The Prokaryotes pp 3855-3864 | Cite as

Prokaryotic Symbionts of Amoebae and Flagellates

  • Kwang W. Jeon

Abstract

Amoebae and flagellates have long been known to be associated with both extracellular and intracellular symbionts (Hall, 1969; Kirby, 1941 a; Lee et al., 1985). The presence of prokaryotic symbionts on and in flagellates and in some amoebae, as observed by light microscopy, was reported by several authors during the late 1800s and the early part of this century, as was comprehensively reviewed by Kirby (1941a). Symbiont-bearing flagellates were chiefly found in termite guts, and only a few free-living flagellates were found to have adhering symbionts. Hall (1969) extensively reviewed the literature on symbionts of protozoa published since 1941. Both in flagellates and amoebae, the suspected presence of some of the small bacterial symbionts had to be confirmed later by more sophisticated methods such as electron microscopy and specific staining.

Keywords

Symbiotic Bacterium Bacterial Symbiont Endosymbiotic Bacterium Bacterial Endosymbiont Acanthamoeba Castellanii 
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Literature Cited

  1. Ahn, T. I., and Jeon, K. W. 1979. Growth and electron microscopic studies on an experimentally established bacterial endosymbiosis in amoebae. J. Cell. Physiol. 98: 49–58.PubMedCrossRefGoogle Scholar
  2. Ahn, T. I., and Jeon, K. W. 1982. Structural and biochemical characteristics of the plasmalemma and vacuole membranes in amoebae. Exp. Cell Res. 137: 253–268.PubMedCrossRefGoogle Scholar
  3. Armstrong, J. A., and Hart, P. D. 1971. Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J. Exp. Med. 134: 713–740.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Beams, H. W., King, R. L., Thamisian, T. N., and Devine, R. I960. Electron microscope studies on Lophomonas striata with special reference to the nature and position of the striations. J. Protozool. 7: 91–101.Google Scholar
  5. Buchanan, R. E., and Gibbons, N. E. (ed.). 1974. Bergey’s manual of determinative bacteriology, 8th ed. Williams Wilkins, Baltimore.Google Scholar
  6. Cavalier-Smith, T. 1975. The origin of nuclei and of eukaryotic cells. Nature 256: 463–468.CrossRefGoogle Scholar
  7. Chang, K.-P. 1975. Reduced growth of Blastocrithidia culicis and Crithidia oncopelti freed of intracellular symbiotes by chloramphenicol. J. Protozool. 22: 271–276.PubMedCrossRefGoogle Scholar
  8. Chang, K.-P., and Trager, W. 1974. Nutritional significance of symbiotic bacteria in two species of hemoflagellates. Science 183: 532–533.CrossRefGoogle Scholar
  9. Chapman-Andresen, C. 1971. Biology of the large amoebae. Annu. Rev. Microbiol. 25: 27–48.PubMedCrossRefGoogle Scholar
  10. Chapman-Andresen, C., and Hayward, A. F 1963. Bacterial complexes in Amoeba proteus. British-Dutch-Scandinavian Mtg. Soc. Exp. Biol., Oxford, England.Google Scholar
  11. Chesnick, J. M., and Cox, E. R. 1986. Specialization of endoplasmic reticulum architecture in response to a bacterial symbiosis in Peridinium balticum (Pyrrhophyta). J. Phycol. 22: 291–298.CrossRefGoogle Scholar
