The Prokaryotes pp 3865-3890 | Cite as

Prokaryotic Symbionts of Ciliates

  • Klaus Heckmann
  • Hans-Dieter Görtz


Prokaryotes living in ciliates were first noticed over a century ago by J. Müller (1856). Rod-shaped structures were observed in the macro-nuclei and micronuclei of a number of ciliates, and less commonly, in their cytoplasm. In the beginning, it was not clear whether they were parasites or spermatozoa because the micronucleus was considered to be a testis and the macronucleus an ovary, while chromosome filaments and endonuclear symbionts were mistaken for spermatozoa. This view was corrected by Bütschli (1876), who also wrote the first review on parasites in ciliates (Bütschli, 1889). Accounts of early observations of bacteria in protozoa that followed this initial period were reviewed by Kirby (1941), Wichterman (1953), and Ball (1969).


Bacterial Symbiont Methanogenic Bacterium Food Vacuole Infectious Form Killer Strain 
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Literature Cited

  1. Allen, S. L., and T. A. Nerad. 1978. Method for the simultaneous establishment of many axenic cultures of Paramecium. J. Protozool. 25: 134–139.PubMedGoogle Scholar
  2. Bak, A. L., F. T. Black, C. Christiansen, and E. A. Freundt. 1969. Genome size of mycoplasmal DNA. Nature (London) 224: 1209–1210.Google Scholar
  3. Ball, G. H. 1969. Organisms living on and in protozoa, p. 565–718. In T. T. Chen (ed.), Research in protozoology, vol. 3. Pergamon Press, Oxford.Google Scholar
  4. Beale, G. H., and A. Jurand. 1966. Three different types of mate-killer (mu) particle in Paramecium aurelia (syngen 1). J. Cell Sci. 1: 31–34.PubMedGoogle Scholar
  5. Beale, G. H., A. Jurand, and J. R., Preer, Jr. 1969. The classes of endosymbiont of Paramecium aurelia. J. Cell Sci. 5: 65–91.Google Scholar
  6. Bedingfield, G., J. Gibson, and R. W. Home. 1984. A comparative study of the structure of isolated refractile bodies (R-bodies) from Paramecium. I. The effect of treatment with EDTA or EGTA. Micron Microsc. Acta 15: 235–246.Google Scholar
  7. Borchsenius, O. N., J. J. Skoblo, and D. V. Ossipov. 1983. Holospora curviuscula-a new species of macronuclear symbiotic bacteria of Paramecium bursaria. Cytologia 25: 91–97.Google Scholar
  8. Boss, A. 0.-L., O. N. Borchsenius, and D. V. Ossipov. 1987. Pseudolyticum multiflagellatum n. g., n. sp.-A new symbiotic bacterium in the cytoplasm of Paramecium caudatum (Ciliata, Protozoa). Cytologia 29: 94–99.Google Scholar
  9. Bütschli, O. 1876. Studien über die ersten Entwicklungsvorgänge der Eizelle, die Zelltheilung und die Conjugation der Infusorien. Abh. Senckenb. Naturforsch. Ges. 10: 213–464.Google Scholar
  10. Bütschli, O. 1889. Protozoa. Abt. III. Infusoria und System der Radiolaria, p. 1098–2035. In: H. G. Bronn (ed.), Klassen and Ordnungen des Thierreichs, vol. 1. C. E Winter, Leipzig.Google Scholar
  11. Chen, T. T. 1955. Paramecin 34, a killer substance produced by Paramecium bursaria. Proc. Soc. Exp. Biol. Med. 88: 541–543.PubMedGoogle Scholar
  12. Demar-Gervais, C., and J. Genermont. 1976. Recherches génétiques sur Euplotes vannus: les charactères “monstre” et “killer.” J. Protozool. 23 (suppl.): 8A.Google Scholar
  13. Dilts, J. A. 1976. Covalently closed, circular DNA in kappa endosymbionts of Paramecium. Genet. Res. 627: 161–170.Google Scholar
  14. Dilts, J. A. 1986. The importance of the refractile body in expression of the killer trait in Paramecium. In: R. B. Wickner, A. Hinnebusch, A. M. Lambowitz, I. C. Gunsalus and A. Hollaender (ed.), Extrachromosomal dements in lower eukaryotes. Plenum Press, New York.Google Scholar
  15. Dilts, J. A., and R. L. Quackenbush. 1986. A mutation in the R body-coding sequence destroys expression of the killer trait in P. tetraurelia. Science 232: 641–643.PubMedGoogle Scholar
  16. Dini, E, and P. Luporini. 1976. The mate-killer trait in a stock of Euplotes crassus (Dujardin) (Ciliata, Hypotrichida). Monitore Zool. Ital. (N.S.) 10: 15–24.Google Scholar
  17. Dini, F., and R Luporini. 1982. The inheritance of the mate-killer trait in Euplotes crassus (Hypotrichida, Ciliophora). Protistologica 18: 179–184.Google Scholar
