Hostname: page-component-745bb68f8f-b95js Total loading time: 0 Render date: 2025-01-10T21:00:41.678Z Has data issue: false hasContentIssue false
  • English
  • Français

In situ studies on the cytochemistry and ultrastructure of a symbiotic marine dinoflagellate

Published online by Cambridge University Press:  11 May 2009

D. L. Taylor
D. L. Taylor
Affiliation:
Department of Zoology, University College of Swansea1
Get access Rights & Permissions [Opens in a new window]

Extract

The intertidal actinian Anemonia sulcata is known to harbour yellow-brown algal symbionts which are similar in appearance to the zooxanthellae of hermatypic, or reef-building, corals and a number of other invertebrate species. The cytochemistry and structural morphology of the zooxanthella has been studied by light and electron microscopy, to help define it taxonomically and to reveal something about its relations with the actinian. These investigations confirm that it is a dinoflagellate and have revealed several structural adaptations which are formed as a result of the peculiar mode of life adopted by this alga. Of significance is the fine structure of the periplast, which may have a considerable bearing upon the type of relationship which can exist between the host and its symbiont. These findings are discussed in terms of other known instances of algal-invertebrate symbiosis.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 48 , Issue 2 , June 1968 , pp. 349 - 366
Copyright
Copyright © Marine Biological Association of the United Kingdom 1968

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adams, C. W. M. & Sloper, J. C., 1955. Techniques for demonstrating neurosecretory material in the human hypothalamus. Lancet, Part 1, pp. 651–2.CrossRefGoogle Scholar
Adams, C. W. M. & Sloper, J. C., 1956. The hypothalamic elaboration of posterior pituitary principles in man, the rat and the dog. Histochemical evidence from a performic acid-Alcian blue technique for cystine. J. Endocr., Vol. 13, pp. 221–8.CrossRefGoogle Scholar
Allen, M. B., 1956. Excretion of organic compounds by Chlamydomonas. Arch. Microbiol., Vol. 24, pp. 163–8.Google ScholarPubMed
Ax, P. & Apelt, G., 1965. Die ‘Zooxanthellen’ von Convoluta convoluta (Turbellaria: Acoela) entstehen aus Diatomeen. Erster Nachweis einer Endosymbiose zwischen Tieren und Kieselalgen. Die Naturwissenschaften, Jahrgang 52, Heft 15, pp. 444–6.Google Scholar
Boschma, H., 1925. On the symbiosis of certain Bermuda coelenterates and zooxanthellae. Proc. Am. Acad. Arts Sci., Vol. 60, pp. 451–60.CrossRefGoogle Scholar
Boschma, H., 1926. On the food of reef corals. Proc. Acad. Sci. Amst., Vol. 29, PP. 993–7.Google Scholar
Bouck, G. B., 1965. Fine structure and organelle associations in brown algae. J. Cell Biol., Vol. 26, pp. 528–38.CrossRefGoogle ScholarPubMed
Buchner, P., 1965. Endosymbiosis of Animals with Plant Microorganisms. 909 pp. New York: Interscience Publishers.Google Scholar
Cassellman, W. G. B., 1959. Histochemical Technique. 148 pp. London: Methuen.Google Scholar
Caullery, M., 1952. Parasitism and Symbiosis, pp. 230–235. London: Sidgwick and Jackson.Google Scholar
Chatton, E., 1923. Les Péridiniens parasites des Radiolaires. C. r. Acad. Sci., Paris, T. 177, pp. 1246–9.Google Scholar
Chiba, Y., 1951. Cytochemical studies on chloroplasts. I. Cytological demonstration of nucleic acids in chloroplasts. Cytologia, Vol. 16, pp. 259–64.Google Scholar
Christensen, T., 1965. Systematisk Botanik, nr. 2, Alger. Botanik., Bd. 2, pp. 1–180.Google Scholar