  12. Choi, E. Y., and Jeon, K. W. 1988. The presence of a spectrin-like protein on symbiosome membranes of symbiont-bearing Amoeba proteus as studied with monoclonal antibodies. Endocyt. Cell Res. 6: 99–108.Google Scholar
  13. Cleveland, L. R., and Grimstone, A. V. 1964. The fine structure of the flagellate Mixotricha paradoxa and its associated micro-organisms. Proc. Roy. Soc. B159: 668–686.CrossRefGoogle Scholar
  14. Cleveland, L. R., Hall, S. R., Sanders, E. P., and Collier, J. 1934. The wood-feeding roach Cryptocercus, its Protozoa and the symbiosis between Protozoa and roach. Am. Acad. Arts Sci. Mem. 17: 185–342.Google Scholar
  15. Cohen, A. I. 1957. Electron microscopic observations of Amoeba proteus in growth and inanition. J. Biophys. Biochem. Cytol. 3: 859–866.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Cross, J. B. 1946. The flagellate subfamily Oxymonadinae. Univ. Calif. Pub. Zool. 53: 67–162.Google Scholar
  17. Dangeard, P. A. 1896. Contribution a l’etude des Acrasiees. Bot. 5: 1–20.Google Scholar
  18. Daniels, E. W. 1973. Ultrastructure, p. 125–169. In: K. W. Jeon, (ed.). The Biology of amoeba. Academic Press, New York.Google Scholar
  19. Daniels, E. W., and Breyer, E. P. 1967. Ultrastructure of the giant amoeba Pelomyxa palustris. J. Protozool. 14: 167–179.CrossRefGoogle Scholar
  20. Daniels, E. W., Breyer, E. P., and Kudo, R. R. 1965. Fine structure of the giant, algae-eating amoeba Pelomyxa palustris. Am. Zool. 5: 734–740.Google Scholar
  21. Daniels, E. W., Breyer, E. P., and Kudo, R. R. 1966. Pelomyxa palustris Greeff II. Its ultrastructure. Z. Zell-forsch. 73: 367–383.Google Scholar
  22. Davis, H. S. 1943. A new polymastigine flagellate, Costia pyriformis, parasitic on trout. J. Parasitol. 29: 385–386.CrossRefGoogle Scholar
  23. Doddema, H., and van der Veer, J. 1983. Crypt. Algol. 4: 89–98.Google Scholar
  24. Drozanski, W. 1963a. Studies of intracellular parasites of free-living amoebae. Acta Microbiol. Pol. 12: 3–8.Google Scholar
  25. Drozanski, W. 1963b. Observations on intracellular infection of amoebae by bacteria. Acta Microbiol. Pol. 12: 924.Google Scholar
  26. Drozanski, W., and Chemielewski, T. 1979. Electron microscopic studies of Acanthamoeba castellanii. Acta Microbiol. Pol. 28: 123–130.Google Scholar
  27. Drozanski, W., Drozanska, D., and Wicinska, M. 1984. The cell wall of the obligate intracellular bacterial parasite of small free-living amoebae. I. Morphology and chemical composition of the rigid layer and peptidoglycan. Acta Microbiol. Pol. 33: 195–206.Google Scholar
  28. Duboscq, O., and Grasse, P.-P. 1926. Les Schizophytes de Devescovina billi n. sp. Compt. Rend. Soc. Biol. Paris 94: 33–34.Google Scholar
  29. Duboscq, O., Grasse, R-P., and Rose, M. 1937. Les flagelles de l’Anacanthotermes ochraceus Sjost du Sud-Algerien. Compt. Rend. Acad. Sci. Paris 205: 574–576.Google Scholar
  30. Freymuller, E., and Camargo, E. P. 1981. Ultrastructural differences between species of trypanosomatids. J. Protozool. 28: 175–182.PubMedCrossRefGoogle Scholar
  31. Gaines, G., and Elbrachter, M. 1987. Heterotrophic nutrition, p. 224–268. In: F. J. R. Taylor (ed.) The biology of dinoflagellates. Blackwell Publications, Oxford.Google Scholar
