Abstract
The marine spongeTheonella swinhoei (lithistid Family Theonellidae, Order Astrophorida) has yielded many important, bioactive natural products, most of which share structural features with bacterial natural products. The presence of microbial symbionts inT. swinhoei has been reported, and it was originally suggested that the cytotoxic macrolide swinholide A and many of the bioactive cyclic peptides fromT. swinhoei were all produced by symbiotic cyanobacteria. By transmission electron microscopy, we found four distinct cell populations to be consistently present inT. swinhoei: eukaryotic sponge cells, unicellular heterotrophic bacteria, unicellular cyanobacteria and filamentous heterotrophic bacteria. Purification and chemical analyses of each cell type showed the macrolide swinholide A to be limited to the mixed population of unicellular heterotrophic bacteria, and an anti-fungal cyclic peptide occurred only in the filamentous heterotrophic bacteria. Contrary to prior speculation, no major metabolites were located in the cyanobacteria or sponge cells.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Yasumoto, T., Murata, M., Oshima, Y., Matsumoto, G. L., and Clardy, J., American Chemical Society Symposium Series, No. 262: Seafood Toxins, p. 207. Ed. E. P. Ragelis. American Chemical Society, Washington DC 1984.
Unson, M. D., and Faulkner, D. J., Experientia49 (1993) 349.
Kitigawa, I., Kobayashi, M., Katori, T., Yamashita, M., Tanaka, J., Doi, M., and Ishida, T. J., Am. Chem. Soc.112 (1990) 3710.
Bewley, C. A., and Faulkner, D. J., J. org. Chem.59 (1994) 4849.
Wilkinson, C. R., Endocytobiology: Endosymbiosis and Cell Biology, p. 553. Eds W. Schwemmler and H. E. A. Schenk. DeGruyter, Berlin 1980.
Faulkner, D. J., He, H., Unson, M. D., Bewley, C. A., and Garson, M. J., Gazz. Chim. Ital.123 (1993) 301.
Kobayashi, M., Kawazoe, K., Okamoto, T., Sasaki, T., and Kitagawa, I., Chem. pharm. Bull.42 (1994) 19.
Paterson, I., Yeung, K. S., Ward, R. A., and Cumming, J. G., J. Am. chem. Soc.116 (1994) 9391.
Bubb, M. R., Spector, I., Bershadsky, A. D., and Korn, E. D., J. biol. Chem.270 (1995) 3463.
Ishibashi, M., Moore, R. E., Patterson, G. M. L., Xu, C., and Clardy, J., J. org. Chem.51 (1986) 5300.
Rinehart, K. L., Harada, K., Namikoshi, M., Chen, C., Harvis, C. A., Munro, M. H. G., Blunt, J. W., Mulligan, P. E., Beasley, V. R., Dahlem, A. M., and Carmichael, W. W., J. Am. chem. Soc.110 (1988) 8557.
Botes D. P., Tuinman, A. A., Wessels, P. L., Viljoen, C. C., Kruger, H., Williams, D. H., santikarn, S., Smith, R. J. and Hammond, S. J., J. chem. Soc., Perkin Trans.I (1984) 2311.
Carmichael, W. W., Scient. Am.270 (1994) 64.
Fusetani, N., and Matsunaga, S., Chem. Rev.93 (1993) 1793.
Hinde, R., Pironet, F., and Borowitzka, M. A., Mar. Biol.119 (1994) 99.
Lewin, R. L., and Cheng, L., Prochloron: A Microbial Enigma, p. 1. Eds R. L. Lewin and L. Cheng. Chapman and Hall, New York, NY 1989.
Moore, R. E., Patterson, G. M. L., and Carmichael, W. W., Memoirs of the California Academy of Sciences, No. 13: Biomedical Importance of Marine Organisms, p. 143. Ed. D. G. Fautin. California Academy of Sciences, San Francisco 1988.
Sollas, W. J., Report on the scientific results of the voyage of H.M.S. Challenger during the years 1873–1876, H. M, S. O., Zoology,25 (1888) 284.
Sato, T. J., Electron Microsc.17 (1968) 158.
Bewley, C. A., Debitus, C. and Faulkner, D. J., J. Am. chem. Soc.116 (1994) 7631.
Bewley, C. A., PhD Diss., University of California, San Diego 1995.
Valeria, M., Paloma, L. G., Minale, L., Zampella, A., Verbist, J. F., Roussakis, C., Debitus, C. Kato, Y. Fusetani, N., Matsunaga, S., and Hashimoto, K., Tetrahedron49 (1993) 8657.
D'Auria, M. V., Paloma, L. G., Minale, L., Zampella, A., Verbist, J. F., Roussakis, C., Debitus, C., and Patissou, J., Tetrahedron50 (1994) 4829.
Strohl, W. R., and Larkin, J. M., Appl. environ. Microbiol.36 (1978) 755.
Lawry, N. H., Jani, V., and Jensen, T. E., Curr. Microbiol.6 (1981) 71.
Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M., and Stanier, R. Y., J. gen. Microbiol.111 (1979) 1.
Woese, C. R., Stakebrandt, E., Macke, T. J., and Fox, G. E., Syst. appl. Microbiiol.6 (1985) 143.
Stahl, D. A., Lane, D. J., Olsen, G. J., Heller, D. J., Schmidt, T. M., and Pace, N. R., Int. J. Syst. Bacteriol.37 (1987) 116.
Moore, R. E., Patterson, C. M. L., Mynderse, J. S., Barchi, J., Norton, T. R., Furusawa, E., and Furusawa, S., Pure appl. Chem.58 (1986) 263.
Flam, F., Science266 (1994) 1324.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bewley, C.A., Holland, N.D. & Faulkner, D.J. Two classes of metabolites fromTheonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia 52, 716–722 (1996). https://doi.org/10.1007/BF01925581
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01925581