Abstract
Natural products with promising biomedical properties have been described from sponges, but the problem of supply is usually a limiting factor for their pharmacological evaluation. Mycale cecilia produces an array of metabolites containing a pyrrole-2-carbaldehyde moiety (e.g., mycalazals and mycalenitriles) that have shown activity as growth inhibitors of the human prostate carcinoma cell line LNcaP. This study shows that the culture of M. cecilia is a viable method to supply mycalazals while protecting the wild population. Small implants were bound to ceramic tiles, and after 3 to 4 days, the tissue samples formed a secure attachment. Subsequently, these explants were simultaneously cultured in their natural environment and in small tanks for 60 days. Sponges in the tanks were fed a diet consisting of a mixture of two microalgae (Tetraselmis sp. and Isochrysis sp.) and powdered yeast Saccharomyces cerevisiae. The final survival of the explants differed significantly between the two farming methods: It was higher in the natural environment (95 ± 7.07%; overall mean ± standard error) than in the enclosed system (65 ± 21.21%). Growth was also higher than in the tanks, and after 60 days, it increased to 207% in the sea and 65% in the tanks, which represented a daily increase of 3.5% and 1.5%, respectively. At the end of the trial, both the explants cultured in the sea and in the tanks retained the production of bioactive metabolites. The mean concentration of pyrrole-2-carbaldehyde derivatives in wild and cultured sponges was determined by 1H-NMR. These results demonstrate that in-sea aquaculture of M. cecilia is a viable method for supplying the amounts of mycalazal-type compounds needed to advance the studies on their bioactivity.
Similar content being viewed by others
References
Abdo DA, Battershill CN, Harvey ES (2006) Manipulation of environmental variables and the effect on the growth of Haliclona sp.: implications for open-water aquaculture. Mar Biol Res 2:326–332
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
Battershill CN, Page M (1996) Sponge aquaculture for drug production. Aquaculture Update Spring, pp. 5–6
Belarbi EH, Contreras Gómez A, Chisti Y, García Camacho F, Molina Grima E (2003a) Producing drugs from marine sponges. Biotechnol Adv 21:585–598
Belarbi EH, Ramírez Domínguez M, Cerón García MC, Contreras Gómez A, García Camacho F, Molina Grima E (2003b) Cultivation of explants of the marine sponge Crambe crambe in closed systems. Biomol Eng 20:333–337
Blunt JW, Copp BR, Hu W-P, Munro MHG, Northcote PT, Prinsep MR (2009) Marine natural products. Nat Prod Rep 26:170–244 and previous reviews of this series
Burres NS, Clement JJ (1989) Antitumor activity and mechanism of action of the novel marine natural products mycalamide-A and -B and onnamide. Cancer Res 49:2935–2940
Butler MS (2008) Natural product to drugs: natural product-derived compounds in clinical trials. Nat Prod Rep 25:475–516
Carballo JL, Hernández-Zanuy A, Naranjo S, Kukurtzü B, García Cagide A (1999) Recovery of Ecteinascidia turbinata Herman 1880 (Ascidiacea: Perophoridae) populations after different levels of harvesting on a sustainable basis. Bull Mar Sci 65(3):755–776
Carballo JL, Naranjo S, Kukurtzü B, De La Calle F, Hernández-Zanuy A (2000) Production of Ecteinascidia turbinata (Ascidiacea: Perophoridae) for obtaining anticancer compounds. J World Aquac Soc 31(4):481–490
de Caralt S, Uriz MJ, Wijffels RH (2007) Cell culture from sponges: pluripotency and immortality. Trends Biotechnol 25:467–471
de Voogd NJ (2007) The mariculture potential of the Indonesian reef-dwelling sponge Callyspongia (Euplacella) biru: growth, survival and bioactive compounds. Aquaculture 262:54–64
Duckworth AR (2003) Effect of wound size on the growth and regeneration of two temperate subtidal sponges. J Exp Mar Biol Ecol 287:139–153
Duckworth A, Battershill C (2003) Sponge aquaculture for the production of biologically active metabolites: the influence of farming protocols and environment. Aquaculture 221:311–329
Duckworth AR, Pomponi SA (2005) Relative importance of bacteria, microalgae and yeast for growth of the sponge Halichondria melanadocia (De Laubenfels, 1936): a laboratory study. J Exp Mar Biol Ecol 323:151–159
