Examination of marine-based cultivation of three demosponges for acquiring bioactive marine natural products

Marine Drugs

Volumn 9, Issue 11, 2011, Pages 2201-2219

  Bergman, Oded ^a   Mayzel, Boaz ^a   Anderson, Matthew A ^b   Shpigel, Muki ^c   Hill, Russell T ^b   Ilan, Micha ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF MARYLAND CENTER FOR ENVIRONMENTAL SCIENCE   (United States)

^c NATIONAL CENTER FOR MARICULTURE   (Israel)

Author keywords

Aquaculture; Denaturing Gradient Gel Electrophoresis (DGGE); Mariculture; Marine natural products; Red sea

Indexed keywords

HALITOXIN; LATRUNCULIN B; MARINE TOXIN; NATURAL PRODUCT; SWINHOLIDE A; UNCLASSIFIED DRUG;

AMPHIMEDON CHLOROS; ARTICLE; BACTERIUM CULTURE; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; GROWTH RATE; MARICULTURE; MARINE SPECIES; MICROBIAL COMMUNITY; MICROBIAL CONSORTIUM; MICROORGANISM; NEGOMBATA MAGNIFICA; NONHUMAN; SPECIES CULTIVATION; SPECIES DIFFERENCE; SURVIVAL RATE; THEONELLA SWINHOEI;

EID: 82655166473     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md9112201     Document Type: Article

References (71)