  32. Geitler, L. 1948. Symbiosen zwischen Chrysomonaden und knospenden bakterien-artigen Organismen sowie Beobachtungen über Organisationseigentümlichkeiten der Chrosomonaden. Österreich. Bot. Zeitschr. 95: 300–324.CrossRefGoogle Scholar
  33. Gerola, F. M., and Bassi, M. 1978. A case of parasitism in Euglena. J. Submicr. Cytol. 10: 261–263.Google Scholar
  34. Gill, J. W., and Vogel, H. J. 1962. Lysine synthesis and phylogeny: biochemical evidence for a bacterial-type endosymbiote in the protozoon Herpetomonas (Strigomonas) oncopelti. Biochim. Biophys. Acta 56: 200–201.PubMedCrossRefGoogle Scholar
  35. Gill, J. W., and Vogel, H. J. 1963. A bacterial endosymbiote in Crithidia (Strigomonas) oncopelti: biochemical and morphological aspect. J. Protozool. 10: 148–152.CrossRefGoogle Scholar
  36. Giovannoni, S. J., DeLong, E. E, Olsen, G. J., and Pace, N. R. 1988. Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial cells. J. Bacteriol. 170: 720–726.PubMedPubMedCentralGoogle Scholar
  37. Goldschmidt, R. 1907. Lebensgeschichte der Mastigamoben, Mastigella vitrea n. sp. und Mastigina setosa n. sp. Arch. Protistenk 1 (Suppl.), 83–168.Google Scholar
  38. Goldstein, L., and Ko, C. 1976. A method for the mass culturing of large free-living amoebas. Methods Cell Biol. 13: 239–246.PubMedCrossRefGoogle Scholar
  39. Gould-Veley, L. J. 1905. A further contribution to the study of Pelomyxa palustris (Greeff). J. Linn. Soc. 29: 374–395.CrossRefGoogle Scholar
  40. Grasse, P. P. 1926. Sur la nature des cotes cuticulaires des Polymastix et Lophomonas striata. Compt. Rend. Soc. Biol. Paris 94: 1014–1015.Google Scholar
  41. Gray, M. W., and Doolittle, W. F. 1982. Has the endosymbiont hypothesis been proven? Microbiol. Rev. 46: 142.Google Scholar
  42. Grimstone, A. V. 1961. The fine structure of Streblomastix strix. Proc. I Int. Congr. Protozool., p. 121.Google Scholar
  43. Gromov, V., Seravin, L. N., and Gerasimova, Z. R 1977. Bacteria-corticae symbionts of Trichonympha turkestanica, a protozoan from the gut tract of termite Hodotermes murgabicus. Mikrobiol. (russ.) 46: 971–973.Google Scholar
  44. Guttman, H. N., and Eisenman, R. N. 1965. “Cure” of Crithidia (Strigomonas) oncopelti of its bacterial endosymbiote. Nature 206:113–114.Google Scholar
  45. Hall, G. H. 1969. Organisms living on and in protozoa, p. 566–718. In: T.-T. Chen (ed.), Research in protozoology, vol. 3. Pergamon Press, London.Google Scholar
  46. Hall, J., and Voelz, H. 1985. Bacterial endosymbionts of Acanthamoeba sp. J. Parasitol. 71: 89–95.PubMedCrossRefGoogle Scholar
  47. Hamburger, B. 1958. Bakteriensymbiose bei Volvox aureus Ehrenberg. Arch. Mikrobiol. 29: 291–310.PubMedCrossRefGoogle Scholar
  48. Han, J. H., and Jeon, K. W. 1980. Isolation and partial characterization of two plasmid DNAs from endosymbiotic bacteria in Amoeba proteus. J. Bacteriol. 141: 1466–1469.PubMedPubMedCentralGoogle Scholar
  49. Jeon, K. W. 1972. Development of cellular dependence on infective organisms: Micrurgical studies in amoebas. Science 176: 1122–1123.PubMedCrossRefGoogle Scholar
