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Specificity in dinomastigote-marine invertebrate symbioses: An evaluation of hypotheses of mechanisms involved in producing specificity

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Cell to Cell Signals in Plant, Animal and Microbial Symbiosis

Part of the book series: NATO ASI Series ((ASIH,volume 17))

Abstract

It is now fairly well recognized that the symbioses between microalgae and invertebrates demonstrate specificity (Trench, 1979, 1987). The realization that specificity existed in such associations was not forthcoming until the specific identities of the interacting organisms were resolved, and this depended to a large extent on the isolation, culture and taxonomic analysis of the algae involved. After isolation and culture of the ‘zoochlorellae’ from the flatworm Convoluta roscoffensis, Parke and Manton (1967) identified the algae as the prasinophyte Tetraselmis (Platymonas) convolutae (Hori et al 1982), and the ‘zooxanthellae’ symbiotic with Convoluta convoluta were identified as the diatom Licmophora sp. by Apelt (1969) after they were isolated and brought into culture. Based on the isolation and culture of symbiotic dinomastigotes, D.L. Taylor (1971, 1974) could distinguish between the amphidinioid and gymnodinioid symbionts.

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References

  • Apelt, G. 1969. Die Symbiose zwischen dem acoelen Trubellar Convoluta convoluta und Diatomen der Gattung Licmophora. Mar. Biol. 3:165–187.

    Article  Google Scholar 

  • Blank, R.J. and Trench, R.K. 1985a. Speciation and symbiotic dinoflagellates. Science 229:656–658.

    Article  PubMed  CAS  Google Scholar 

  • Blank, R.J. and Trench, R.K. 1985b. Symbiodinium microadriaticum: A single species? 5th Int’l. Coral Reef Congr. (Tahiti) 6:113–117.

    Google Scholar 

  • Blank, R.J. and Trench, R.K. 1986. Nomenclature of endosym-biotic dinoflagellates. Taxon 35:286–294.

    Article  Google Scholar 

  • Chang, S.S., Prézelin, B.B. and Trench, R.K. 1983. Mechanisms of photoadaptation in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Mar. Biol. 76:219–229.

    Article  CAS  Google Scholar 

  • Cook, C.B. 1980. Infection of invertebrates with algae. In: Cellular Interactions in Symbiosis and Parasitism, C.B. Cook, P.W. Pappas and E.D. Rudolph (eds.). Ohio State University Press, Columbus. pp. 47–74.

    Google Scholar 

  • Colley, N.J. and Trench, R.K. 1983. Selectivity in phagocytosis and persistence of symbiotic algae by the scyphis-toma stage of the jellyfish Cassiopeia xamachana. Proc. R. Soc. Lond. (B) 219:61–82.

    Article  Google Scholar 

  • Colley, N.J. and Trench, R.K. 1985. Cellular events in the reestablishment of a symbiosis between a marine dinoflagellate and a coelenterate. Cell Tissue Res, 239:93–103.

    Article  Google Scholar 

  • Douglas, A.E. and Huss, V.A.R. 1986. On the characteristics and taxonomic position of symbiotic Chlorella. Arch. Microbiol. 145:80–84.

    Article  Google Scholar 

  • Douglas, A.E. and Smith, D.C. 1984. The green hydra symbiosis. VIII. Mechanisms in symbiont regulation. Proc. R. Soc. Lond. (B) 221:291–319.

    Article  Google Scholar 

  • Epp, R.W. and Lewis, W.M. Jr. 1981. Photosynthesis in copepods. Science 214:1349–1350.

    Article  PubMed  CAS  Google Scholar 

  • Pitt, W.K. and Trench, R.K. 1983. Endocytosis of the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal by endodermal cells of the scyphistomae of Cassiopeia xamachana and resistance of the algae to host digestion. J. Cell Sci. 64:195–212.

    Google Scholar 

  • Freudenthal, H.D. 1962. Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella. Taxonomy, life cycle and morphology. J. Protozool. 9:45–52.

    Google Scholar 

  • Holland, A. and Carré, D. 1974. Lex Xanthelles des Radiolaires sphaerocollides, des Acanthaires et de Velella velella. Infrastructure-cytochemie-taxonomie. Protistologica 10:573–601.

    Google Scholar 

  • Hori, T., Norris, R.E. and Chihara, M. 1982. Studies on the ultrastructure and taxonomy of the genus Tetraselmis (Prasinophyceae). I. Subgenus Tetraselmis. Bot. Mag. Tokyo 95:49–61.

    Article  Google Scholar 

  • Jolley, E. and Smith, D.C. 1980. The green hydra symbiosis. II. The biology of the establishment of the association. Proc. R. Soc. Lond. (B) 207:311–333.

    Article  Google Scholar 

  • Loeblich, A.R. 1984. Dinoflagellate evolution. In: Dinoflagellates, D.L. Spector (ed.). Academic Press, New York, London, pp. 481–552.

