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Chapter 18 : Microbes from Marine Sponges: A Treasure Trove of Biodiversity for Natural Products Discovery

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Abstract:

Microbes associated with marine sponges are of interest in marine biotechnology for several reasons. Sponge-associated microbes are a resource for drug discovery. Studies on the diversity of microbes associated with sponges and development of methods to culture additional sponge symbionts are important in order to contribute to the future production of new pharmaceuticals. Of particular importance for natural products discovery is the presence in marine sponges of groups of bacteria such as cyanobacteria and actinomycetes, with a good track record for production of bioactive compounds. More generally, the tremendous diversity of bacteria in marine sponges will remain largely untapped as long as >99% of these bacteria remain uncultured and advances are needed in culturing methods for sponge-derived microbes. Many bioactive compounds of potential pharmaceutical importance have already been obtained from microbes isolated from marine sponges. In the examples given here, sponges are used solely as sources of microbes for screening rather than attempts being made to isolate specific microbes that are producers of bioactive compounds previously characterized from the sponges themselves.

Citation: Hill R. 2004. Microbes from Marine Sponges: A Treasure Trove of Biodiversity for Natural Products Discovery, p 177-190. In Bull A (ed), Microbial Diversity and Bioprospecting. ASM Press, Washington, DC. doi: 10.1128/9781555817770.ch18

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Figure 1

Densely packed bacteria within the mesohyl of ( ).

Citation: Hill R. 2004. Microbes from Marine Sponges: A Treasure Trove of Biodiversity for Natural Products Discovery, p 177-190. In Bull A (ed), Microbial Diversity and Bioprospecting. ASM Press, Washington, DC. doi: 10.1128/9781555817770.ch18
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Image of Figure 2
Figure 2

Neighbor-joining phylogenetic tree from analysis of about 500 bp of 16S rRNA gene sequence from clones obtained from the unidentified Indonesian sponge 01IND 35.The scale bar represents 0.1 substitutions per nucleotide position. Culturable isolates from sponge 35 are boxed. Sequences shown in bold are those whose nearest relatives, based on BLAST searches, are also from sponges.

Citation: Hill R. 2004. Microbes from Marine Sponges: A Treasure Trove of Biodiversity for Natural Products Discovery, p 177-190. In Bull A (ed), Microbial Diversity and Bioprospecting. ASM Press, Washington, DC. doi: 10.1128/9781555817770.ch18
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Figure 3

Structure of halichondrin B.

Citation: Hill R. 2004. Microbes from Marine Sponges: A Treasure Trove of Biodiversity for Natural Products Discovery, p 177-190. In Bull A (ed), Microbial Diversity and Bioprospecting. ASM Press, Washington, DC. doi: 10.1128/9781555817770.ch18
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References