  50. Jeon, K. W. 1980. Symbiosis of bacteria with Amoeba, p. 245–262. In: C. B. Cook, P. Pappas, and E. Rudolph (ed.), Cellular interactions in symbiotic and parasitic relationships. Ohio State University Press, Columbus.Google Scholar
  51. Jeon, K. W. 1983. Integration of bacterial endosymbionts in amoebae. Int. Rev. Cytol. Suppl. 14: 29–47.Google Scholar
  52. Jeon, K. W. 1986. Bacterial endosymbionts as extrachromosomal elements in Amoebas, p. 363–371. In: R. B. Wickner, A. Hinnebusch, A. Labowitz, I. C. Gunsalus, and A. Hollaender (ed.), Extrachromosomal elements in lower eukaryotes. Plenum Press, New York.CrossRefGoogle Scholar
  53. Jeon, K. W. 1987. Change of cellular “pathogens” into required cell components. Ann. N. Y. Acad. Sci. 503: 359–371.PubMedCrossRefGoogle Scholar
  54. Jeon, K. W., and Ahn, T. I. 1978. Temperature sensitivity: A cell character determined by obligate endosymbionts in amoebas. Science 202: 635–637.PubMedCrossRefGoogle Scholar
  55. Jeon, K. W., and Hah, J. C. 1977. Effect of chloramphenicol on bacterial endosymbiotes in a strain of Amoeba proteus. J. Protozool. 24: 289–293.PubMedCrossRefGoogle Scholar
  56. Jeon, K. W., and Jeon, M. S. 1975. Cytoplasmic filaments and cellular wound healing in Amoeba proteus. J. Cell Biol. 67: 243–249.PubMedPubMedCentralCrossRefGoogle Scholar
  57. Jeon, K. W., and Jeon, M. S. 1976. Endosymbiosis in amoebae: Recently established endosymbionts have become required cytoplasmic components. J. Cell. Physiol. 89: 337–347.PubMedCrossRefGoogle Scholar
  58. Jeon, K. W., and Jeon, M. S. 1982. Experimental cross-infection of Chaos carolinensis with endosymbiotic bacteria from Amoeba proteus. J. Protozool.. 29: 493A.Google Scholar
  59. Jeon, K. W., and Lorch, I. J. 1967. Unusual intra-cellular bacterial infection in large, free-living amoebae. Exp. Cell Res. 48: 236–240.PubMedCrossRefGoogle Scholar
  60. Kim, H. B., and Jeon, K. W. 1986. Protein synthesis by bacterial endosymbionts in amoebae. Endocyt. Cell Res. 3: 299: 309.Google Scholar
  61. Kim, H. B., and Jeon, K. W. 1987a. A monoclonal antibody against a symbiont-synthesized protein in the cytosol of symbiont-dependent amoebae. J. Protozool. 34: 393–397.CrossRefGoogle Scholar
  62. Kim, H. B., and Jeon, K. W. 1987b. Actin-like protein accumulated within symbiont-containing vesicles of amoebae as studied using a monoclonal antibody. Endocyt. Cell Res. 4: 151–166.Google Scholar
  63. Kirby, H. 1932. Protozoa in termites of genus Armitermes. Parasitol. 24: 289–304.CrossRefGoogle Scholar
  64. Kirby, H. 1936. Two polymastigote flagellates of the genera Pseudodevescovina and Cauduceia. Quart. J. Micros. Sci. 79: 309–335.Google Scholar
  65. Kirby, H. 1938a. The devescovinid flagellates Caduceia theobromae Franca, Pseudodevescovina ramosa new species, and Macrotrichomanas pulchra Grassi. Univ. Calif. Pub. Zool. 43: 1–40.Google Scholar
  66. Kirby, H. 1938b. Polymastigote flagellates of the genus Foaina Janicki, and two new genera Crucinympha and Bulanympha. Quarterly J. Micros. Sci. 81: 1–25.Google Scholar
  67. Kirby, H. 194la. Organisms living on and in protozoa, p. 1009–1013. In: G. N. Calkins and F. M. Summers, (ed). Protozoa in biological research. Columbia Univ. Press, New York.Google Scholar