1. Hentschel, U.; Schmid, M.; Wagner, M.; Fieseler, L.; Gernert, C.; Hacker, J. Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS Microbiol. Ecol. 2001, 35, 305-312. (Pubitemid 32320007)
2. Blunt, J.W.; Copp, B.R.; Hu, W.P.; Munro, M.G.H.; Northcote, P.T.; Prinsep, M.P. Marine natural products. Nat. Prod. Rep. 2009, 26, 170-244.
3. Faulkner, D.J. Marine natural products. Nat. Prod. Rep. 1998, 15, 113-158. (Pubitemid 28202595)
4. Proksch, P.; Ebel, R.; Edrada, R.A.; Schupp, P.; Lin, W.H.; Sudarsono Wray, V.; Steube, K. Detection of pharmacologically active natural products using ecology. Selected examples from Indopacific marine invertebrates and sponge-derived fungi. Pure Appl. Chem. 2003, 75, 343-352.
5. Sipkema, D.; Franssen, M.C.; Osinga, R.; Tramper, J.; Wijffels, R.H. Marine sponges as pharmacy. Mar. Biotechnol. 2005, 7, 142-162. (Pubitemid 41187741)
6. Schmitz, F.J.; Bowden, B.F.; Toth, S.I. Antitumor and Cytotoxic Compounds from Marine Organisms. In Marine Biotechnology: Pharmaceutical and Bioactive Natural Products; Attaway, D.H., Zaborsky, O.R., Eds.; Plenum Press: New York, NY, USA, 1993; Volume 1, pp. 197-308.
7. Carballo, J.; Yanez, B.; Zubia, E.; Ortega, M.; Vega, C. Culture of explants from the sponge Mycale cecilia to obtain bioactive mycalazal-type metabolites. Mar. Biotechnol. 2010, 12, 516-525.
8. Sipkema, D.; Osinga, R.; Schatton, W.; Mendola, D.; Tramper, J.; Wijffels, R.H. Large-scale production of pharmaceuticals by marine sponges: Sea, cell, or synthesis? Biotechnol. Bioeng. 2005, 90, 201-222. (Pubitemid 40571480)
9. Custodio, M.R.; Prokic, I.; Steffen, R.; Koziol, C.; Borojevic, R.; Brümmer, F.; Nickel, M.; Müller, W.E.G. Primmorphs generated from dissociated cells of the sponge Suberites domuncula: A model system for studies of cell proliferation and cell death. Mech. Ageing Dev. 1998, 105, 45-59. (Pubitemid 28539180)
10. Müller, W.E.G.; Wiens, M.; Batel, R.; Steffen, R.; Borojevic, R.; Custodio, M.R. Establishment of a primary cell culture from a sponge: primmorphs from Suberites domuncula. Mar. Ecol. Prog. Ser. 1999, 178, 205-219. (Pubitemid 29178221)
11. Zhang, X.; Cao, X.; Zhang, W.; Yu, X.; Jin, M. Primmorphs from archaeocytes-dominant cell population of the sponge Hymeniacidon perleve: Improved cell proliferation and spiculogenesis. Biotechnol. Bioeng. 2003, 84, 583-590. (Pubitemid 37356380)
12. Rinkevich, B.; Blisko, R.; Ilan, M. Further steps in the initiation of cell cultures from embryos and adult sponge colonies. Vitro Cell. Dev. Biol. 1998, 34, 753-756. (Pubitemid 29077058)
13. Sipkema, D.; Snijders, A.P.L.; Schroen, C.G.P.H.; Osinga, R.; Wijffels, R.H. The life and death of sponge cells. Biotechnol. Bioeng. 2003, 85, 239-247. (Pubitemid 38182216)
14. Ilan, M.; Contini, H.; Carmeli, S.; Rinkevich, B. Progress towards cell cultures from a marine sponge that produces bioactive compounds. J. Mar. Biotechnol. 1996, 4, 145-149. (Pubitemid 126648969)
15. Rinkevich, B. Cell cultures from marine invertebrates: Obstacles, new approaches and recent improvements. J. Biotechnol. 1999, 70, 133-153. (Pubitemid 29299269)
16. Osinga, R. Biotechnological aspects of marine sponges. J. Biotechnol. 2003, 100, 91-92. (Pubitemid 35341334)
17. Duckworth, A.R. Effect of wound size on the growth and regeneration of two temperate subtidal sponges. J. Exp. Mar. Biol. Ecol. 2003, 287, 139-153. (Pubitemid 36260853)
18. Belarbi, E.H.; Domínguez, M.R.; Cerón García, M.C.; Contreras Gómez, A.; García Camacho, F.; Molina Grima, E. Cultivation of explants of the marine sponge Crambe crambe in closed systems. Biomol. Eng. 2003, 20, 333-337. (Pubitemid 36959684)
