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Symbiosis within a symbiosis: Intracellular bacteria within the endosymbiotic protistNephromyces

Abstract

The marine protistNephromyces Giard, 1888 is a chronic endosymbiont of molgulid tunicates. Ultrastructural and cytochemical studies of this protist, isolated from molgulid hosts collected from the Pacific, Atlantic and Gulf Coasts of the United States, indicate thatNephromyces is itself chronically infected with Gramnegative, intracellular bacteria. Molgulid tunicates are thus the locus of a nested,tripartite endosymbiosis. Intracellular bacteria are present in both trophic and reproductive stages ofNephromyces, suggesting that the bacterial-Nephromyces symbiosis is an hereditary association. The presence of endosymbionts inNephromyces raises the possibility that some ofNephromyces' metabolic characteristics, in particular its high urate oxidase activity, might be supplied not byNephromyces itself, but rather by its intracellular bacteria, possibly functioning as peroxisomal analogues.

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Literature cited

  • Brock, T. D., Madigan, M. T. (1988). Biology of microorganisms. 5th ed. Prentice-Hall, Englewood Cliffs, New Jersey

    Google Scholar 

  • Coleman, A. W., Goff, L. (1991). Algal DNA: a new vista for the phycologist. J. Phycol. 27: (in press)

  • Coleman, A. W., Maguire, M. J., Coleman, J. R. (1981). Mithramycin-and 4′-5-diamidino-2-phenylindole (DAPI)-DNA staining for fluorescence microspectrophotometric measurement of DNA in nuclei, plastids, and virus particles. J. Histochem. Cytochem. 29: 959–968

    Google Scholar 

  • Eisenman, E. A., Alfert, M. (1981). A new fixation procedure for preserving the ultrastructure of marine invertebrate tissues. J. Microscopy 125: 117–120

    Google Scholar 

  • Giard, A. (1888). Sur lesNephromyces, genre nouveau de champignons parasites de rein des Molgulidees. C.r.hebd. Séanc. Acad. Sci., Paris 106: 1180–1182

    Google Scholar 

  • Hammond, S. M., Lambert, P. A., Rycroft, A. N. (1984). The bacterial cell surface. Kapitan Szabo Publishers, Washington, D.C.

    Google Scholar 

  • Login, G. R. (1978). Microwave fixation versus formalin fixation of surgical and autopsy tissue. Am. J. med. Technol. 44: 435–437

    Google Scholar 

  • Margulis, L. (1981). Symbiosis in cell evolution. W. H. Freeman, San Francisco

    Google Scholar 

  • Margulis, L., Schwartz, K. V. (1982). Five kingdoms. W. H. Freeman, San Francisco

    Google Scholar 

  • Rogers, H. J., Perkins, H. R., Ward, J. B. (1980). Microbial cell walls and membranes. Chapman & Hall, London

    Google Scholar 

  • Saffo, M. B. (1982). Distribution of the endosymbiontNephromyces Giard within the ascidian family Molgulidae. Biol. Bull. mar. biol. Lab., Woods Hole 162: 95–104

    Google Scholar 

  • Saffo, M. B. (1983). A new mutualism? the symbiosis of molgulid tunicates with the protistNephromyces. Am. Zool. 23: p. 1006

    Google Scholar 

  • Saffo, M. B. (1988). Nitrogen waste or nitrogen source? Urate degradation in the renal sac of molgulid tunicates. Biol. Bull. mar. biol. Lab., Woods Hole 175: 403–409

    Google Scholar 

  • Saffo, M. B. (1990). Symbiogenesis and the evolution of mutualism: lessons from a tripartite endosymbiosis. In: Margulis, L., Fester, R. (eds.) Symbiosis as a source of evolutionary innovation, MIT Press (in press)

  • Saffo, M. B., Davis, W. (1982). Modes of infection of the ascidianMolgula manhattensis by its endosymbiontNephromyces Giard. Biol. Bull. mar. biol. Lab., Woods Hole 162: 105–112

    Google Scholar 

  • Saffo, M. B., Fultz, S. (1986). Chitin in the symbiotic protistNephromyces. Can. J. Bot. 64: 1306–1310

    Google Scholar 

  • Saffo, M. B., Lowenstam, H. (1978). Calcareous deposits in the renal sac of a molgulid tunicate. Science, N.Y. 200: 1166–1168

    Google Scholar 

  • Saffo, M. B., Nelson, R. (1983). The cells ofNephromyces: developmental stages of a single life cycle. Can. J. Bot. 61: 3230–3239

    Google Scholar 

  • Sieburth, J. M. (1979). Sea microbes. Oxford University Press, New York

    Google Scholar 

  • Smith, D. C. (1979). From extracellular to intracellular: the establishment of a symbiosis. Proc. R. Soc. (Ser. B) 204: 115–130

    Google Scholar 

  • Smith, D. C., Douglas, A. E. (1987). The biology of symbiosis. Edward Arnold, London

    Google Scholar 

  • Smyth, J. D. (1973). Some interface phenomena in parasitic protozoa and platyhelminths. Can. J. Zool. 51: 367–377

    Google Scholar 

  • Soldo, A. T. (1983). The biology of the xenosome, an intracellular symbiont. Int. Rev. Cytol. (Suppl.) 14: 79–109

    Google Scholar 

  • Stanier, R. Y., Doudoroff, M., Adelberg, E. A. (1963). The microbial world. 2nd ed. Prentice-Hall, Englewood Cliffs, New Jersey.

    Google Scholar 

  • Stanier, R. Y., Ingraham, J. L., Wheelis, M. L., Painter, P. R. (1986). The microbial world. 5th ed. Prentice-Hall, Englewood Cliffs, New Jersey

    Google Scholar 

  • Starr, M. P., Schmidt, J. M. (1981). Prokaryote diversity. In: Starr, M. P., Stolp, H., Trüper, H. G., Balows, A., Schlegel, H. G. (eds). The prokaryotes, Vol. 1. Springer-Verlag, Berlin, p. 3–42

    Google Scholar 

  • Surek, B., Melkonian, M. (1983). Intracellular bacteria in the Euglenophyceae: prolonged axenic culture of an algal-bacterial system. In: Schenk, H. E. A., Schwemmler, W. (eds.). Endocytobiology. II. Walter de Gruyter, Berlin, p. 475–486

    Google Scholar 

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Communicated by M. G. Hadfield, Honolulu

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Saffo, M.B. Symbiosis within a symbiosis: Intracellular bacteria within the endosymbiotic protistNephromyces . Mar. Biol. 107, 291–296 (1990). https://doi.org/10.1007/BF01319828

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  • DOI: https://doi.org/10.1007/BF01319828

Keywords

  • United States
  • Oxidase Activity
  • Gulf Coast
  • Reproductive Stage
  • Metabolic Characteristic