  68. Kirby, H. 194lb. Devescovinid flagellates of termites. I. The genus Devescovina. Univ. Calif. Pub. Zool. 45: 1–92.Google Scholar
  69. Kirby, H. 1942a. Devescovinid flagellates of termites. II. The genera Caduceia and Macrotrichomonas. Univ. Calif. Pub. Zool. 45: 93–166.Google Scholar
  70. Kirby, H. 1942b. Devescovinid flagellates of termites. II. The genera Foaina and Parajoenia. Univ. Calif. Pub. Zool. 45: 167–246.Google Scholar
  71. Kirby, H. 1944. The structural characteristics and nuclear parasites of some species of Trichonympha in termites. Univ. Calif. Pub. Zool. 49: 185–282.Google Scholar
  72. Kirby, H. 1946. Gigantomonas herculea Dogiel, a polymastigote flagellate with flagellated and amoeboid phases of development. Univ. Calif. Pub. Zool. 53: 163–226.Google Scholar
  73. Kirby, H. 1949. Devscovinid flagellates of termites. V. The genus Hyperdevescovina, the genus Bullanympha, and undescribed or unrecorded species. Univ. Calif. Pub. Zool. 53: 319–422.Google Scholar
  74. Kochert, G., and Olson, L. W. 1970. Endosymbiotic bacteria in Volvox carteri. Trans. Am. Micros. Soc. 89: 475–478.CrossRefGoogle Scholar
  75. Koidzumi, M. 1921. Studies on the intestinal Protozoa found in the termites of Japan. Parasitol. 13: 235–309.CrossRefGoogle Scholar
  76. Krylov, M. V., Podlipaev, S. A., Khaetskii, A. S., Belova, L. M., Frolov, A. O., Niyazbekova, and B. Ya. 1985. Is only one species present in a culture of Crithidia oncopelti kinetoplastmonada trypanosomatidae? Zool. Zh. 64: 165–171.Google Scholar
  77. Lauterborn, R. 1916. Die sapropelische Lebewelt. Ein Beitrag zur Biologie des Faulschlammes naturlicher Gewasser. Verh. Naturwis. Ver. Heidelberg 13: 395–481.Google Scholar
  78. Lee, J. J., and Fredrick, J. E (ed). 1987. Endocytobiology III, vol. 503, Ann. N.Y. Acad. Sci. N.Y. Academy of Sciences, New York.Google Scholar
  79. Lee, J. J., Soldo, A. T., Lee, M. J., Reisser, W., Jeon, K. W., and Gortz, H.-D. 1985. The extent of algal and bacterial endosymbiosis in protozoa. J. Protozool. 32: 391–403.CrossRefGoogle Scholar
  80. Leiner, M., and Wohlfeil, W. 1953. Pelomyxa palustris Greeff und ihre symbiontischen Bakterien. Arch. Protistenk. 98: 227–286.Google Scholar
  81. Lorch, I. J., and Jeon, K. W. 1980. Resuscitation of amoebae deprived of essential symbiotes: Micrurgical studies. J. Protozool. 27: 423–426.CrossRefGoogle Scholar
  82. Lorch, I. J., and Jeon, K. W. 1981. Rapid induction of cellular strain specificity by newly acquired cytoplasmic components in amoebas. Science 211: 949–951.PubMedCrossRefGoogle Scholar
  83. Lorch, I. J., and Jeon, K. W. 1982. Nuclear lethal effect and nucleocytoplasmic incompatibility induced by endosymbionts in Amoeba proteus. J. Protozool. 29: 468–470.CrossRefGoogle Scholar
  84. Margulis, L. 1970. Origin of eukaryotic cells. Yale Univ. Press, New Haven.Google Scholar
  85. Margulis, L. 1981. Symbiosis and cell evolution. W. H. Freeman, San Francisco.Google Scholar
  86. Mackinnon, D. L. 1914. Observations on amoebae from the intestine of the crane-fly larva, Tipula sp. Arch. Protistenk. 32: 267–277.Google Scholar