  18. Doddema, H. J., and G. D. Vogels. 1978. Improved identification of methanogenic bacteria by fluorescence microscopy. Appl. Environ. Microbiol. 36: 752–754.PubMedPubMedCentralGoogle Scholar
  19. Dorner, R. W. 1957. Stability of paramecin 34 at different temperatures and pH values. Science 126: 1243–1244.PubMedGoogle Scholar
  20. Estève, J.-C. 1978. Une population de type “killer” chez Paramecium caudatum (Ehrenberg). Protistologica 14: 201–207.Google Scholar
  21. Fauré-Fremiet, E. 1909. Sur un cas de symbiose par un infusoir cilié. C.R. Soc. Biol. 67: 113–114.Google Scholar
  22. Fauré-Fremiet, E. 1950a. Ecologie des ciliés psammophiles litteraux. Bull. Biol. France-Belgique 84: 35–75.Google Scholar
  23. Fauré-Fremiet, E. 1950b. Caulobactéries épizoiques associées aux Centrophorella (Cilies holotriches). Bull. Soc. Zool. France 75: 134–137.Google Scholar
  24. Fauré-Fremiet, E. 1951. The marine sand dwelling ciliates of Cape Cod. Biol. Bul. 100: 59–70.Google Scholar
  25. Fauré-Fremiet, E. 1952. Symbionts bactériens des ciliés du genre Euplotes. C.R. Acad. Sci. 235: 402–403.Google Scholar
  26. Favinger, J., R. Stadtwald, and H. Gest. 1989. Rhoa’ospirillum centenum, sp. nov., a thermotolerant cyst-forming anoxygenic photosynthetic bacterium. Antonie van Leeuwenhoek 55: 291–296.Google Scholar
  27. Fenchel, T., T. Perry, and A. Thane. 1977. Anaerobiosis and symbiosis with bacteria in free-living ciliates. J. Protozool. 24: 154–163.PubMedGoogle Scholar
  28. Figueroa-de Soto, V. E., and A. T. Soldo. 1977. Characterization and base sequence homologies of the DNA of xenosomes and related particles. Int. Congr. Protozool., 5th, New York, 339.Google Scholar
  29. Fok. A. K., and R. D. Allen. 1979. Axenic Paramecium caudatum. I. Mass culture and structure. J. Protozool. 26: 463–470.Google Scholar
  30. Fokin, S. I. 1988. A bacterial symbiont of the macronucleus perinuclear space in the ciliate Paramecium duboscqui. Cytologia 30: 632–635.Google Scholar
  31. Fokin, S. I., A. 0.-L. Boss, and D. V. Ossipov, 1987b. Virus-containing cytoplasmic symbiont of the ciliate Paramecium woodruffi. Cytologia 29: 1303–1306.Google Scholar
  32. Fokin, S. I., and D. V. Ossipov. 1986. Pseudocaedobacter glomeratus n. sp.-A cytoplasmic symbiont of the cil- iate Paramecium pentaurelia. Cytologia 28: 1000–1004.Google Scholar
  33. Fokin, S. I., D. V. Ossipov, I. I. Skoblo, M. S. Rautian, and E. V. Sabaneyeva. 1987a. Nonospora macronucleata g. n., sp. n.-A vegetative nucleus symbiont of the ciliate Paramecium caudatum. Cytologia 29: 963–970.Google Scholar
  34. Frankel, J. 1973. Dimensions of control of cortical patterns in Euplotes: the role of pre-existing structure, the clonal life cycle, and the genotype. J. Exp. Zool. 183: 71–94.Google Scholar
  35. Freiburg, M. 1985. Isolation and characterization of macronuclei of Paramecium caudatum infected with the macronucleus-specific bacterium Holospora obtusa. J. Cell Sci. 73: 389–398.PubMedGoogle Scholar
  36. Fujishima, M., and K. Heckmann. 1984. Intra-and inter-species transfer of endosymbionts in Euplotes. J. Exp. Zool. 230: 339–345.Google Scholar
  37. Fujishima, M., and K. Nagahara. 1984. Isolation of endonuclear symbiont Holospora obtusa from mass cultures of Paramecium caudatum. Proc. 55th Ann. Meet. Zool. Soc. Japan, p. 36. Toryokosoku Press, Morioka.Google Scholar
  38. Gellissen, G., and G. Michaelis. 1987. Gene transfer: Mitochondria to nucleus, p. 391–401. In: J. J. Lee, and F. Fredrick (ed.), Endocytobiology III. Ann. N.Y. Acad. Sci. 503Google Scholar
  39. Gibson, I. 1974. The endosymbionts of Paramecium. Crit. Rev. Microbiol. 3: 243–273.Google Scholar
  40. Gibson, I. 1984. A comparison of the refractile bodies (R-bodies) of certain bacteria. III. Nucleotide sequence homologies and R-body function. Micron Microsc. Acta 15: 253–260.Google Scholar
  41. Gibson, I., and G. H. Beale. 1961. Genic basis of the mate-killer trait in Paramecium aurelia stock 540. Genet. Res. 2: 82–91.Google Scholar
  42. Goosen, N. K., A. M. C. Horemans, S. J. W. Hillebrand, C. K. Stumm, and G. D. Vogels. 1988. Cultivation of the sapropelic ciliate Plagiopyla nasuta Stein and isolation of the endosymbiont Methanobacterium formicicum. Arch. Microbiol. 150: 165–170.Google Scholar