Duckworth AR, Samples GA, Wright AE, Pomponi SA (2003) In vitro culture of the tropical sponge Axinella corrugata (Demospongiae): effect of food cell concentration on growth, clearance rate, and biosynthesis of stevensine. Mar Biotechnol 5:519–527
Duckworth AR, Battershill CN, Schiel DR (2004) Effects of depth and water flow on growth, survival and bioactivity of two temperate sponges cultured in different seasons. Aquaculture 242:237–250
Faulkner DJ (2002) Marine natural products. Nat Prod Rep 19:1–48 (and previous reviews of this series)
Frost TM (1980) Clearance rate determinations for the freshwater sponge Spongilla lacustris: effects of temperature, particle type and concentration, and sponge size. Arch Hydrobiol 90:330–356
Fry WG (1971) The biology of larvae of Ophlitaspongia seriata from two North Wales populations. In: Crisp DJ (ed) Proceedings of the fourth European marine biology symposium. Cambridge University Press, Cambridge, pp 155–178
Fusetani N, Yasumuro K, Matsunaga S, Hashimoto K (1989) Mycalolides A–C, hybrid macrolides of ulapualides and halichondramide, from a sponge of the genus Mycale. Tetrahedron Lett 30:2809–2812
Gerrodette T, Flechsig AO (1979) Sediment-induced reduction in the pumping rate of the tropical sponge Verongia lacunosa. Mar Biol 55:103–110
Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum, New York, pp 26–60
Hadas E, Shpigel M, Ilan M (2005) Sea ranching of the marine sponge Negombata magnifica (Demospongiae, Latrunculiidae) as a first step for latrunculin B mass production. Aquaculture 244:159–169
Hood KA, West LM, Rouwé B, Northcote PT, Berridge MV, Wakefield SJ, Miller JH (2002) Peloruside A, a novel antimitotic agent with placitaxel-like microtubule stabilizing activity. Cancer Res 62:3356–3360
Huzil JT, Chik JK, Slysz GW, Freedman H, Tuszynski J, Taylor RE, Sackett DL, Schriemer DC (2008) A unique mode of microtubule stabilization induced by peloruside A. J Mol Biol 378:1016–1030
Keyzers RA, Davies-Coleman MT (2005) Anti-inflammatory metabolites from marine sponges. Chem Soc Rev 34:355–365
Klöppel A, Pfannkuchen M, Putz A, Proksch P, Brümmer F (2008) Ex situ cultivation of Aplysina aerophoba close to in situ conditions: ecological, biochemical and histological aspects. Mar Ecol 29:1–14
Matsunaga S, Sugawara T, Fusetani N (1998) New mycalolides from the marine sponge Mycale magellanica and their interconversion. J Nat Prod 61:1164–1167
Mendola D (2003) Aquaculture of three phyla of marine invertebrates to yield bioactive metabolites: process developments and economics. Biomol Eng 20:441–458
Mendola D, Naranjo S, Duckworth AR, Osinga R (2006) The promise of aquaculture for delivering sustainable supplies of new drugs from the sea: examples from in-sea, and tank-based invertebrate culture projects from around the world. In: Proksch P, Müller WEG (eds) Frontiers in marine biotechnology. Horizon Bioscience, Norfolk, pp 22–72
Mendola D, de Caralt S, Uriz MJ, Fred van den End JVL, Wijffels R (2008) Environmental flow regimes for Dysidea avara sponges. Mar Biotechnol 10:622–630
Müller WE, Wimmer W, Schatton W, Böhm M, Batel R, Filic Z (1999) Initiation of an aquaculture of sponges for the sustainable production of bioactive metabolites in open systems: example, Geodia cydonium. Mar Biotechnol 1:569–579
Munro MHG, Blunt JW, Dumdei EJ, Hickford SJH, Lill RE, Li S, Battershill CN, Duckworth AR (1999) The discovery and development of marine compounds with pharmaceutical potential. J Biotechnol 70:15–25
Nakao Y, Yoshida S, Matsunaga S, Shindoh N, Terada Y, Nagai K, Yamashita JK, Ganesan A, van Soest RWM, Fusetani N (2006) Azumamides A–E: histone deacetylase inhibitory cyclic tetrapeptides from the marine sponge Mycale izuensis. Angew Chem Int Ed 45:7553–7555
Naranjo SA, Kukurtçu HB, Barbero C, Martin S, Carballo JL (2001) Aquaculture of Ecteinascidia turbinata Herdman, 1880 as source of marine anticancer agents. In: Lambert C, Yokosawa H (eds) Biology of ascidians. Springer, Berlin, pp 355–360
Newman DJ, Cragg GM (2004) Marine natural products and related compounds in clinical and advanced preclinical trials. J Nat Prod 67:1216–1238
Northcote PT, Blunt JW, Munro MHG (1991) Pateamine: a potent cyototoxin from the New Zealand marine sponge Mycale sp. Tetrahedron Lett 32:6411–6414