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1. Aicher, T. D.,, K. R. Buszek,, F. G. Fang,, C. J. Forsyth,, S. H. Jung,, Y. Kishi,, P. M. Scola,, D. M. Spero,, and S. K. Yoon. 1992. Total synthesis of halichondrin B and norhalichondrin B. J. Am. Chem. Soc. 114: 3162 3264.
2. Ang, K. K.,, M. J. Holmes,, T. Higa,, M. T. Hamann,, and U. A. Kara. 2000. In vivo antimalarial activity of the beta-carboline alkaloid manzamine. A. Antimicrob. Agents Chemother. 44: 1645 1649.
3. Berthold, R. J.,, M. A. Borowitzka,, and M. A. Mackay. 1982. The ultrastructure of Oscillatoria spongeliae, the blue-green algal endosymbiont of the sponge Dysidea herbacea. Phycologia 21: 327 335.
4. Bewley, C. A.,, and D. J. Faulkner. 1998. Lithistid sponges: star performers or hosts to the stars. Angew. Chem. Int. Ed. 37: 2162 2178.
5. Bewley, C. A.,, N. D. Holland,, and D. J. Faulkner. 1996. Two classes of metabolites from Theonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia 52: 716 722.
6. Borowitzka, M. A.,, R. Hinde,, and F. Pironet,. 1988. Carbon fixation by the sponge Dysidea herbacea and its endosymbiont Oscillatoria spongeliae, p. 151 155. In J. H. Choat,, D. J. Barnes,, M. A. Borowitzka,, J. C. Coll,, P. J. Davies,, P. Flood,, B. G. Hatcher,, D. Hopley,, P. A. Hutchings,, D. Kingsey,, G. R. Orme,, M. Pichón,, P. F. Sale,, P. W. Sammarco,, C. C. Wallace,, C. R. Wilkinson,, E. Wolanski,, and O. Bellwood (ed.), Proceedings of the 6th International Coral Reef Symposium. Symposium Executive Committee, Townsville, Australia.
7. Brauers, G.,, R. A. Edrada,, R. Ebel,, P. Proksch,, V. Wray,, A. Berg,, U. Grafe,, C. Schachtele,, F. Totzke,, G. Finkenzeller,, D. Marme,, J. Kraus,, M. Munchbach,, M. Michel,, G. Bringmann,, and K. Schaumann. 2000. Anthraquinones and betaenone derivatives from the sponge-associated fungus Microsphaeropsis species: novel inhibitors of protein kinases. J. Nat. Prod. 63: 739 745.
8. Burja, A. M.,, and R. T. Full. 2001. Microbial symbionts of the Australian Great Barrier Reef sponge Candidaspongia flabellata. Hydrobiologia 461: 41 47.
9. Chen, F.,, and R. E. Hodson,. 2001. In situ PCR/RT-PCR coupled with in situ hybridization for detection of functional gene and gene expression in prokaryotic cells, p. 409 424. In J. Paul (ed.), Methods in Marine Microbiology. Academic Press, San Diego, Calif.
10. Davidson, S. K.,, and M. G. Haygood. 1999. Identification of sibling species of the bryozoan Bugula neritina that produce different anticancer bryostatins and harbor distinct strains of the bacterial symbiont "Candidatus Endobugula sertula." Biol. Bull. 196: 273 280.
11. Davidson, S. K.,, S. W. Allen,, G. E. Lim,, C. M. Anderson,, and M. G. Haygood. 2001. Evidence for the biosynthesis of bryostatins by the bacterial symbiont "Candidatus Endobugula sertula" of the bryozoan Bugula neritina. Appl. Environ. Microbiol. 67: 4531 4537.
12. Dickey, R. W.,, S. C. Bobzin,, D. J. Faulkner,, F. A. Bencsath,, and D. Andrzejewski. 1990. The identification of okadaic acid from a Caribbean dinoflagellate Prorocentrum concavum. Toxicon 28: 371 377.
13. Draisci, R.,, L. Giannetti,, L. Lucentini,, C. Marchiafava,, K. J. James,, A. G. Bishop,, B. M. Healy,, and S. S. Kelly. 1998. Isolation of a new okadaic acid analogue from phytoplankton implicated in diarrhetic shellfish poisoning. J. Chromatogr. A 798: 137 145.
14. El Sayed, K. A.,, M. Kelly,, U. A. Kara,, K. K. Ang,, I. Katsuyama,, D. C. Dunbar,, A. A. Khan,, and M. T. Hamann. 2001. New manzamine alkaloids with potent activity against infectious diseases. J. Am. Chem. Soc. 123: 1804 1808.
15. Elyakov, G. B.,, T. Kuznetsova,, V. V. Mikhailov,, I. I. Maltsev,, V. G. Voinov,, and S. A. Fedoreyev. 1991. Brominated diphenyl ethers from a marine bacterium associated with the sponge Dysidea sp. Experientia 47: 632 633.