  43. Görtz, H.-D. 1981. Ein neues symbiontisches Bakterium in Paramecium sexaurelia. Verh. Dtsch. Zool. Ges. 74: 227.Google Scholar
  44. Görtz, H.-D. 1983. Endonuclear symbionts in ciliates, p. 145–176. In: K. W. Jeon (ed.), Intracellular symbiosis. Supplement 14. Int. Rev. Cytol. Academic Press, New York.Google Scholar
  45. Görtz, H.-D. 1987. Different endocytobionts simultaneously colonizing ciliate cells. Ann. N.Y. Acad. Sci. 503: 261–268.Google Scholar
  46. Görtz, H.-D., N. Ahlers and H. Robenek. 1989. Ultrastructure of the infectious and reproductive forms of Holospora obtusa: A bacterium infecting the macronucleus of Paramecium caudatum. J. Gen Microbiol. 135: 3079–3085.Google Scholar
  47. Görtz, H.-D., and J. Dieckmann. 1980. Life cycle and infectivity of Holospora elegans Hafkine, a micronucleus-specific symbiont of Paramecium caudatum (Ehrenberg). Protistologica 16: 591–603.Google Scholar
  48. Görtz, H.-D., and M. Freiburg. 1984. Bacterial symbionts in the micronucleus of Paramecium bursaria. Endocyt. Cell Res. 1: 37–46.Google Scholar
  49. Görtz, H.-D., M. Freiburg, and M. Wiemann. 1988. Polypeptide differences between infectious and reproductive forms of Holospora obtusa, an endonucleobiotic bacterium in the macronucleus of Paramecium caudatum. Endocyt. Cell Res. 5: 233–244.Google Scholar
  50. Görtz, H.-D., and M. Wiemann. 1987. Colonization of the ciliate Stentor malt iformis by three different endocytobionts. Endocyt. Cell Res. 4: 177–184.Google Scholar
  51. Görtz, H.-D., and M. Wiemann. 1989. Route of infection of the bacteria Holospora elegans and Holospora obtusa into the nuclei of Paramecium caudatum. Eur. J. Protistol. 24: 101–109.PubMedGoogle Scholar
  52. Grimes, G. W., and J. R. Preer, Jr. 1971. Further observation on the correlation between kappa and page-like particles in Paramecium. Genet. Res. 18: 115–116.Google Scholar
  53. Gromov, B. V., and D. V. Ossipov. 1981. Holospora (ex Hafkine 1890) nom. rev., a genus of bacteria inhabiting the nuclei of paramecia. Int. J. Syst. Bacteriol. 31: 348–352.Google Scholar
  54. Hafkine, M.-W. 1890. Maladies infectieuses des paramécies. Ann. Inst. Pasteur (Paris) 4: 148–162.Google Scholar
  55. Heatherington, S. 1934. The sterilization of protozoa. Biol. Bull. 67: 315–321.Google Scholar
  56. Heckmann, K. 1963. Paarungssystem und genabhängige Paarungstypdifferenzierung bei dem hypotrichen Ciliaten Euplotes vannus O. F. Müller. Arch. Protistenk. 106: 393–421.Google Scholar
  57. Heckmann, K. 1975 Omikron, ein essentieller Endosymbiont von Euplotes aediculatus. J. Protozool. 22: 97–104.Google Scholar
  58. Heckmann, K. 1983. Endosymbionts of Euplotes, p. 111–144. In: K. W. Jeon (ed.), Intracellular symbiosis. Supplement 14. Int. Rev. Cytol. Academic Press, New York.Google Scholar
  59. Heckmann, K., and J. Frankel. 1968. Genic control of cor- tical pattern in Euplotes. J. Exp. Zool. 168: 11–38.PubMedGoogle Scholar
  60. Heckmann, K., J. R. Preer, Jr., and W. H. Straetling. 1967. Cytoplasmic particles in the killers of Euplotes minuta and their relationship to the killer substance. J. Protozool. 14: 360–363.Google Scholar
  61. Heckmann, K., and H. J. Schmidt. 1987. Polynucleobacter necessarius gen. nov., sp. nov., an obligately endosymbiotic bacterium living in the cytoplasm of Euplotes aediculatus. Int. J. Syst. Bact. 37: 456–457.Google Scholar
  62. Heckmann, K., H. J. Schmidt, and M. Fujishima. 1986. Omikron and omikron-like endosymbionts of Euplotes, p. 327–335. In: R. B. Wickner, A. Hinnebusch, A. M. Lambowitz, I. C. Gunsalus and A. Hollaender (ed.), Extrachromosomal elements in lower eukaryotes. Plenum Press, New York.Google Scholar
  63. Heckmann, K., R. ten Hagen, and H. -D. Görtz. 1983. Fresh-water Euplotes species with a 9 type 1 cirrus pattern depend upon endosymbionts. J. Protozool. 30: 284–289.Google Scholar
  64. Holtzman, H. E. 1959. A kappa-like particle in a non-killer stock of Paramecium aurelia., syngen 5. J. Protozool. 6 (suppl.): 26.Google Scholar
  65. Jenkins, R. A. 1970. The fine structure of a nuclear envelope associated endosymbiont of Paramecium. J. Gen. Microbiol. 61: 355–359.Google Scholar