  87. McLaughlin, G. L., and Cain, G. D. 1985a. Cell surface proteins of symbiotic and aposymbiotic strains of Crithidia oncopelti and Blastocrithidia culicis. Comp. Biochem. Physiol. 82B: 469–477.Google Scholar
  88. McLaughlin, G. L., and Cain, G. D. 1985b. Characterization of whole-cell and organelle protein synthesis in normal and aposymbiotic strains of Crithidia oncopelti and Blastocrithidia culicis. Comp. Biochem. Physiol. 82B: 479–486.CrossRefGoogle Scholar
  89. McLaughlin, G. L., Wood, D. L., and Cain, G. D. 1983. Lipids and carbohydrates in symbiotic and aposymbiotic Crithidia oncopelti and Blastocrithidia culicis. Comp. Biochem. Physiol. 76B: 143–152.CrossRefGoogle Scholar
  90. Moulder, J. W. 1979. The cell as an extreme environment. Proc. Roy. Soc. Lond. B204: 199–210.CrossRefGoogle Scholar
  91. Nagler, K. 1910. Fakultative parasitische Micrococcen in Amoben. Arch. Protistenk. 19: 246–254.Google Scholar
  92. NMewton, B. A. 1956. A synthetic growth medium for the trypanosomid flagellate Strigomonas (Herpetomonas) oncopelti. Nature 177: 279–280.CrossRefGoogle Scholar
  93. Newton, B. A. 1957. Nutritional requirements and biosynthetic capabilities of the parasitic flagellate Strigomonas oncopelti. J. Gen. Microbiol. 17: 708–717.PubMedCrossRefGoogle Scholar
  94. Newton, B. A., and Home, R. W. 1957. Intracellular structures in Strigomonas oncopelti. I. Cytoplasmic structures containing ribonucleoprotein. Exp. Cell Res. 13: 563–574.Google Scholar
  95. Novey, F. G., McNeal, W. J., and Torrey, H. N. 1907. The trypanosomes of mosquitoes and other insects. J. Infect. Dis. 4: 223–276.CrossRefGoogle Scholar
  96. Nurse, E. M. 1945. Protozoa from New Zealand termites. Trans. Roy. Soc. N.Z. 74: 305–314.Google Scholar
  97. Park, M. S., and Jeon, K. W. 1988. A symbiont gene coding for a protein required for the host amoeba: Cloning and expression in phage-transformed E. coli. Endocyt. Cell Res. 5: 215–224.Google Scholar
  98. Park, M. S., and Jeon, K. W. 1989. Nucleotide sequence of a symbiont gene coding for a protein required for the host amoeba. Endocyt. Cell Res. 7: 37–44.Google Scholar
  99. Penard, E. 1902. Faune rhizopodique du bassin du Leman. H. Koundig, Geneva.Google Scholar
  100. Proca-Ciobanu, M., Lupascu, G. H., Petrovic, A. L., and Ionescu, M. D. 1975. Electron microscopic study of a pathogenic Acanthamoeba castellanii strain. The presence of bacterial endosymbionts. Int. J. Parasitol. 5: 49–54.PubMedCrossRefGoogle Scholar
  101. Radchenko, A. I. 1983. Morphology and ultrastructure of the euglenoid flagellate Peranema trichophorum. Tsitol. 25: 141–147.Google Scholar
  102. Raff, R. A., and Mahler, H. R. 1972. The non-symbiotic origin of mitochondria. Science 177: 575–582.PubMedCrossRefGoogle Scholar
  103. Roth, E., Jeon, K., and Stacey, G. 1988. Homology in endosymbiotic systems: The term “Symbiosome,” p. 220–225. In: Molecular genetics of plant-microbe interactions. R. Palacios and D. P. S. Verma (ed.), APS Press, St. Paul, MN.Google Scholar
  104. Roth, L. E. 1959. An electron-microscope study of the cytology of the protozoan Peranema trichophorum. J. Protozool. 6: 107–116.CrossRefGoogle Scholar