Cotte, J., 1922. Études sur les comportements et les réactions des actinies. Bull. Inst. océanogr. Monaco., T. 410, pp. 1–44.Google Scholar
Crisp, D. J. & Southward, A. J., 1958. The distribution of intertidal organisms along the coasts of the English Channel. J. mar. biol. Ass. U.K., Vol. 37, pp. 157–208.CrossRefGoogle Scholar
Dingle, A. D. & Fulton, C., 1966. Development of the flagellar apparatus of Naegleria. J. Cell Biol., Vol. 31, pp. 43–54.Google Scholar
Dodge, J. D., 1966. The Dinophyceae. In The Chromosomes of Algae (Ed. Godward, M. B. E.), pp. 96–115, London: Edward Arnold.Google Scholar
Dodge, J. D., 1967. Fine structure of the dinoflagellate Aureodinium pigmentosum gen. et sp.nov. Br. phycol. Bull., Vol. 3, pp. 327–37.Google Scholar
Doyle, W. & Doyle, M. M., 1940. The structure of zooxanthellae. Publs Carnegie Instn. No. 517, Papers Tortugas Lab., Vol. 32, pp 127–42.Google Scholar
Dragesco, J. & Hollande, A., 1965. Sur la présence de trichocystes fibreux chez les Péridiniens; leur homologie avec les trichocystes fusiformes Ciliés. C. r. hebd. Séanc. Acad. Sci., Paris, T. 260, pp. 2073–6.Google Scholar
Droop, M. R., 1963. Algae and invertebrates in symbiosis. In Symbiotic Associations (ed. Nutman, P. S. and Mosse, B.), pp. 171–99, Cambridge University Press.Google Scholar
Drum, R. W. & Pankratz, H. S., 1965. Fine structure of an unusual cytoplasmic inclusion in the diatom genus Rhopalodia. Protoplasma, Vol. 60, pp. 141–9.Google Scholar
Echlin, P., 1967. The biology of Glaucosystis nostochinearum I. The morphology and fine structure. Br. phycol. Bull., Vol. 3, pp. 225–41.Google Scholar
Evans, L. V., 1966. Distribution of pyrenoids among some brown algae. J. Cell Sci., Vol. 1, pp. 449–55.Google Scholar
Flaumenhaft, E., Conrad, S. M. & Katz, J. J., 1960. Nucleic acids in some deuterated green algae. Science, Vol. 132, pp. 892–4.CrossRefGoogle ScholarPubMed
Fogg, G. E., 1962. Extracellular products. In Physiology and Biochemistry of the Algae (ed. Lewin, R. A.), pp. 475–93, New York: Academic Press.Google Scholar
Freudenthal, H. D., 1962. Symbiodinium gen.nov. and S. microadriaticum sp.nov., a zooxanthella, taxonomy, life cycle, morphology. J. Protozool., Vol. 9, pp. 45–52.Google Scholar
Fritsch, F. E., 1935. The Structure and Reproduction of the Algae. Vol. 1, 928 pp. Cambridge University Press.Google Scholar
Fritsch, F. E., 1952. Algae in association with heterotrophic and holozoic organisms. Proc. R. Soc., Vol. 139, pp. 85–192.Google Scholar
Geddes, P., 1882. On the nature and functions of the ‘yellow cells’ of radiolarians and coelenterates. Proc. R. Soc. Edinb., Vol. 11, pp. 377–96.Google Scholar
Gibbs, S. P., 1962. Nuclear envelope-chloroplast relationships in algae. J. Cell Biol., Vol. 14, pp. 433–44.Google Scholar
Goreau, T. F., 1961. Problems of growth and calcium decomposition in reef corals. Endeavour, Vol. 20, pp. 69–70.Google Scholar
Goreau, T. F. & Goreau, N. I., 1960. Distribution of labelled carbon in reef building corals with and without zooxanthellae. Science, Vol. 31, pp. 68–9.Google Scholar
Greenwood, A. D., 1964. The structure of chloroplasts in lower plants.Abstracts, 10th Internat. Bot. Congr. Edinburgh, pp. 212–13.Google Scholar
Hall, W. T. & Claus, G., 1963. Ultrastructural studies on the blue-green algal symbiont in Cyanophora paradoxa Korschikoff. J. Cell. Biol., Vol. 19, pp. 551–63.Google Scholar
Hall, W. T. & Claus, G., 1967. Ultrastructural studies on the cyanelles of Glaucocystis nostochinearum Itzigsohn. J. Phycol., Vol. 3, pp. 37–51.Google Scholar
Hovasse, R., 1937. Les zooxanthelles sont des dinoflagellés. C. r. hebd. Séance. Acad. Sci., Paris., T. 205, pp. 1015–18.Google Scholar