  66. Kahl, A. 1933. Ciliata libera et ectocommensalia, p. 29146. In: G. Grimpe and E. Wagler (ed.), Die Tierwelt der Nord-und Ostsee, Teil II. Akad. Verlagsgesellschaft Becker & Erler, Leipzig.Google Scholar
  67. Kahl, A. 1935. Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria). 4. Peritricha und Chonotricha. Nachtrag, p. 806–842. In: F. Dahl (ed.), Die Tierwelt Deutschlands. G. Fischer, Jena.Google Scholar
  68. Kanabrocki, J. A., J. Lalucat, B. J. Cox, and R. L. Quackenbush. 1986. Comparative study of refractile (R) bodies and their genetic determinants: relationship of type 51 R bodies to R bodies produced by Pseudomonas taeniospiralis. J. Bacteriol. 168: 1019–1022.PubMedPubMedCentralGoogle Scholar
  69. Kirby, H., Jr. 1941. Organisms living on and in protozoa, p. 1009–1113. In: G. N. Calkins and E M. Summers (ed.), Protozoa in biological research. Columbia Univ. Press, New York.Google Scholar
  70. Kuhlmann, H. -W., and K. Heckmann. 1989. Adolescence in Euplotes octocarinatus. J. Exp. Zool. 251: 316–328.Google Scholar
  71. Lalucat, J., O. Meyer, E Mayer, R. Pares, and H. G. Schlegel. 1979. R bodies in newly isolated free-living hydrogen-oxydizing bacteria. Arch Microbiol. 121: 9–15.Google Scholar
  72. Lalucat, J., B. Wells, and I. Gibson. 1986. Relationships between R bodies of certain bacteria. Micron. Microsc. Acta 17: 243–245.Google Scholar
  73. Landis, W. G. 1981. The ecology, role of the killer trait, and interactions of five species of the Paramecium aurelia complex inhabiting the littoral zone. Can. J. Zool. 59: 1734–1743.Google Scholar
  74. Landis, W. G. 1987. Factors determining the frequency of the killer trait within populations of the Paramecium aurelia complex. Genetics 115: 197–206.PubMedPubMedCentralGoogle Scholar
  75. Lauterborn, R. 1901. Die “sapropelische” Lebewelt. Zool. Anz. 24: 50–55.Google Scholar
  76. Laval, M. 1970. Présence de bactéries intranucléaires chez Zoothamnium pelagicum. Congr. Intern. Microsc. Electron., 7th, Grenoble, 403–404.Google Scholar
  77. Liebmann, H. 1937. Bakteriensymbiose bei Faulschlammziliaten. Biol. Zbl. 57: 442–445.Google Scholar
  78. Liebmann, H. 1938. Biologie und Chemismus der Bleilochsprerre. Arch. Hydrobiol. 33: 1–81.Google Scholar
  79. Luporini, P. 1974. Killer and autogamous strains of Euplotes crassus Dujardin from the Somalien coast. Monit. Zool. Ital. 5 (suppl.) (N.S.): 129–132.Google Scholar
  80. Meenaghan, H., K. Reilly, B. Wells, and I. Gibson. 1984. A comparison of the refractile bodies (R-bodies) of certain bacteria. II. Effects of pH on the structure. Micron Microsc. Acta 15: 247–252.Google Scholar
  81. Müller, J. 1856. Beobachtungen an Infusorien. Monatsberichte der Berliner Akademie 389–393.Google Scholar
  82. Mueller, J. A. 1963. Separation of kappa particles with infective activity from those with killing activity and identification of the infective particles in Paramecium aurelia. Exp. Cell Res. 30: 492–508.Google Scholar
  83. Müller, M. 1988. Energy metabolism of protozoa without mitochondria. Ann. Rev. Microbiol. 42: 465–488.Google Scholar
  84. Nobili, R., G. Rosati, and E. Verni. 1976. The killer-trait in Euplotes crassus. Boll. Zool. 43: 251–258.Google Scholar
  85. Ossipov, D. V. 1973. Specific infectious specificity of the omega-particles, micronuclear symbiotic bacteria of Paramecium caudatum. Cytologia 15: 211–217.Google Scholar
  86. Ossipov, D. V. 1981. Problems of nuclear heteromorphism in the unicellular organisms. NAUKA, Leningrad.Google Scholar
  87. Ossipov, D. V., and S. A. Podlipaev. 1977. Electron microscope examinations of early stages of infection of Paramecium caudatum by bacterial symbionts of the macronucleus (Iota-bacteria). Acta Protozool. 16: 289–308.Google Scholar
  88. Ossipov, D. V., I. I. Skoblo, O. N. Borchsenius, M. S. Rautian, and S. A. Podlipaev. 1980. Holospora acuminata-a new species of symbiotic bacterium from the micronucleus of the ciliate Paramecium bursaria Focke. Cytologia 22: 922–929.Google Scholar
  89. Ossipov, D. V., I. I. Skoblo, and M. S. Rautian. 1975. Iota-particles, macronuclear symbiotic bacteria of the ciliate Paramecium caudatum clone M115. i-+cta Protozool. 14: 263–280.Google Scholar
