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Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host

Abstract

Aerobic and aerotolerant organisms have evolved defenses against the toxic effects of molecular oxygen1. One protective mechanism involves the breakdown of the harmful superoxide radical by the enzyme superoxide dismutase (SOD). However, levels of oxygen elevated only slightly above normal atmospheric (P O2 of 159 mm Hg) may overpower a cell's defense systems2–4. Although most animals do not naturally encounter oxygen pressures above 1 atm, hyperbaric oxygen levels normally occur in the tissues of marine animals that harbour intracellular algal symbionts, which in light generate more oxygen than is consumed by the combined host and symbionts5–10. We have now found that sea anemones Anthopleura elegantissima (Brandt) containing zooxanthellae (the symbiotic dinoflagellate Symbiodinium microadriaticum) in their gastrodermal tissues have SOD activities nearly two orders of magnitude greater than individuals totally lacking zooxanthellae.

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References

  1. Halliwell, B. Cell Biol. int. Rep. 2, 113–128 (1978).

    Article  CAS  Google Scholar 

  2. Fridovich, I. Science 27, 462–466 (1977).

    Google Scholar 

  3. Yagi, K. & Ohishi, N. in Biochemical and Medical Aspects of Active Oxygen (eds Hayaishi, O. & Asada, K.) 299–307 (University of Tokyo Press, Tokyo, 1977).

    Google Scholar 

  4. Barthelemy, L., Beland, A. & Chastel, C. Resp. Physiol. 44, 261–268 (1978).

    Article  Google Scholar 

  5. Pearse, V. B. Biol. Bull. 147, 641–651 (1974).

    Article  Google Scholar 

  6. Wethey, D. S. & Porter, J. W. in Coelenterate Ecology and Behavior (ed. Mackie, G. O.) 59–66 (Plenum, New York, 1976).

    Book  Google Scholar 

  7. Crossland, C. J. & Barnes, D. J. Mar. Biol. 40, 185–194 (1977).

    Article  CAS  Google Scholar 

  8. Svoboda, A. & Porrmann, T. in Nutrition in the Lower Metazoa (eds Smith, D. C. & Tiffon, Y.) 87–99 (Pergamon, New York, 1980).

    Book  Google Scholar 

  9. Trench, R. K., Wethey, D. S. & Porter, J. W. Biol. Bull. 161, 180–198 (1981).

    Article  Google Scholar 

  10. Mangum, C. P. & Johansen, K. Pacific Sci. (in the press).

  11. Trench, R. K. A. Rev. Pl. Physiol. 30, 485–531 (1979).

    Article  CAS  Google Scholar 

  12. Muscatine, L. in Primary Productivity in the Sea (ed. Falkowski, P. G.) 381–402 (Plenum, New York, 1980).

    Book  Google Scholar 

  13. Hill, H. A. O. Ciba Fdn Symp. 65, 5–17 (1979).

    ADS  CAS  Google Scholar 

  14. Halliwell, B. in Superoxide and Superoxide Dismutases (eds Michelson, A. M., McCord, J. M. & Fridovich, I.) 335–349 (Academic, New York, 1977).

    Google Scholar 

  15. Fee, J. A. in Biological and Clinical Aspects of Superoxide and Superoxide Dismutase (eds Bannister, W. H. & Bannister, J. V.) 41–48 (Elsevier, Amsterdam, 1980).

    Google Scholar 

  16. Fridovich, I. Science 201, 875–880 (1978).

    Article  ADS  CAS  Google Scholar 

  17. Roos, D. & Weening, R. S. Ciba Fdn Symp. 65, 225–262, (1979).

    CAS  Google Scholar 

  18. Hassan, H. M. & Fridovich, I. in Enzymic Basis of Detoxication (ed. Jakoby, W. B.) 311–332 (Academic, New York, 1980).

    Book  Google Scholar 

  19. Trench, R. K. Proc. R. Soc. B177, 237–250 (1971).

    ADS  CAS  Google Scholar 

  20. Fitt, W. K. & Pardy, R. L. Mar. Biol. 61, 199–205 (1981).

    Article  Google Scholar 

  21. Asada, K., Kanematsu, S. & Uchida, K. Archs Biochem. Biophys. 179, 243–256 (1977).

    Article  CAS  Google Scholar 

  22. Steele, R. D. J. Zool. Lond. 179, 387–405 (1976).

    Article  Google Scholar 

  23. Muscatine, L., McCloskey, L. R. & Morian, R. E. Limnol. Oceanogr. 26, 601–611 (1981).

    Article  ADS  CAS  Google Scholar 

  24. Pearse, V. B. Biol. Bull. 147, 630–640 (1974).

    Article  Google Scholar 

  25. Fredericks, C. A. Mar. Biol. 38, 25–28 (1976).

    Article  CAS  Google Scholar 

  26. Shick, J. M. & Brown, W. I. J. exp. Zool. 201, 149–155 (1977).

    Article  Google Scholar 

  27. Fridovich, I. & McCord, J. J. biol. Chem. 244, 6049–6055 (1969).

    PubMed  Google Scholar 

  28. Tyler, D. D. Biochem. J. 147, 493–504 (1975).

    Article  CAS  Google Scholar 

  29. Marshall, M. J. & Worsfold, M. Analyt. Biochem. 86, 561–573 (1978).

    Article  CAS  Google Scholar 

  30. Jeffrey, S. W. & Humphrey, G. H. Biochem. Physiol. Pflanzen. 167, 191–194 (1975).

    Article  CAS  Google Scholar 

  31. Yentsch, C. S. & Menzel, D. W. Deep-Sea Res. 10, 221–231 (1963).

    CAS  Google Scholar 

  32. Itzhaki, R. F. & Gill, D. M. Analyt. Biochem. 9, 401–410 (1964).

    Article  CAS  Google Scholar 

  33. Bradford, M. M. Analyt. Biochem. 72, 248–254 (1976).

    Article  CAS  Google Scholar 

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Dykens, J., Shick, J. Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature 297, 579–580 (1982). https://doi.org/10.1038/297579a0

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