Experientia

, Volume 52, Issue 7, pp 716–722

Two classes of metabolites fromTheonella swinhoei are localized in distinct populations of bacterial symbionts

  • C. A. Bewley
  • N. D. Holland
  • D. J. Faulkner
Research Articles

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.

Key words

Aphanocapsa feldmanni Beggiatoa cyanobacteria lithistid sponge Theonella swinhoei secondary metabolites swinholide A symbiosis 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    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.Google Scholar
  2. 2.
    Unson, M. D., and Faulkner, D. J., Experientia49 (1993) 349.Google Scholar
  3. 3.
    Kitigawa, I., Kobayashi, M., Katori, T., Yamashita, M., Tanaka, J., Doi, M., and Ishida, T. J., Am. Chem. Soc.112 (1990) 3710.Google Scholar
  4. 4.
    Bewley, C. A., and Faulkner, D. J., J. org. Chem.59 (1994) 4849.Google Scholar
  5. 5.
    Wilkinson, C. R., Endocytobiology: Endosymbiosis and Cell Biology, p. 553. Eds W. Schwemmler and H. E. A. Schenk. DeGruyter, Berlin 1980.Google Scholar
  6. 6.
    Faulkner, D. J., He, H., Unson, M. D., Bewley, C. A., and Garson, M. J., Gazz. Chim. Ital.123 (1993) 301.Google Scholar
  7. 7.
    Kobayashi, M., Kawazoe, K., Okamoto, T., Sasaki, T., and Kitagawa, I., Chem. pharm. Bull.42 (1994) 19.PubMedGoogle Scholar
  8. 8.
    Paterson, I., Yeung, K. S., Ward, R. A., and Cumming, J. G., J. Am. chem. Soc.116 (1994) 9391.Google Scholar
  9. 9.
    Bubb, M. R., Spector, I., Bershadsky, A. D., and Korn, E. D., J. biol. Chem.270 (1995) 3463.PubMedGoogle Scholar
  10. 10.
    Ishibashi, M., Moore, R. E., Patterson, G. M. L., Xu, C., and Clardy, J., J. org. Chem.51 (1986) 5300.Google Scholar
  11. 11.
    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.Google Scholar
  12. 12.
    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.Google Scholar
  13. 13.
    Carmichael, W. W., Scient. Am.270 (1994) 64.Google Scholar
  14. 14.
    Fusetani, N., and Matsunaga, S., Chem. Rev.93 (1993) 1793.Google Scholar
  15. 15.
    Hinde, R., Pironet, F., and Borowitzka, M. A., Mar. Biol.119 (1994) 99.Google Scholar
  16. 16.
    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.Google Scholar
  17. 17.
    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.Google Scholar
  18. 18.
    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.Google Scholar
  19. 19.
    Sato, T. J., Electron Microsc.17 (1968) 158.Google Scholar
  20. 20.
    Bewley, C. A., Debitus, C. and Faulkner, D. J., J. Am. chem. Soc.116 (1994) 7631.Google Scholar
  21. 21.
    Bewley, C. A., PhD Diss., University of California, San Diego 1995.Google Scholar
  22. 22.
    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.Google Scholar
  23. 23.
    D'Auria, M. V., Paloma, L. G., Minale, L., Zampella, A., Verbist, J. F., Roussakis, C., Debitus, C., and Patissou, J., Tetrahedron50 (1994) 4829.Google Scholar
  24. 24.
    Strohl, W. R., and Larkin, J. M., Appl. environ. Microbiol.36 (1978) 755.Google Scholar
  25. 25.
    Lawry, N. H., Jani, V., and Jensen, T. E., Curr. Microbiol.6 (1981) 71.Google Scholar
  26. 26.
    Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M., and Stanier, R. Y., J. gen. Microbiol.111 (1979) 1.Google Scholar
  27. 27.
    Woese, C. R., Stakebrandt, E., Macke, T. J., and Fox, G. E., Syst. appl. Microbiiol.6 (1985) 143.Google Scholar
  28. 28.
    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.Google Scholar
  29. 29.
    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.Google Scholar
  30. 30.
    Flam, F., Science266 (1994) 1324.PubMedGoogle Scholar

Copyright information

© Birkhäuser Verlag 1996

Authors and Affiliations

  • C. A. Bewley
    • 1
  • N. D. Holland
    • 1
  • D. J. Faulkner
    • 1
  1. 1.Scripps Institution of OceanographyUniversity of California, San DiegoLa JollaUSA

Personalised recommendations