16. Faulkner, D. J. 2002. Marine natural products. Nat. Prod. Rep. 19: 1 48.
17. Faulkner, D. J.,, M. K. Harper,, M. G. Haygood,, C. E. Salomon,, and E. W. Schmidt,. 2000. Symbiotic bacteria in sponges: sources of bioactive substances, p. 107 119. In N. Fusetani (ed.), Drugs from the Sea. Karger, Basel, Switzerland.
18. Friedrich, A. B.,, H. Merkert,, T. Fendert,, J. Hacker,, P. Proksch,, and U. Hentschel. 1999. Microbial diversity in the marine sponge Aplyina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridization (FISH). Mar. Biol. 134: 461 470.
19. Friedrich, A. B.,, I. Fischer,, P. Proksch,, J. Hacker,, and U. Hentschel. 2001. Temporal variation of the microbial community associated with the Mediterranean sponge Aplysina aerophoba. FEMS Microbiol. Ecol. 38: 105 113.
20. Fuerst, J. A.,, R. I. Webb,, M. J. Garson,, L. Hardy,, and H. M. Reiswig. 1999. Membrane-bounded nuclear bodies in a diverse range of microbial symbionts of Great Barrier Reef sponges. Mem. Qld. Mus. 44: 193 203.
21. Fusetani, N.,, K. Shinoda,, and S. Matsunaga. 1993. Cinachyrolide A: a potent cytotoxic macrolide possessing two spiroketals from marine sponge Cinachyra. J. Am. Chem. Soc. 115: 3977 3981.
22. Garson, M. J.,, J. E. Thompson,, R. M. Larsen,, C. N. Battershill,, P. T. Murphy,, and P. R. Bergquist. 1992. Terpenes in sponge cell membranes: cell separation and membrane fractionation studies with the tropical marine sponge Amphimedon sp. Lipids 27: 378 388.
23. Gillespie, D. E.,, S. F. Brady,, A. D. Bettermann,, N. P. Cianciotto,, M. R. Liles,, M. R. Rondón,, J. Clardy,, R. M. Goodman,, and J. Handelsman. 2002. Isolation of antibiotics turbomycin a and B from a metagenomic library of soil microbial DNA. Appl. Environ. Microbiol. 68: 4301 4306.
24. Gillor, O.,, S. Carmeli,, Y. Rahamin,, Z. Fishelson,, and M. Ilan. 2000. Immunolocalization of the toxin latrunculin B within the Red Sea sponge Negombata magnifica (Demospongiae, Latrunculiidae). Mar. Biotechnol. 2: 213 223.
25. Groweiss, A.,, U. Shmueli,, and Y. Kashman. 1983. Marine toxins of Latrunculia magnifica. J. Org. Chem. 48: 3512 3516.
26. Gulavita, N. K.,, S. P. Gunasekera,, and S. A. Pomponi. 1992. Isolation of latrunculin A, 6,7-epoxylatrunculin A, fijianolide A, and euryfuran from a new genus of the family Thorectidae. J. Nat. Prod. 55: 506 508.
27. Hart, J. B.,, R. E. Lili,, S. J. H. Hichford,, J. W. Blunt,, and M. H. G. Munro,. 2000. The halichondrins: chemistry, biology, supply and delivery, p. 134 153. In N. Fusetani (ed.), Drugs from the Sea. Karger, Basel, Switzerland.
28. Haygood, M. G.,, and S. K. Davidson,. 1998. Bacterial symbionts of the bryostatin-producing bryozoan Bugula neritina, p. 281 284. In Y. Le Gal, and H. O. Halvorson (ed.), New Developments in Marine Biotechnology. Plenum, New York, N.Y.
29. Haygood, M. G.,, E. W. Schmidt,, S. K. Davidson,, and D. J. Faulkner. 1999. Microbial symbionts of marine invertebrates: opportunities for microbial biotechnology. J. Mol. Microbiol. Biotechnol. 1: 33 43.
30. Hentschel, U.,, J. Hopke,, M. Horn,, A. B. Friedrich,, M. Wagner,, J. Hacker,, and B. S. Moore. 2002. Molecular evidence for a uniform microbial community in sponges from different oceans. Appl. Environ. Microbiol. 68: 4431 4440.
31. Hill, R. T.,, O. Peraud,, J. J. Enticknap,, and M. T. Hamann. 2002. Molecular analysis of the microbial communities associated with marine sponges: importance for natural products discovery, p. 67 75. In Proceedings of the 2002 International Meeting of the Federation of Korean Microbiological Societies, 22 to 23 October 2002, Millenium Town, Chungcheongbuk-do, Korea. Federation of Korean Microbiology Societies, Korea.