19. Osinga, R.; de Beukelaer, P.B.; Meijer, E.M.; Tramper, J.; Wijffels, R.H. Growth of the sponge Pseudosuberites (aff.) andrewsi in a closed system. J. Biotechnol. 1999, 70, 155-161. (Pubitemid 29299270)
20. Belarbi, E.H.; Gomes, A.C.; Chisti, Y.; Garcia-Camacho, F.G.; Grima, E.M. Producing drugs from marine sponges. Biotechnol. Adv. 2003, 21, 585-598.
21. Duckworth, A.R.; Battershill, C.N. Developing farming structures for production of biologically active sponge metabolites. Aquaculture 2003, 217, 139-156. (Pubitemid 36219189)
22. Page, M.J.; Northcote, P.T.; Webb, V.L.; Mackey, S.; Handley, S.J. Aquaculture trials for the production of biologically active metabolites in the New Zealand sponge Mycale hentscheli (Demospongiae: Poecilosclerida). Aquaculture 2005, 250, 256-269. (Pubitemid 41525602)
23. Milanese, M.; Sarà, M.; Manconi, R.; Ben Abdalla, A.; Pronzato, R. Commercial sponge fishing in Libya: historical records, present status and perspectives. Fish. Res. 2008, 89, 90-96. (Pubitemid 350181148)
24. Duckworth, A.R.; Battershill, C.N.; Bergquist, P.R. Influence of explant procedures and environmental factors on culture success of three sponges. Aquaculture 1997, 156, 251-267. (Pubitemid 27523453)
25. Corriero, G.; Longo, C.; Mercurio, M.; Nonnis Marzano, C.; Lembo, G.; Spedicato, M.T. Rearing performance of Spongia officinalis on suspended ropes off the Southern Italian Coast (Central Mediterranean Sea). Aquaculture 2004, 238, 195-205. (Pubitemid 39123646)
26. Hadas, E.; Shpigel, M.; Ilan, M. Sea ranching of the marine sponge Negombata magnifica (Demospongiae, Latrunculiidae) as a first step for latrunculin B mass production. Aquaculture 2005, 244, 159-169.
27. Koopmans, M.; Wijffels, R.H. Seasonal growth rate of the sponge Haliclona oculata (Demospongiae: Haplosclerida). Mar. Biotechnol. 2008, 10, 502-510.
28. Duckworth, A.R. Farming sponges to supply bioactive metabolites and bath sponges: A review. Mar. Biotechnol. 2009, 11, 669-679.
29. de Caralt, S.; Sanchez-Fontenla, J.; Uriz, M.J.; Wijffels, R.H. In situ aquaculture methods for Dysidea avara (Demospongiae, Porifera) in the Northwestern Mediterranean. Mar. Drugs 2010, 8, 1731-1742.
30. Wang, G. Diversity and biotechnological potential of the sponge-associated microbial consortia. J. Ind. Microbiol. Biotechnol. 2006, 33, 545-551. (Pubitemid 43876116)
31. Taylor, M.W.; Radax, R.; Steger, D.; Wagner, M. Sponge-associated microorganisms: Evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 2007, 71, 295-347. (Pubitemid 46954308)
32. Hentschel, U.; Hopke, J.; Horn, M.; Friedrich, A.B.; Wagner, M.; Hacker, J.; Moore, B.S. Molecular evidence for a uniform microbial community in sponges from different oceans. Appl. Environ. Microbiol. 2002, 68, 4431-4440. (Pubitemid 34988126)
33. Hill, R.T. Microbes from marine sponges: A treasure trove of biodiversity for natural products discovery. In Microbial Diversity and Bioprospecting; Bull, A.T., Ed.; ASM Press: Washington, DC, USA, 2004; pp. 177-190.
34. Berthold, R.J.; Borowitzka, M.A.; Mackay, M.A. The ultrastructure of Oscillatoria spongeliae, the blue-green algal endosymbiont of the sponge Dysidea herbacea. Phycologia 1982, 21, 327-335.
35. Hentschel, U.; Usher, K.M.; Taylor, M.W. Marine sponges as microbial fermenters. FEMS Microbiol. Ecol. 2006, 55, 167-177.
36. Weisz, J.B.; Lindquist, N.; Martens, C.S. Do associated microbial abundances impact marine demosponge pumping rates and tissue densities? Oecologia 2008, 155, 367-376.