  90. Pond, E R., I. Gibson, J. Lalucat, and R. L. Quackenbush. 1989. R-body producing bacteria. Microbiol. Rev. 53: 25–67.PubMedPubMedCentralGoogle Scholar
  91. Preer, J. R., Jr. 1948a. The killer cytoplasmic factor kappa: its rate of reproduction, the number of particles per cell, and its size. Am. Naturalist 82: 35–42.Google Scholar
  92. Preer, J. R., Jr. 1948b. A study of some properties of the cytoplasmic factor “kappa,” in Paramecium aurelia, variety 2. Genetics 33: 349–404.PubMedPubMedCentralGoogle Scholar
  93. Preer, J. R., Jr. 1950. Microscopically visible bodies in the cytoplasm of the “killer” strains of Paramecium au-relia. Genetics 35: 344–362.PubMedPubMedCentralGoogle Scholar
  94. Preer, J. R., Jr. 1977. The killer system in Paramecium- kappa and its viruses. Microbiology 1977: 576–578.Google Scholar
  95. Preer, J. R., Jr. L. A. Hufnagel, and L. B. Preer. 1966. Structure and behavior of “R” bodies from killer paramecia. J. Ultrastr. Res. 15: 131–143.Google Scholar
  96. Preer, J. R., Jr., and A. Jurand. 1968. The relation between virus-like particles and R bodies of Paramecium au-relia. Genet. Res. 12: 331–340.PubMedGoogle Scholar
  97. Preer, J. R., Jr., and L. B. Preer. 1967. Virus-like bodies in killer paramecia. Proc. Natl. Acad. Sci. USA 58: 1. 774–1781.Google Scholar
  98. Preer, J. R., Jr., and L. B. Preer. 1982. Revival of names of protozoan endosymbionts and proposal of Holospora caryophila nom. nov. Int. J. Syst. Bacteriol. 32: 140–141.Google Scholar
  99. Preer, J. R., Jr., and L. B. Preer. 1984. Endosymbionts of protozoa, p. 795–811. In: N. R. Krieg (ed.), Bergey’s manual of systematic bacteriology, vol. 1. Williams and Wilkins, Baltimore.Google Scholar
  100. Preer, J. R., Jr. L. B. Preer, and A. Jurand. 1974. Kappa and other endosymbionts of Paramecium aurelia. Bacteriol. Rev. 38: 113–163.PubMedPubMedCentralGoogle Scholar
  101. Preer, J. R., Jr., L.B. Preer, B. Rudman, and A. Jurand. 1971. Isolation and composition of bacteriophage-like particles from kappa of killer paramecia. Mol. Gen. Genet. 111: 202–208.Google Scholar
  102. Preer, J. R., Jr., and P. Stark. 1953. Cytological observations on the cytoplasmic factor “kappa” in Paramecium au-relia. Exp. Cell Res. 5: 478–491.PubMedGoogle Scholar
  103. Preer, L. B. 1969. Alpha, an infectious macronuclear sym- biont of Paramecium aurelia. J. Protozool. 16: 570–578.PubMedGoogle Scholar
  104. Preer, L. B. 1981. Prokaryotic symbionts of Paramecium, p. 2127–2136. In: M. P. Starr, H. Stolp, H. G. Trüper, A. Balows, H. G. Schlegel (ed.)-,. The prokaryotes, 1st ed.-, Springer-Verlag, New York.Google Scholar
  105. Preer, L. B., A. Jurand, J. R. Preer, Jr., and B. Rudman. 1972. The classes of kappa in Paramecium aurelia. J. Cell Sci. 11: 581–600.Google Scholar
  106. Preer, L. B., and J. R. Preer, Jr. 1964. Killing activity from lysed particles of Paramecium. Genet. Res. 5: 230–239.Google Scholar
  107. Preer, L. B., B. Rudman, and J. R. Preer, Jr. 1974. Induction of R bodies by ultraviolet light in killer paramecia. J. Gen. Microbiol. 80: 209–215.Google Scholar
  108. Quackenbush, R. L. 1978. Genetic relationships among bacterial endosymbionts of Paramecium aurelia: polynucleotide sequence relationships among members of Caedobacter. J. Gen. Microbiol. 108: 181–187.Google Scholar
  109. Quackenbush, R. L. 1982. In: Validation of the publication of new names and new combinations previously effectively published outside the IJSB. List No. 8. Int. J. Syst. Bacteriol. 32:266–268.Google Scholar
  110. Quackenbush, R. L. 1983. Plasmids from bacterial endosymbionts of hump-killer paramecia. Plasmid 9: 298306.Google Scholar
  111. Quackenbush, R. L. 1988. Endosymbionts of killer paramecia, p. 406–418. In H.-D. Görtz (ed.), Paramecium. Springer Verlag, Heidelberg.Google Scholar
  112. Quackenbush, R. L., and J. A. Burbach. 1983. Cloning and expression of DNA sequences associated with the killer trait of Paramecium tetraurelia stock 47. Proc. Natl. Acad. Sci. USA 80: 250–254.PubMedPubMedCentralGoogle Scholar
