité et d’Ecologie marine et continentale (IMBE), CNRS, IRD, Aix Marseille Université, Université Avignon, Station Marine d’EndoumeMarseilleFrance
  3. 3.Biological FacultySaint-Petersbourg State UniversitySt. PetersbourgRussia

Personalised recommendations