    Google Scholar 

  • Loeblich, A.R. and Sherley, J.L. 1979. Observations on the theca of the motile phase of free-living and symbiotic Zooxanthella microadriatica (Freudenthal) comb. nov. J. mar. biol. Ass. U.K. 59:195–206.

    Article  Google Scholar 

  • McAuley, P.J. and Smith, D.C. 1982. The green hydra symbiosis. V. Stages in the intracellular recognition of algal symbionts by digestive cells. Proc. R. Soc. Lond. (B) 216:7–23.

    Article  Google Scholar 

  • McNeil, P.L. 1981. Mechanisms of nutritive endocytosis. I. Phagocytic versatility and cellular recognition in Chlorohydra digestive cells; a scanning electron microscopic study. J. Cell Sci. 49:311–339.

    PubMed  CAS  Google Scholar 

  • McNeil, P.L. and Smith, D.C. 1982. The green hydra symbiosis. IV. Entry of symbionts into digestive cells. Proc. R. Soc. Lond. (B) 216:1–6.

    Article  Google Scholar 

  • Meints, R.H. and Pardy, R.L. 1980. Quantitative demonstration of cell surface involvement in a plant-animal symbiosis: lectin inhibition of reassociation. J. Cell Sci. 52:243–269.

    Google Scholar 

  • Muscatine, L. 1967. Glycerol excretion by symbiotic algae from corals and Tridacna and its control by the host. Science 156:516–519.

    Article  PubMed  CAS  Google Scholar 

  • Muscatine, L. 1973. Nutrition of corals. In: Biology and Geology of Coral Reefs, Vol. II. O.A. Jones and R. Endean (eds.). Academic Press, New York. pp. 77–115.

    Google Scholar 

  • Muscatine, L. and Cernichiari, E. 1969. Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol. Bull. 137:506–523.

    Article  CAS  Google Scholar 

  • Muscatine, L., Cook, C.B., Pardy, R.L. and Pool, R.R. 1975. Uptake, recognition and maintenance of symbiotic Chlorella by Hydra viridis. Symp. Soc. Exp. Biol. 29:175–203.

    PubMed  Google Scholar 

  • Muscatine, L. and McAuley, P.J. 1982. Transmission of symbiotic algae to eggs of green hydra. Cytobios 33:111–124.

    PubMed  CAS  Google Scholar 

  • Pardy, R.L. and Muscatine, L. 1973. Recognition of symbiotic algae by Hydra viridis. A quantitative study of the uptake of living algae by aposymbiotic H. viridis. Biol Bull. 145:565–579.

    Article  Google Scholar 

  • Parke, M. and Manton, I. 1967. The specific identity of the algal symbiont of Convoluta roscoffensis. J. mar. biol. Ass. U.K. 47:445–464.

    Article  Google Scholar 

  • Pool, R.R. 1979. The role of algal antigenic determinants in the recognition of algal symbionts by Chlorohydra. J. Cell Sci. 35:367–379.

    PubMed  Google Scholar 

  • Pool, R.R. and Muscatine, L. 1980. Phagocytic recognition and the establishment of Hydra viridis-Chlorella symbiosis. Endocytobiology Vol. I. W. Schwemmler and H.E.A. Schenk (eds.). Walter de Gruyter & Co. Berlin, New York. pp. 225–238.

    Google Scholar 

  • Provasoli, L., Yamasu, T. and Manton, I. 1968. Experiments on the resynthesis of symbiosis in Convoluta rescoffensis with different flagellate cultures. J . mar, biol. Ass. U.K. 48:456–479.

    Google Scholar 

  • Rahat, M. and Reich, V. 1987. A reevaluation of alleged requirements for the establishment of alga/hydra symbioses and host/symbiont specificity — preadaptation and vacuolar ecology. Symbiosis (in press).

    Google Scholar 

  • Reisser, W., Radunz, A. and Wiessner, W. 1982. Participation of algal surface structures in the cell recognition process during infection of aposymbiotic Paramecium bursaria with symbiotic Chlorella. Cytobios. 33:39–50.

    PubMed  CAS  Google Scholar 

  • Schoenberg, D.A. and Trench, R.K. 1980a. Genetic variation in Symbiod inium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. I. Isoenzyme and soluble protein patterns of axenic cultures of S. microadriaticum. Proc. R. Soc. Lond. (B) 207:405–427.

    Article  CAS  Google Scholar 

  • Schoenberg, D.A. and Trench, R.K. 1980b. Genetic variation in Symbiod inium (=Gymnod inium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. III. Specificity and infectivity of S. microadriaticum. Proc. R. Soc. Lond. (B) 207:445–460.

    Article  Google Scholar 

  • Smith, D.C. 1981. The role of nutrient exchange in recognition between symbionts. Ber. Deutsch. Bot. Ges. 94:517–528.