  113. Quackenbush, R. L., B. J. Cox, and J. A. Kanabrocki. 1986. Extrachromosomal elements of extrachromosomal elements of Paramecium and their extrachromosomal elements, p. 265–278. In: R. B. Wickner, A. Hinnebusch, A. M. Lambowitz, I. C. Gunsalus and A. Hollaender (ed.), Extrachromosomal elements in lower eukaryotes. Plenum Press, New York.Google Scholar
  114. Raikov, I. B. 1971. Bactéries épizoiques et mode de nutrition du cilié psammophile Kentrophoros fistulosum Fauré-Fremiet (étude au microscope électronique). Protistologica 7: 365–378.Google Scholar
  115. Raikov, I. B. 1974. Étude ultrastructurale des bactéries épizoiques et éndozoiques de Kentrophoros latum Raikov, cilié holotriche mésopsammique. Cahiers de Biologie Marine 15: 379–393.Google Scholar
  116. Rosati, G., and E. Verni. 1975. Macronuclear symbionts in Euplotes crassus (Ciliata Hypotrichida). Boll. Zool. 42: 231–232.Google Scholar
  117. Rosati, G., and F. Verni. 1977. Bacteria-like endosymbionts in Euplotes crassus. Int. Congr. Protozool., 5th, New York, 443.Google Scholar
  118. Rosati, G., F Verni, and P. Luporini. 1976. Cytoplasmic bacteria-like endosymbionts in Euplotes crassus (Du-jardin) (Ciliata, Hypotrichida). Monitore Zool. Ital. (N.S.) 10: 449–460.Google Scholar
  119. Ruthmann, A., and K. Heckmann. 1961. Formwechsel und Struktur des Makronucleus von Bursaria truncatella. Arch. Protistenkd. 105: 313–340.Google Scholar
  120. Sauerbrey, E. 1928. Beobachtungen über einige neue oder wenig bekannte marine Ciliaten. Arch. Protistenk. 62: 355–407.Google Scholar
  121. Schmidt, H. J. 1982. Isolation of omikron-endosymbionts from mass cultures of Euplotes aediculatus and characterization of their DNA. Exp. Cell Res. 140: 417–425.PubMedGoogle Scholar
  122. Schmidt, H. J. 1984. Studies on protein synthesis in kappa particles. J. Gen. Microbiol. 130: 1517–1523.Google Scholar
  123. Schmidt, H. J., M. Freiburg, and H.-D. Görtz. 1987a. Comparison of the infectious forms of two bacterial endonucleobionts, Holospora elegans and H. obtusa, from the ciliate Paramecium caudatum. Microbios. 49: 189–197.Google Scholar
  124. Schmidt, H. J., H.-D. Görtz, E R. Pond, and R. L. Quackenbush. 1988. Characterization of Caedibacter endonucleobionts from the macronucleus of Paramecium caudatum and the identification of a mutant with blocked R-body synthesis. Exp. Cell Res. 174: 49–57.PubMedGoogle Scholar
  125. Schmidt, H. J., H.-D. Görtz, and R. L. Quackenbush. 1987c. Caedibacter caryophila. sp. nov., a killer symbiont inhabiting the macronucleus of Paramecium caudatum. Int. J. Syst. Bacteriol. 37: 459–462.Google Scholar
  126. Schmidt, H. J., E R. Pond, and H.-D. Görtz. 1987b. Refractile bodies (R bodies) from the macronuclear killer particle Caedibacter caryophila. J. Cell Sci. 88: 177–184.Google Scholar
  127. Schneller, M. V. 1958. A new type of killing action in a stock of Paramecium aurelia from Panama. Proc. Indian. Acad. Sci. 67: 302.Google Scholar
  128. Schneller, M. V., T. M. Sonneborn, and J. A. Mueller. 1959. The genetic control of kappa-like particles in Paramecium aurelia. Genetics 44: 533–534.Google Scholar
  129. Schönefeld, U., A. W. Alfermann, and J. E. Schultz. 1986. Economic mass cultivation of Paramecium tetraurelia on a 200-liter scale. J. Protozool. 33: 222–225.Google Scholar
  130. Siegel, R. W. 1953. A genetic analysis of the mate-killer trait in Paramecium aurelia, variety 8. Genetics 38: 550–560.PubMedPubMedCentralGoogle Scholar
  131. Siegel, R. W., and K. Heckmann. 1966. Inheritance of autogamy and the killer trait in Euplotes minuta. J. Protozool. 13: 34–48.PubMedGoogle Scholar
  132. Simon, E. M., and M. V. Schneller. 1973. The preservation of ciliated protozoa at low temperature. Cryobiology 10: 421–426.PubMedGoogle Scholar
  133. Skoblo, I. I., O. N. Borchsenius, N. A. Lebedeva, and D. V. Ossipov. 1985. A new species of symbiotic bacteria of Paramecium bursaria, Ciliophora, Protozoa. Cytologia 27: 1292–1297.Google Scholar
  134. Skoblo, I. I., and N. A. Lebedeva. 1986. Infection of the nuclear apparatus of Paramecium bursaria (Ciliata) by the symbiotic bacterium Holospora curviuscula. Cytologia 28: 367–372.Google Scholar