Karakashian, S. J., 1966. Quoted from Oschman, J. L., 1966. Development of the symbiosis of Convoluta roscoffensis Graff, and Platymonas sp. J. Phycol., Vol. 2, pp. 105–11.Google Scholar
Kawaguti, S., 1944. On the physiology of reef corals. VII. Zooxanthellae of the reef coral is Gymnodinium sp. Dinoflagellata; its culture in vitro. Palao trop. biol. Stn. Stud., Vol. 2, pp. 675–9.Google Scholar
Kawaguti, S., 1964. Zooxanthellae in the corals are intercellular symbionts. Proc. Japan Acad., Vol. 40, pp. 545–8.CrossRefGoogle Scholar
Kawaguti, S., 1965. An electron microscopic proof for the path of nutritive substances from zooxanthellae to the reef coral tissue. Proc. Japan Acad., Vol. 40, pp. 832–5.Google Scholar
Keeble, F. & Gamble, F., 1907. The origin and nature of the green cells of Convoluta roscoffensis. Q. Jl microsc. Sci., Vol. 51, pp. 167–219.Google Scholar
Kirk, J. T. O. & Tilney-Bassett, R. A. E., 1967. The Plastids: Their Chemistry, Structure, Growth and Inheritance. 608 pp.London and San Francisco: W. H. Freeman and Co.Google Scholar
Klebs, G., 1884. Ein Kleiner Beitrag zur Kenntnis der Peridinien. Bot. Ztg., Vol. 10, pp. 46–7.Google Scholar
Leadbeater, B. & Dodge, J. D., 1966. The fine structure of Woloszynskia micra sp.nov., a new marine dinoflagellate. Br. phycol. Bull., Vol. 3, pp. 1–17.Google Scholar
Leedale, G. F., 1967. Euglenoid Flagellates. 242 pp. London: Prentice Hall.Google Scholar
Manton, I., 1964. Observations on the fine structure of the zoospore and young germling of Stigeoclonium. J. exp. Bot., Vol. 15, pp. 399–411.Google Scholar
Manton, I., 1966a. Some possibly significant structural relations between chloroplasts and other cell components. In Proc. N.A.T.O. Adv. Stud. Inst. (Aberystwyth), Vol. 1 (ed. Goodwin, T. W.), pp. 23–47, London: Academic Press.Google Scholar
Manton, I., 1966b. Further observations on the fine structure of Chrysochromulina chiton, with special reference to the pyrenoid. J. Cell Sci., Vol. 1, pp. 187–92.Google Scholar
Manton, I. & Harris, K., 1966. Observations on the micro-anatomy of the brown flagellate Sphaleromantis tetragonia Skuja with special reference to the flagellar apparatus and scales. J. Linn. Soc. Bot., Vol. 59, pp. 397–403.CrossRefGoogle Scholar
Manton, I. & Parke, M., 1965. Observations on the fine structure of two species of Platymonas with reference to flagellar scales and the mode of origin of the theca. J. mar. biol. Ass., U.K., Vol. 45, pp. 743–54.Google Scholar
Mclaughlin, J. J. A. & Zahl, P. A. (1957). Studies in marine biology. II. In vitro culture of zooxanthellae. Proc. Soc. exp. Biol. Med., Vol. 95, pp. 115–20.Google Scholar
McLaughlin, J. J. A. & Zahl, P. A., 1958. Axenic zooxanthellae from various invertebrate hosts. Proc. N. Y. Acad. Sci., Vol. 77, pp. 55–72.Google Scholar
McLaughlin, J. J. A. & Zahl, P. A., 1962. Axenic cultivation of the dinoflagellate symbiont from the coral Cladocora. Arch. Mikrobiol., Vol. 42, pp. 40–1.CrossRefGoogle Scholar
McLaughlin, J. J. A. & Zahl, P. A., 1966. Endozoic Algae. In Symbiosis (ed. Henry, M. S.), Vol. 1, pp. 257–97. New York: Academic Press.Google Scholar
Mclauglin, J. J. A., Zahl, P. A., Nowak, A. & Marchisotto, J., 1963. Some constituents of zooxanthellae grown in axenic culture. Proc. 1st Internat. Congr. Protozool., Prague. Czech. Acad. Sci., pp. 204–5.Google Scholar
Metzner, H., 1952. Cytochemische Untersuchungen über das Workommen von Nukleinsauren in Chloroplasten. Biol. Zentr., Bd. 71, pp. 257–72.Google Scholar