32. Hodson, R. E.,, W. A. Dustman,, R. P. Garg,, and M. A. Moran. 1995. In situ PCR for visualization of microscale distribution of specific genes and gene products in prokaryotic communities. Appl. Environ. Microbiol. 61: 4074 4082.
33. Hooper, J. N. A.,, and R. W. M. Van Soest. 2002. Systema Porifera: A Guide to the Classification of Sponges. Kluwer Academic/Plenum Publishers, New York, N.Y.
34. Hu, J.-F.,, M. T. Hamann,, R. Hill,, and M. Kelly,. 2003. The manzamine alkaloids. In G. A. Cordell (ed.), The Alkaloids. Academic Press, San Diego, Calif.
35. Imamura, N.,, M. Nishijima,, K. Adachi,, and H. Sano. 1993. Novel antimycin antibiotics, urauchimycins A and B, produced by marine actinomycete. J. Antibiot. 46: 241 246.
36. Jensen, P. R.,, and W. Fenical,. 2000. Marine microorganisms and drug discovery: current status and future potential, p. 6 19. In N. Fusetani (ed.), Drugs from the Sea. Karger, Basel, Switzerland.
37. Kakou, Y.,, P. Crews,, and G. J. Bakus. 1987. Dendrolasin and latrunculin A from the Fijian sponge Spongia mycofijiensis and an associated nudibranch Chromodoris lochi. J. Nat. Prod. 50: 482 484.
38. Kelman, D.,, Y. Kashman,, E. Rosenberg,, M. Ilan,, I. Ifrach,, and Y. Loya. 2001. Antimicrobial activity of the reef sponge Amphimedon viridis from the Red Sea: evidence for selective toxicity. Aquat. Microb. Ecol. 24: 9 16.
39. Kobayashi, J.,, and M. Ishibashi. 1993. Bioactive metabolites of symbiotic marine microorganisms. Chem. Rev. 93: 8305 8308.
40. Kobayashi, M., 2000. Search for biologically active substances from marine sponges, p. 46 58. In N. Fusetani (ed.), Drugs from the Sea. Karger, Basel, Switzerland.
41. Lee, Y. K.,, J.-H. Lee,, and H. K. Lee. 2001. Microbial symbiosis in marine sponges. J. Microbiol. 39: 254 264.
42. Lopez, J. V.,, P. J. McCarthy,, K. E. Janda,, R. Willoughby,, and S. A. Pomponi. 1999. Molecular techniques reveal wide phyletic diversity of heterotrophic microbes associated with Discodermia spp. (Porifera: Demospongia). Mem. Qld. Mus. 44: 329 341.
43. Mendola, D., 2000. Aquacultural production of bryostatin 1 and ecteinascidin 743, p. 120 133. In N. Fusetani (ed.), Drugs from the Sea. Karger, Basel, Switzerland.
44. Molinski, T. F. 1993. Marine pyridoacridine alkaloids: structure, synthesis, and biological chemistry. Chem. Rev. 93: 1825 1838.
45. Muller, W. E.,, B. Diehl-Seifert,, C. Sobel,, A. Bechtold,, Z. Kljajic,, and A. Dorn. 1986. Sponge secondary metabolites: biochemical and ultrastructural localization of the antimitotic agent avarol in Dysidea avara. J. Histochem. Cytochem. 34: 1687 1690.
46. Murakami, Y.,, Y. Oshima,, and T. Yasumoto. 1982. Identification of okadaic acid as a toxic component of a marine dinoflagellate Prorocentrum lima. Bull. Jpn. Soc. Sci. Fish. 48: 69 72.
47. Muyzer, G.,, E. C. de Waal,, and A. G. Uitterlinden. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59: 695 700.
48. Nickel, M.,, S. Leininger,, G. Proll,, and F. Brümmer. 2001. Comparative studies on two potential methods for the biotechnological production of sponge biomass. J. Biotechnol. 92: 169 178.
49. Oclarit, J. M.,, H. Okada,, S. Ohta,, K. Kaminura,, Y. Yamaoka,, T. Iizuka,, S. Miyashiro,, and S. Ikegami. 1994. Anti-bacillus substance in the marine sponge, Hyatella species, produced by an associated Vibrio species bacterium. Microbios 78: 7 16.
50. Olson, J. B.,, C. C. Lord,, and P. J. McCarthy. 2000. Improved recoverability of microbial colonies from marine sponge samples. Microb. Ecol. 40: 139 147.
51. Osinga, R.,, J. Tramper,, and R. H. Wijffels. 1999. Cultivation of marine sponges. Mar. Biotechnol. 1: 509 532.