  105. Roth, L. E., and Daniels, E. W. 1961. Infective organisms in the cytoplasm of Amoeba proteus. J. Biophys. Biochem. Cytol. 9: 317–323.PubMedPubMedCentralCrossRefGoogle Scholar
  106. Sagan, L. 1967. On the origin of mitosing cells. J. Theoret. Biol. 14: 225–275.CrossRefGoogle Scholar
  107. Skuja, H. 1958. Eine neue vorwiegend sessil oder rhizopodial aufretende synbakteriotische Polytomee aus einem Schwefelgewasser. Sven. Bot. Tidkr. 52: 379–390.Google Scholar
  108. Sousa-Silva, E., and Franca, S. 1985. The association dinoflagellate-bacteria: Their ultrastructural relationship in two species of dinoflagellates. Protistol. 21: 429–446.Google Scholar
  109. Steidinger, S. A., and Baden, D. G. 1984. Toxic marine dinoflagellates, p. 201–262. In: D. L. Spector (ed.), Dinoflagellates. Academic Press, New York.CrossRefGoogle Scholar
  110. Sutherland, J. L. 1933. Protozoa from Australian termites. Quart. J. Micros. Sci. 76: 145–173.Google Scholar
  111. Taylor, F. J. R. 1974. Implications and extensions of the serial endosymbiosis theory of the origin of eukaryotes. Taxon 23: 229–258.CrossRefGoogle Scholar
  112. Trager, W. 1959. The enhanced folic and folinic acid contents of erythrocytes infected with malaria parasites. Exp. Parasitol. 8: 265–273.PubMedCrossRefGoogle Scholar
  113. Tschermak-Woess, E. 1950. Über eine Synbakteriose und ähnliche Symbiosen. Oesterreich. Bot. Zeitschr. 97: 188–206.CrossRefGoogle Scholar
  114. Turner, J. B., and Friedmann, E. I. 1974. Fine structure of capitular filaments in the coenocytic green alga Penicillus. J. Phycol. 10: 125–134.Google Scholar
  115. Uzzell, T., and Spolsky, C. 1974. Mitochondria and plastids as endosymbionts: a revival of special creation ? Am. Sci. 62: 334–343.PubMedGoogle Scholar
  116. Uzzell, T., and Spolsky, C. 1981. Two data sets: Alternative explanations and interpretations. Ann. N.Y. Acad. Sci. 361: 481–499.PubMedCrossRefGoogle Scholar
  117. van Bruggen, J. J. A., Stumm, C. K., and Vogels, G. D. 1983. Symbiosis of methanogenic bacteria and sapropelic protozoa. Arch. Microbiol. 136: 89–95.CrossRefGoogle Scholar
  118. van Bruggen, J. J. A., Stumm, C. K., Zwart, K. B., and Vogels, G. D. 1985. Endosymbiotic methanogenic bacteria of the sapropelic amoeba Mastigella. EEMS Microbiol. Ecol. 31: 187–192.Google Scholar
  119. Watson, J. D., Hopkins, N. H., Roberts, J. W., Steiz, J. A., and Weiner, A. M. 1987. Molecular biology of the gene, 4th ed. p. 1154–1155. Benjamin Cummins, Menlo Park, CA.Google Scholar
  120. Wenyon, C. M. 1907. Observations on Protozoa in the in- testine of mice. Arch. Protistenk. Suppl. 1: 169–201.Google Scholar
  121. Wilcox, L. W. 1986. Prokaryotic endosymbionts in the chloroplast stroma of the dinoflagellate Woloszynskia pascheri. Protoplasma 135: 71–79.CrossRefGoogle Scholar
  122. Wolstenholme, D. R., and Plaut, W. 1964. Cytoplasmic DNA synthesis in Amoeba proteus III. Further studies on the nature of the DNA-containing elements. J. Cell Biol. 22: 505–513.PubMedPubMedCentralCrossRefGoogle Scholar

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  • Kwang W. Jeon

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