37. Mohamed, N.M.; Rao, V.; Hamann, M.T.; Kelly, M.; Hill, R.T. Monitoring bacterial diversity of the marine sponge Ircinia strobilina upon transfer into aquaculture. Appl. Environ. Microbiol. 2008, 74, 4133-4143. (Pubitemid 351962439)
38. Taylor, M.W.; Schupp, P.J.; de Nys, R.; Kjelleberg, S.; Steinberg, P.D. Biogeography of bacteria associated with the marine sponge Cymbastela concentrica. Environ. Microbiol. 2005, 7, 419-433. (Pubitemid 40290130)
39. Webster, N.S.; Taylor, M.W.; Behnam, F.; Lucker, S.; Rattei, T.; Whalan, S.; Horn, M.; Wagner, M. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ. Microbiol. 2010, 12, 2070-2082.
40. Lee, O.O.; Lau, S.C.K.; Qian, P.Y. Consistent bacterial community structure associated with the surface of the sponge Mycale adhaerens bowerbank. Microb. Ecol. 2006, 52, 693-707.
41. Webster, N.S.; Cobb, R.E.; Negri, A.P. Temperature thresholds for bacterial symbiosis with a sponge. ISME J. 2008, 2, 830-842.
42. Webster, N.S.; Webb, R.I.; Ridd, M.J.; Hill, R.T.; Negri, A.P. The effects of copper on the microbial community of a coral reef sponge. Mar. Biotechnol. 2001, 3, 600-608.
43. Webster, N.S.; Xavier, J.R.; Freckelton, M.; Motti, C.A.; Cobb, R. Shifts in microbial and chemical patterns within the marine sponge Aplysina aerophoba during a disease outbreak. Environ. Microbiol. 2008, 10, 3366-3376.
44. Webster, N.S.; Cobb, R.E.; Soo, R.; Anthony, S.L.; Battershill, C.N.; Whalan, S.; Evans-Illidge, E. Bacterial community dynamics in the marine sponge Rhopaloeides odorabile under in situ and ex situ cultivation. Mar. Biotechnol. 2010, 13, 296-304.
45. Mohamed, N.M.; Enticknap, J.J.; Lohr, J.E.; McIntosh, S.M.; Hill, R.T. Changes in bacterial communities of the marine sponge Mycale laxissima on transfer into aquaculture. Appl. Environ. Microbiol. 2008, 74, 1209-1222. (Pubitemid 351287093)
46. Isaacs, L.T.; Kan, J.; Nguyen, L.; Videau, P.; Anderson, M.A.; Wright, T.L.; Hill, R.T. Comparison of the bacterial communities of wild and captive sponge Clathria prolifera from the Chesapeake Bay. Mar. Biotechnol. 2009, 11, 758-770.
47. Friedrich, A.B.; Fischer, I.; Proksch, P.; Hacker, H.; Hentschel, U. Temporal variation of the microbial community associated with the Mediterranean sponge Aplysina aerophoba. FEMS Microbiol. Ecol. 2001, 38, 105-113. (Pubitemid 34084864)
48. Thoms, C.; Horn, M.; Wagner, M.; Hentschel, U.; Proksch, P. Monitoring microbial diversity and natural product profiles of the sponge Aplysina cavernicola following transplantation. Mar. Biol. 2003, 142, 685-692. (Pubitemid 36704443)
49. Hoffmann, F.; Rapp, H.T.; Reitner, J. Monitoring microbial community composition by fluorescence in situ hybridization during cultivation of the marine cold-water sponge Geodia barretti. Mar. Biotechnol. 2006, 8, 373-379. (Pubitemid 44221546)
50. Ilan, M. Reproductive biology, taxonomy, and aspects of chemical ecology of Latrunculiidae (Porifera). Biol. Bull. 1995, 188, 306-312.
51. Kelman, D.; Kashman, Y.; Rosenberg, E.; Ilan, M.; Ifrach, I.; Loya, Y. Antimicrobial activity of the reef sponge Amphimedon viridis from the Red Sea: evidence for selective toxicity. Aquatic Microb. Ecol. 2001, 24, 9-16. (Pubitemid 34235278)
52. Burns, E.; Ifrach, I.; Carmeli, S.; Pawlik, J.R.; Ilan, M. Comparison of anti-predatory defenses of Red Sea and Caribbean sponges. I. Chemical defense. Mar. Ecol. Prog. Ser. 2003, 252, 105-114. (Pubitemid 36599439)
53. Oren, M. Aspects of Sponge Culture for the Production of Bioactive Materials. M.Sc. Thesis, Department of Zoology, Tel Aviv University, Tel Aviv, Israel, 2004.