52. Osinga, R.,, R. Kleijn,, E. Groenendijk,, P. Niesink,, J. Tramper,, and R. H. Wijffels. 2001. Development of in vivo sponge cultures: particle feeding by the tropical sponge Pseudosuberites aff. andrewsi. Mar. Biotechnol. 3: 544 554.
53. Pettit, G. R.,, Z. A. Cichacz,, F. Gao,, C. L. Herald,, M. R. Boyd,, J. M. Schmidt,, and J. N. A. Hooper. 1993. Isolation and structure of spongiostatin 1. J. Org. Chem. 58: 1302 1304.
54. Preston, C. M.,, K. Y. Wu,, T. F. Molinski,, and E. F. DeLong. 1996. A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc. Natl. Acad. Sci. USA 93: 6241 6246.
55. Rein, K. S.,, and J. Borrone. 1999. Polyketides from dinoflagellates: origins, pharmacology and biosynthesis. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 124: 117 131.
56. Rinehart, K. L. 2000. Antitumor compounds from tunicates. Med. Res. Rev. 20: 1 27.
57. Rondón, M. R.,, P. R. August,, A. D. Bettermann,, S. F. Brady,, T. H. Grossman,, M. R. Liles,, K. A. Loiacono,, B. A. Lynch,, I. A. MacNeil,, C. Minor,, C. L. Tiong,, M. Gilman,, M. S. Osburne,, J. Clardy,, J. Handelsman,, and R. M. Goodman. 2000. Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl. Environ. Microbiol. 66: 2541 2547.
58. Ruby, E. G.,, and K.-H. Lee. 1998. The Vibrio fischeri-Euprymna scolopes light organ association: current ecological paradigms. Appl. Environ. Microbiol. 64: 805 812.
59. Sakai, R.,, T. Higa,, C. W. Jefford,, and G. Bernardinelli. 1986. Manzamine A: an antitumor alkaloid from a sponge. J. Am. Chem. Soc. 108: 6404 6405.
60. Salomon, C. E.,, T. Deerinck,, M. H. Ellisman,, and D. J. Faulkner. 2001. The cellular localization of dercitamide in the Palauan sponge Oceanapia sagittaria. Mar. Biol. 139: 313 319.
61. Santavy, D. L.,, P. Willenz,, and R. R. Colwell. 1990. Phenotypic study of bacteria associated with the Caribbean sclerosponge, Ceratoporella nicholsoni. Appl. Environ. Microbiol. 56: 1750 1762.
62. Schleper, C.,, E. F. DeLong,, C. M. Preston,, R. A. Feldman,, K. Y. Wu,, and R. V. Swanson. 1998. Genomic analysis reveals chromosomal variation in natural populations of the uncultured psychrophilic archaeon Cenarchaeum symbiosum. J. Bacteriol. 180: 5003 5009.
63. Schmidt, E. W.,, C. A. Bewley,, and D. J. Faulkner. 1998. Theopalauamide, a bicyclic glycopeptide from filamentous bacterial symbionts of the lithistid sponge Theonella swinhoei. J. Org. Chem. 63: 1254 1258.
64. Schmidt, E. W.,, A. Y. Obraztsova,, S. K. Davidson,, D. J. Faulkner,, and M. G. Haygood. 2000. Identification of the antifungal peptide-containing symbiont of the marine sponge Theonella swinhoei as a novel δ -proteobacterium, "Candidatus Entotheonella palauensis." Mar. Biol. 136: 969 977.
65. Schmitz, F. J.,, D. J. Vanderah,, K. H. Hollenbeak,, C. E. L. Enwall,, Y. Gopichand,, P. K. Sengupta,, M. B. Hossain,, and C. van der Helm. 1983. Metabolites from the marine sponge Tedania ignis—a new atisanedial and several known diketopiperazines. J. Org. Chem. 48: 3941 3945.
66. Smith, A. B., III,, M. D. Kaufman,, T. J. Beauchamp,, M. J. LaMarche,, and H. Arimoto. 1999. Gram-scale synthesis of (+)-discodermolide. Org. Lett. 1: 1823 1826.
67. Stierle, A. C.,, J. H. I. Cardellina,, and F. L. Singleton. 1988. A marine Micrococcus produces metabolites ascribed to the sponge Tedania ignis. Experientia 44: 1021.
68. Tachibana, K.,, P. J. Scheuer,, Y. Tsukitani,, H. Kikuchi,, D. van Engen,, J. Clardy,, Y. Gopichand,, and F. J. Schmitz. 1981. Okadaic acid, a cytotoxic polyether from two marine sponges of the genus Halichondria. J. Am. Chem. Soc. 103: 2469 2471.
69. Thompson, J. E.,, K. D. Barrow,, and D. J. Faulkner. 1983. Localization of two brominated metabolites, aerothionin and homoaerothionin, in the spherulous cells of the marine sponge Aplysina fistularis (= Verongia thiona). Acta Zool. 64: 199 210.