  135. Smith, J. E. 1961. Purification of kappa particles of Paramecium aurelia, stock 51. Am. Zool. 1: 390.Google Scholar
  136. Smith-Sonneborn, J. E., and W. J. Van Wagtendonk. 1964. Purification and chemical characterization of kappa of stock 51, Paramecium aurelia. Exp. Cell Res. 33: 50–59.PubMedGoogle Scholar
  137. Soldo, A. T. 1963. Axenic culture of Paramecium. Some observations on the growth behavior and nutritional requirements of a particle-bearing strain of Paramecium aurelia 299 lambda. Ann. N.Y. Acad. Sci 108: 380–388.PubMedGoogle Scholar
  138. Soldo, A. T. 1974. Intracellular particles in Paramecium, p. 377–442. In: W. J. Van Wagtendonk (ed.), Paramecium-a current survey. Elsevier, Amsterdam, London, New York.Google Scholar
  139. Soldo, A. T. 1983. The biology of the xenosome, an intracellular symbiont, p. 79–109. In: K. W. Jeon (ed.), Intracellular symbiosis, Supplement 14. Int. Rev. Cytol. Academic Press, New York.Google Scholar
  140. Soldo, A. T. 1987. Parauronema acutum and its xenosomes: a model system. J. Protozool. 34: 447–451.Google Scholar
  141. Soldo, A. T., and S. A. Brickson. 1978. Observations on the ultrastructure, mode of infectivity and host range of xenosomes. Tissue and Cell 10: 609–618.PubMedGoogle Scholar
  142. Soldo, A. T., S. A. Brickson, and G. A. Castiglione. 1987. Inclusion bodies in xenosomes purified on percoll gradients as revealed by electron microscopy. J. Protozool. 34: 6–9.Google Scholar
  143. Soldo, A. T., S. A. Brickson, G. A. Castiglione, and A. E. Freytag. 1986a. Association of transformation of xenosomes from nonkiller to killer with extrachromosomal DNA. J. Bacteriol. 168: 96–102.PubMedPubMedCentralGoogle Scholar
  144. Soldo, A. T., S. A. Brickson, and A. Freytag. 1986b. Structure and characterization of extrachromosomal DNA of killer xenosomes, intracellular symbionts of a marine protozoan, p. 291–302. In: R. B. Wickner, A. Hinnebusch, A M Lambowitz, I. C. Gunsalus and A. Hollaender (ed.), Extrachromosomal elements in lower eukaryotes. Plenum Press, New York.Google Scholar
  145. Soldo, A. T., S. A. Brickson, and E Larin. 1983. The size and structure of the DNA genome of symbiont xeno-some particles in the ciliate Parauronema acutum. J. Gen. Microbiol. 129: 1317–1325.PubMedGoogle Scholar
  146. Soldo, A. T., and G. A. Godoy. 1973a. Observations on the production of folic acid by symbiont lambda particles of Paramecium aurelia stock 299. J. Protozool. 20: 502.Google Scholar
  147. Soldo, A. T., and G. A. Godoy. 1973b. Molecular complex- ity of Paramecium symbiont lambda deoxyribonucleic acid: evidence for the presence of a multicopy genome. J. Mol. Biol. 73: 93–108.PubMedGoogle Scholar
  148. Soldo, A. T., and G. A. Godoy. 1974. The molecular complexity of mu and pi symbiont DNA of Paramecium aurelia. Nucleic Acids Res. 1: 387–396.PubMedPubMedCentralGoogle Scholar
  149. Soldo, A. T., G. A. Godoy, and S. A. Brickson. 1974. Infectious particles in a marine ciliate. Nature (London) 249: 284–286.Google Scholar
  150. Soldo, A. T., G. A. Godoy, and W. J. Van Wagtendonk. 1966. Growth of particle-bearing and particle-free Paramecium aurelia in axenic culture. J. Protozool. 13: 492–497.Google Scholar
  151. Soldo, A. T., and W. J. Van Wagtendonk. 1969. The nutrition of Paramecium aurelia, stock 299. J. Protozool. 16: 500–506.PubMedGoogle Scholar
  152. Soldo, A. T., W. J. Van Wagtendonk, and G. A. Godoy. 1970. Nucleic acid and protein content of purified endosymbiote particles of Paramecium aurelia. Biochim. Biophys. Acta 204: 325–333.Google Scholar
  153. Sonneborn, T. M. 1938. Mating types, toxic interactions and heredity in Paramecium aurelia. Science 88: 503.Google Scholar
  154. Sonneborn, T. M. 1943. Gene and Cytoplasm. I. The determination and inheritance of the killer character in variety 4 of P. aurelia. II. The bearing of determination and inheritance of characters in P. aurelia on problems of cytoplasmic inheritance, pneumococcus transformations, mutations and development. Proc. Natl. Acad. Sci. USA 29: 329–343.Google Scholar
  155. Sonneborn, T. M. 1950. Methods in the general biology and genetics of Paramecium aurelia. J. Exp. Zool. 113: 87–148.Google Scholar