54. Carmely, S.; Rotem, M.; Kashman, Y. Swinholide A, a new marine macrolide. Complete assignment of the 1H and 13C NMR spectra by 2D NMR techniques. Magn. Res. Chem. 1986, 24, 343-349.
55. Kashman, Y.; Groweiss, A.; Shmueli, U. Latrunculin, a new 2-thiazolidinone macrolide from the marine sponge Latrunculia magnifica. Tetrahedron Lett. 1980, 21, 3629-3632.
56. Schmitz, F.J.; Hollenbeak, K.H.; Campbell, D.C. Marine natural products: Halitoxin, toxic complex of several marine sponges of the genus Haliclona. J. Org. Chem. 1978, 43, 3916-3922. (Pubitemid 9122685)
57. Berlinck, R.G.S.; Ogawa, C.A.; Almeida, A.M.P.; Sanchez, M.A.A.; Malpezzi, E.L.A.; Costa, L.V.; Hajdu, E.; de Freitas, J.C. Chemical and pharmacological characterization of halitoxin from Amphimedon viridis (Porifera) from the southeastern Brazilian coast. Comp. Biochem. Physiol. C 1996, 115, 155-163.
58. Spector, I.; Braet, F.; Shochet, N.R.; Bubb, M.R. New anti-actin drugs in the study of the organization and function of the actin cytoskeleton. Microsc. Res. Tech. 1999, 47, 18-37. (Pubitemid 29474832)
59. Nicolaou, K.C.; Patron, A.P.; Ajito, K.; Richter, P.K.; Khatuya, H.; Bertinato, P.; Miller, R.A.; Tomaszewski, M.J. Total synthesis of Swinholide A, Preswinholide A, and Hemiswinholide A. Chem. A Eur. J. 1996, 2, 847-868. (Pubitemid 26310084)
60. Webster, N.S. Sponge disease: A global threat? Environ. Microbiol. 2007, 9, 1363-1375. (Pubitemid 46763539)
61. Wulff, J.L. Disease prevalence and population density over time in three common Caribbean coral reef sponge species. J. Mar. Biol. Assoc. UK 2007, 87, 1715-1720. (Pubitemid 350211222)
62. Duckworth, A.R.; Battershill, C.N.; Schiel, D.R. Effects of depth and water flow on growth, survival and bioactivity of two temperate sponges cultured in different seasons. Aquaculture 2004, 242, 237-250. (Pubitemid 39584096)
63. Müller, W.E.G.; Wimmer, W.; Schatton, W.; Böhm, M.; Batel, R.; Filic, Z. Initiation of an aquaculture of sponges for the sustainable production of bioactive metabolites in open systems: Example, Geodia cydonium. Mar. Biotechnol. 1999, 1, 569-579. (Pubitemid 30042099)
64. Ferretti, C.; Vacca, S.; Ciucis, C.D.; Marengo, B.; Duckworth, A.R.; Manconi, R.; Pronzato, R.; Domenicotti, C. Growth dynamics and bioactivity variation of the Mediterranean demosponges Agelas oroides (Agelasida, Agelasidae) and Petrosia ficiformis (Haplosclerida, Petrosiidae). Mar. Ecol. 2009, 30, 327-336.
65. Novak, L. Tel Aviv University, Tel Aviv, Israel. Unpublished work, 2011.
66. Webster, N.S.; Negri, A.P.; Munro, M.; Battershill, C.N. Diverse microbial communities inhabit Antarctic sponges. Environ. Microbiol. 2004, 6, 288-300. (Pubitemid 38261027)
67. Thiel, V.; Leininger, S.; Schmaljohann, R.; Brümmer, F.; Imhoff, J.F. Sponge-specific bacterial associations of the Mediterranean sponge Chondrilla nucula (Demospongiae, Tetractinomorpha). Microb. Ecol. 2007, 54, 101-111. (Pubitemid 47036686)
68. Thoms, C.; Hentschel, U.; Schmitt, S.; Schupp, P.J. Rapid tissue reduction and recovery in the sponge Aplysinella sp. Mar. Biol. 2008, 156, 141-153.
69. Bergman, O.; Haber, M.; Mayzel, B.; Anderson, M.A.; Shpigel, M.; Hill, R.T.; Ilan, M. Marine based cultivation of Diacarnus sponges and the bacterial community composition of wild and maricultured sponges and their larvae. Mar. Biotechnol. 2011, doi:10.1007/s10126-011-9391-6.
70. Barthel, D.; Theede, H. A new method for the culture of marine sponges and its application for experimental studies. Ophelia 1986, 25, 75-82.
71. Muyzer, G.; De Waal, E.C.; Uitterlinden, A.G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 1993, 59, 695-700. (Pubitemid 23072343)