    Google Scholar 

  • Spero, H.J. 1982. Phagotrophy in Gymnodinium fungiforme (Pyrrhophyta); the peduncle as an organelle of ingestion. J. Phycol. 18:356–360.

    Article  Google Scholar 

  • Spero, H.J. 1987. Symbiosis in the planktonic foraminifer Orbulina universa and the isolation of its symbiotic dinoflagellate Gymnodinium béii, sp. nov. J. Phycol. (in press).

    Google Scholar 

  • Stanley, G.D. Jr. 1981. Early history of scleractinian corals and its geological consequences. Geol. 9:507–511

    Article  Google Scholar 

  • Thorington, G. and Margulis, L. 1980. Transmission of the algae and bacterial symbionts of green hydra through the host sexual cycle. Endocytobiology Vol. I. W. Schwemmler and H.E.A. Schenk (eds.). Walter de gruyter & Co. Berlin and New York. pp. 175–222.

    Google Scholar 

  • Taylor, D.L. 1971. On the symbiosis between Amphidinium klebsii (Dinophyceae) and Amphiscolops langerhansi (Turbellaria, Acoela). J. mar. biol. Ass. U.K. 51:301–313.

    Article  Google Scholar 

  • Taylor, D.L. 1973. The cellular interactions of algal-invertebrate symbioses. Adv. Mar. Biol. 11:1–56.

    Article  Google Scholar 

  • Taylor, D.L. 1974. Symbiotic algae: taxonomy and biological fitness. In: Symbiosis in the Sea, C.B.W. Vernberg, (ed.). University of South Carolina Press, Columbia. pp. 254–262.

    Google Scholar 

  • Taylor, P.J.R. 1980. On dinoflagellate evolution. Bio Systems 13:65–108.

    Article  PubMed  CAS  Google Scholar 

  • Trench, R.K. 1971a. The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. I. The assimilation of photosynthetic products of zooxanthellae by two marine coelenterates. Proc. R. Soc. Lond. (B) 177:225–235.

    Article  CAS  Google Scholar 

  • Trench, R.K. 1971b. The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. II. Liberation of fixed 14C by zooxanthellae in vitro. Proc. R. Soc. Lond. (B) 177:237–250.

    Article  CAS  Google Scholar 

  • Trench, R.K. 1979. The cell biology of plant-animal symbioses. Ann. Rev. Plant Physiol. 30:485–532.

    Article  CAS  Google Scholar 

  • Trench, R.K. 1980. Uptake, retention and function of chloroplasts in animal cells. Endocytobiology, Vol. I. W. Schwemmler and H.A.E. Schenk, (eds.). Walter de Gruyter & Co. Berlin, New York. pp. 703–727.

    Google Scholar 

  • Trench, R.K. 1987. Dinoflagellates in non-parasitic symbioses. In: The Biology of Dinoflagellates. F.J.R. Taylor (ed.). Blackwell, Oxford. pp. 531–570.

    Google Scholar 

  • Trench, R.J. and Blank, R.J. 1987. Symbiodinium microadriaticum Freudenthal, S. goreauii, sp. nov.? S. kawagutii, sp. nov., and S. pilosum sp. nov.? gymnodinioid dinoflagellate symbionts of marine invertebrates. J. Phycol. (in press).

    Google Scholar 

  • Trench, R.K., Colley, N.J. and Pitt, W.K. 1981. Recognition phenomena in symbioses between marine invertebrates and zooxanthellae? uptake, sequestration and persistence. Ber. Deutsch. Bot. Ges. 94:529–545.

    CAS  Google Scholar 

  • Trench, R.K. and Winsor, H. 1987. Symbiosis with dinoflagellates in two pelagic flatworms, Amphiscolops sp. and Haplodiscus sp. Symbiosis 3:1–22.

    Google Scholar 

  • Weis, D.S. 1981. Further tests for the hypothesis that algal maltose excretion and cell surface ligands are signals in the infection of Paramecium bursaria by Chlorella. Ber. Deutsch. Bot. Ges. 94:547–556.

    Google Scholar 

  • Wulff, J.L. 1985. Clonal organisms and the evolution of mutualism. In: Population Biology and Evolution of Clonal Organisms, J.B.C. Jackson, L.W. Buss and R.E. Cook (eds.). Yale University Press, New Haven. pp. 437–466.

    Google Scholar 

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© 1988 Springer-Verlag Berlin Heidelberg

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Trench, R.K. (1988). Specificity in dinomastigote-marine invertebrate symbioses: An evaluation of hypotheses of mechanisms involved in producing specificity. In: Scannerini, S., Smith, D., Bonfante-Fasolo, P., Gianinazzi-Pearson, V. (eds) Cell to Cell Signals in Plant, Animal and Microbial Symbiosis. NATO ASI Series, vol 17. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-73154-9_23

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  • DOI: https://doi.org/10.1007/978-3-642-73154-9_23

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