Muscatine, L., 1967. Glycerol excretion by symbiotic algae from corals and Tridacna and its control by the host. Science, N.Y., Vol. 156, pp. 516–19.CrossRefGoogle ScholarPubMed
Oschman, J. L., 1966. Development of the symbiosis of Convoluta roscoffensis Graff. and Platymonas sp. J. Phycol., Vol. 2, pp. 105–11.CrossRefGoogle ScholarPubMed
Oschman, J. L. & Grey, P. 1965. A study of the fine structure of Convoluta roscoffensis and its endosymbiotic algae. Trans. Am. microsc. Soc, Vol. 84, pp. 368–375CrossRefGoogle Scholar
Park, H. D.Greenblatt, C. L., Mattern, C. F. T. & Merril, C. R., 1967. Some relations between Chlorohydra, its symbionts and some other chlorophyllous forms. J. exp. Zool., Vol. 164, pp. 141–62.Google Scholar
Parke, M. & Manton, I., 1965. Preliminary observations on the fine structure of Prasinocladus marinus. J. mar. biol. Ass. U.K., Vol. 45, pp. 525–36.CrossRefGoogle Scholar
Parke, M. & Manton, I., 1967. The specific identity of the algal symbiont in Convoluta roscoffensis. J. mar. biol. Ass., U.K., Vol. 47, pp. 445–64.Google Scholar
Pearse, A. G. E., 1961. Histochemistry, Theoretical and Applied. 998 pp. London: Churchill.Google Scholar
Pringsheim, E. G., 1955. Die‘gelben zellen’ der Koralle Cladocora. Pubbl. Staz. zool. Napoli, Vol. 27, pp. 5–9.Google Scholar
Pütter, A., 1911. Der StofFwechsel der Aktinien. Z. allg. Physiol., Vol. 12, pp. 297–322.Google Scholar
Ris, H., 1961. Ultrastructure and molecular organization of genetic systems. Can. J. Genet. Cytol., Vol. 3, pp. 95–120.Google Scholar
Ris, H. & Plaut, W., 1962. Ultrastructure of DNA-containing areas in the chloroplast of Chlamydomonas. J. Cell Biol., Vol. 13, pp. 383–91.Google Scholar
Sarfatti, G. & Bedini, C., 1965. The symbiont alga of the flatworm Convoluta psammophila Bekl. Observed at the electron microscope. Caryologia, Vol. 18, pp. 207–23.Google Scholar
Smith, H. G., 1939. The significance of the relationship between Actinians and Zooxanthellae. J. exp. Biol., Vol. 16, pp. 334–45.Google Scholar
Taylor, D. L., 1968. Chloroplasts as symbiotic organelles in the digestive gland of Elysia viridis (Gastropoda: Opisthobranchia). J. mar. biol. Ass., U.K., Vol. 48, pp. 1–15.Google Scholar
Trendelenberg, W., 1909. Versuche über den Gaswechsel bei Symbiose zwischen Alga und Tier. Arch. Anat. Physiol., Vol. 42, pp. 42–70.Google Scholar
Van Tright, H., 1919. A contribution to the physiology of the freshwater sponges (Spongillidae). Tijdschr. ned. dierk. Vereen, Vol. 17, p. 1.Google Scholar
Yonge, C. M., 1930. Studies on the physiology of corals. II. Digestive enzymes. With notes on the speed of digestion by A. G. Nicholls. Scient. Rep. Gt Barrier Reef Exped., Vol. 1, pp. 59–81.Google Scholar
Yonge, C. M., 1936. Mode of life, feeding, digestion and symbiosis with zooxanthellae in the Tridacnidae. Scient. Rep. Gt Barrier Reef Exped., Vol. 1, pp. 283–321.Google Scholar
Younge, C. M., 1940. Biology of reef building corals. Scient. Rep. Gt Barrier Reef Exped., Vol. 1, pp. 353–91Google Scholar
Yonge, C. M., 1960. Algal mutualism. In Marine Biology: Ecology of Invertebrates (ed. Edmundson, W. T.), Vol. 3, pp. 243–52, New York: New York Academy of Sciences.Google Scholar
Yonge, C. M. & Nicholls, A. G., 1931a. Studies on the physiology of corals. V. The effects of starvation, in light and in darkness, on the relationship between corals and zooxanthellae. Scient. Rep. Gt Barrier Reef Exped., Vol. 1, pp. 177–211.Google Scholar
Yonge, C. M. & Nicholls, A. G., 1931 b. Studies on the physiology of corals. IV. The structure, distribution, and physiology of the zooxanthellae. Scient. Rep. Gt Barrier Reef Exped., Vol. 1, pp. 135–76.Google Scholar