70. Unson, M. D.,, N. D. Holland,, and D. J. Faulkner. 1994. A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue. Mar. Biol. 119: 1 11.
71. Uriz, M. J.,, X. Turon,, J. Galera,, and J. M. Tur. 1996. New light on the cell location of avarol within the sponge Dysidea avara (Dendroceratida). Cell Tissue Res. 285: 519 527.
72. Vacelet, J. 1970. Description de cellules à bactéries intranucleaires chez des éponges Verongia. J. Microsc. (Paris) 9: 333 346.
73. Vacelet, J., and C. Donadey. 1977. Electron microscope study of the association between some sponges and bacteria. J. Exp. Mar. Biol. Ecol. 30: 301 314.
74. Vacelet, J.,, E. Vacelet,, E. Gaino,, and M.-F. Gallissian,. 1994. Bacterial attack of spongin skeleton during the 1986-1990 Mediterranean sponge disease, p. 355 362. In R. W. M. van Soest,, T. M. G. van Kempen,, and J. C. Braekman (ed.), Sponges in Time and Space. Balkema, Rotterdam, The Netherlands.
75. Vogel, S. 1977. Current-induced flow through living sponges in nature. Troc. Nati. Acad. Sci. USA 74: 2069 2071.
76. Webster, N. S.,, and R. T. Hill. 2001. The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by an α -Proteobacterium. Mar. Biol. 138: 843 851.
77. Webster, N. S.,, J. E. M. Watts,, and R. T. Hill. 2001a. Detection and phylogenetic analysis of novel crenarchaeote and euryarchaeote 16S rRNA gene sequences from a Great Barrier Reef sponge. Mar. Biotechnol. 3: 600 608.
78. Webster, N. S.,, K. J. Wilson,, L. L. Blackall,, and R. T. Hill. 2001b. Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl. Environ. Microbiol. 67: 434 444.
79. Webster, N. S.,, A. P. Negri,, R. I. Webb,, and R. T. Hill. 2002. A spongin-boring α -proteobacterium is the etiological agent of disease in the Great Barrier Reef sponge Rhopaloeides odorabile. Mar. Ecol. Prog. Ser. 232: 305 309.
80. Wicke, C.,, M. Huners,, V. Wray,, M. Nimtz,, U. Bilitewski,, and S. Lang. 2002. Production and structure elucidation of glycoglycerolipids from a marine sponge-associated Microbacterium species. J. Nat. Prod. 63: 621 626.
81. Wilkinson, C. R. 1978a. Microbial associations in sponges. I. Ecology, physiology and microbial populations of coral reef sponges. Mar. Biol. 49: 161 167.
82. Wilkinson, C. R. 1978b. Microbial associations in sponges. III. Ultrastructure of the in situ associations of coral reef sponges. Mar. Biol. 49: 177 185.
83. Wilkinson, C. R. 1983. Net primary productivity in coral reef sponges. Science 219: 410 412.
84. Wilkinson, C. R. 1987. Significance of microbial symbionts in sponge evolution and ecology. Symbiosis 4: 135 146.
85. Wilkinson, C. R.,, and R. Garrone,. 1980. Nutrition of marine sponges. Involvement of symbiotic bacteria in the uptake of dissolved carbon, p. 157 161. In D. C. Smith, and Y. Tiffon (ed.), Nutrition in the Lower Metazoa. Pergamon Press, Oxford, United Kingdom.
86. Wilkinson, C. R.,, M. Nowak,, B. Austin,, and R. R. Colwell. 1981. Specificity of bacterial symbionts in Mediterranean and Great Barrier Reef sponges. Microb. Ecol. 7: 13 21.
87. Wilkinson, C. R.,, R. Garrone,, and J. Vacelet. 1984. Marine sponges discriminate between food bacteria and bacterial symbionts: electron microscope radioautography and in situ evidence. Proc. R. Soc. Lond. Sect. B. 220: 519 528.
88. Yousaf, M.,, K. A. El Sayed,, K. V. Rao,, C. W. Lim,, J.-F. Hu,, M. Kelly,, F. Franzblau,, O. Peraud,, R. T. Hill,, and M. T. Hamann. 2002. 12.34-Oxamanzamines, novel biocatalytic and natural products from manzamine producing Indo-Pacific sponges. Tetrahedron 58: 7397 7402.
89. Zhu, G.,, M. J. LaGier,, F. Stejskal,, J. J. Millership,, X. Cai,, and J. S. Keithly. 2002. Cryptosporidium parvum: the first protist known to encode a putative polyketide synthase. Gene 298: 79 89.

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