Ortega MJ, Zubía E, Sánchez MC, Salvá J, Carballo JL (2004) Structure and cytotoxicity of new metabolites from the sponge Mycale cecilia. Tetrahedron 60:2517–2524
Osinga R, Tramper J, Wijffels RH (1999) Cultivation of marine sponges. Mar Biotechnol 1:509–532
Osinga R, Kleijn R, Groenendijk E, Niesink P, Tramper J, Wijffels RH (2001) Development of in vivo sponge cultures: particle feeding by the tropical sponge Pseudosuberites aff. andrewsi. Mar Biotechnol 3:544–554
Osinga R, Belarbi EH, Molina Grima E, Tramper J, Wijffels RH (2003) Progress towards a controlled culture of the marine sponge Pseudosuberites andrewsi in a bioreactor. J Biotechnol 100:141–146
Page MJ, Northcote PT, Webb VL, Mackey S, Handley SJ (2005) Aquaculture trials for the production of biologically active metabolites in the New Zealand sponge Mycale hentscheli (Demospongiae: Poecilosclerida). Aquaculture 250:256–269
Pauli GF, Jaki BU, Lankin DC (2005) Quantitative 1H NMR: Development and potential of a method for natural products analysis. J Nat Prod 68:133–149
Pomponi SA, Willoughby R (1994) Sponge cell culture for production of bioactive metabolites. In: van Soest RWM et al (eds) Sponges in time and space. Balkema, Rotterdam, pp 395–400
Phuwapraisirisan P, Matsunaga S, van Soest RWM, Fusetani N (2002) Isolation of a new mycalolide from the marine sponge Mycale izuensis. J Nat Prod 65:942–943
Romo D, Rzasa RM, Shea HA, Park K, Langenhan JM, Sun L, Akhiezer A, Liu JO (1998) Total synthesis and immunosuppressive activity of (−) pateamine A and related compounds of a β-lactam-based macrocyclization. J Am Soc 120:12237–12254
Rzasa RM, Romo D, Stirling DJ, Blunt JW, Munro MHG (1995) Structural and synthetic studies of the pateamines: synthesis and absolute configuration of the hydroxydienoate fragment. Tetrahedron Lett 36:5307–5310
Salomon CE, Magarvey NA, Sherman DH (2004) Merging the potential of microbial genetics with biological and chemical diversity: an even brighter future for marine natural product drug discovery. Nat Prod Rep 21:105–121
Schaufelberger DE, Koleck MP, Beutler JA, Vatakis AM, Alvarado AB, Andrews P, Marzo LV, Muschik GM, Roach J, Ross JT, Lebherz WB, Reeves MP, Eberwein RM, Rodgers LL, Testerman RP, Snader KM, Forenza S (1991) The large-scale isolation of bryostatin 1 from Bugula neritina following current good manufacturing practices. J Nat Prod 54:1265–1270
Sipkema D, Snijders APL, Schroen CGPH, Osinga R, Wijffels RH (2004) The life and death of sponge cells. Biotechnol Bioeng 85:239–247
Sipkema D, Franssen MCR, Osinga R, Tramper J, Wijffels RH (2005a) Marine sponges as pharmacy. Mar Biotechnol 7:142–162
Sipkema D, Osinga R, Schatton W, Mendola D, Tramper J, Wijffels RH (2005b) Large-scale production of pharmaceuticals by marine sponges: sea, cell, or synthesis? Biotechnol Bioeng 90:201–222
Thakur NL, Müller WEG (2004) Biotechnological potential of marine sponges. Curr Sci 86:1506–1512
West LM, Northcote PT, Hood KA, Miller JH, Page MJ (2000a) Mycalamide D, a new cytotoxic amide from the New Zealand marine sponge Mycale species. J Nat Prod 63:707–709
West LM, Northcote PT, Battershill CN (2000b) Peloruside A: a potent cytotoxic macrolide isolated from the New Zealand marine sponge Mycale sp. J Org Chem 65:445–449
Wulff JL (2006) Resistance vs. recovery: morphological strategies of coral reef sponges. Funct Ecol 20:699–708
Yánez B (2004) Influencia de la temperatura sobre el crecimiento y la supervivencia de algunas esponjas marinas en condiciones de cultivo. MSc Instituto de Ciencias del Mar y Limnología-UNAM, 165 pp
Acknowledgments
JLC is grateful to the Programa de Apoyos para la Superación del Personal Académico (PASPA) de la DGAPA (UNAM) for providing a grant during a sabbatical stay in Spain. We thank Clara Ramírez Jáuregui for help with the literature. This research was supported in part by grants from the Ministerio de Educación y Ciencia (Spain)-FEDER (research project CTQ2004-02361) and Junta de Andalucía (FQM-169).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Carballo, J.L., Yañez, B., Zubía, E. et al. Culture of Explants from the Sponge Mycale cecilia to Obtain Bioactive Mycalazal-Type Metabolites. Mar Biotechnol 12, 516–525 (2010). https://doi.org/10.1007/s10126-009-9235-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-009-9235-9