  156. Sonneborn, T. M. 1959. Kappa and related particles in Paramecium. Adv. Virus Res. 6: 229–356.Google Scholar
  157. Sonneborn, T. M. 1970. Methods in Paramecium research, p. 241–339. In M. Prescott (ed.), Methods in cell physiology, vol. 4. Academic Press, New York.Google Scholar
  158. Sonneborn, T. M. 1975. The Paramecium aurelia complex of fourteen sibling species. Trans. Am. Microsc. Soc. 94: 155–178.Google Scholar
  159. Sonneborn, T. M., J. A. Mueller, and M. V. Schneller. 1959. The classes of kappa-like particles in Paramecium au-relia. Anat. Rec. 134–642.Google Scholar
  160. Stumm, C. K., H. J. Gijzen, and G. D. Vogels. 1982. Association of methanogenic bacteria with ovine rumen ciliates. Brith. J. Nutr. 47: 95–99.Google Scholar
  161. Stumm, C. K., and G. D. Vogels. 1989. Relations of autotrophic bacteria to protozoa, p. 177–191. In H. G. Schlegel, and B. Bwien (ed.), Autotrophic bacteria. Springer Verlag, Berlin.Google Scholar
  162. Takayanagi, T., and S. Hayashi. 1964. Cytological and cytogenetical studies on Paramecium polycarium. V. Lethal interactions in certain stocks. J. Protozool. 11: 128–132.PubMedGoogle Scholar
  163. Thiele, J., O. Honer-Schmid, J. Wahl, G. Kleefeld, and J. E. Schultz. 1980. A new method for axenic mass cultivation of Paramecium tetraurelia. J. Protozool. 27: 118–121.Google Scholar
  164. Van Bruggen, J. J. A., C. K. Stumm, and G. D. Vogels. 1983. Symbiosis of methanogenic bacteria and sapropelic protozoa. Arch. Mikrobiol. 136: 89–95.Google Scholar
  165. Van Bruggen, J. J. A., K. B. Zwart, J. G. F. Hermans, E. M. Van Hove, C. K. Stumm, and G. D. Vogels. 1986. Isolation and characterization of Methanoplanus endosymbiosus sp. nov., an endosymbiont of the marine sapropelic ciliate Metopus contort us Quennerstedt. Arch. Microbiol. 144: 367–374.Google Scholar
  166. Van Bruggen, J. J. A., K. B. Zwart, R. M. Van Assema, C. K. Stumm, and G. D. Vogels. 1984. Methanobacterium formicicum, an endosymbiont of the anaerobic ciliate Metopus striatus McMurrich. Arch. Microbiol. 139: 17.Google Scholar
  167. Van Wagtendonk, W. J., and A. T. Soldo. 1970. Methods used in the axenic cultivation of Paramecium aurelia, p. 117–130. In D. M. Prescott (ed.), Methods in cell physiology, vol. 4. Academic Press, New York.Google Scholar
  168. Vogels, G. D., W. F. Hoppe, and C. K. Stumm. 1980. Association of methanogenic bacteria with rumen ciliates. Appl. Environ. Microbiol. 40: 608–612.PubMedPubMedCentralGoogle Scholar
  169. Wagener, S., and N. Pfennig. 1987. Monoxenic culture of the anaerobic ciliate Trimyema compressum Lackey. Arch. Microbiol. 149: 4–11.Google Scholar
  170. Wagener, S., Bardele, C. F., and N. Pfennig. 1990. Functional integration of Methanobacterium formicicum into the anaerobic ciliate Trimyema compressum. Arch. Microbiol. 153: 496–501.Google Scholar
  171. Wells, B., and R. W. Home. 1983. The ultrastructure of Pseudomonas avenae II. Intracellular refractile (R body) structure. Micron Microsc. Acta 14: 329–344.Google Scholar
  172. Wichterman, R. 1953. The biology of Paramecium. Plenum Press, New York.Google Scholar
  173. Wiemann. M. 1989. The release of Holospora obtusa from Paramecium caudatum observed with a new device for extended in vivo microscopy. J. Protozool. 36: 176–179.Google Scholar
  174. Wiemann, M., and H.-D. Görtz. 1989. Release of the endonucleobiotic bacterium Holospora elegans from its host cell Paramecium caudatum. Eur. J. Protistol. 25: 100–108.PubMedGoogle Scholar
  175. Yarlett, N., A. C. Hann, D. Lloyd, and A. Williams. 1981. Hydrogenosomes in the rumen protozoon Dasytricha ruminantium Schuberg. Biochem. J. 200: 365–372.PubMedPubMedCentralGoogle Scholar
  176. Zwart, K. B., N. K. Goosen, M. W. Van Schijndel, C. A. M. Broers, C. K. Stumm, and G. D. Vogels. 1988. Cytochemical localization of hydrogenase activity in the anaerobic protozoa Trichomonas vaginales, Plagiopyla nasuta and Trimyema compressum. J. Gen. Microbiol. 134: 2165–2170.Google Scholar

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© Springer Science+Business Media New York 1992

Authors and Affiliations

  • Klaus Heckmann
  • Hans-Dieter Görtz

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