Skip to main content
Log in

The toxic symbiontCaedibacter caryophila in the cytoplasm ofParamecium novaurelia

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Endosymbiotic bacteria were observed to inhabit the cytoplasm of the freshwater ciliateParamecium novaurelia. Transmission electron microscopy and toxicity tests with sensitive paramecia showed that the endosymbionts belong to the genusCaedibacter. The bacteria conferred a killer trait to their host paramecia. The production of a proteinaceous inclusion body (“R-body”) in the bacterial cell makes them toxic to other paramecia after they become enclosed in food vacuoles. R-bodies ofCaedibacter sp were associated with phages, which are known in most otherCaedibacter species to code for the R-body proteins. The killer-effect ofP. novaurelia on sensitiveP. caudatum strains was of the “paralysis” type, which is a characteristic of the symbiont speciesCaedibacter caryophila. Until nowC. caryophila was known to inhabit the macronucleus ofParamecium caudatum only. Sequencing of the 16S rRNA-gene proved thatCaedibacter sp from the cytoplasm ofP. novaurelia belongs to the speciesC. caryophila as well. The rDNA-sequence of 1695 bp length differed in a total of only 1 bp from the corresponding gene inC. caryophila from the macronucleus ofP. caudatum. The results indicate that the infection of specific host cell compartments may depend on host genes, but not on different traits of the infecting symbiont species. The occurrence of killer and sensitive paramecia strains together in one pond is discussed with respect to the competitive advantage of the killer trait.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Referrnces

  1. Austin ML (1948) The killing substance, paramecin: activity of single particles. Am Nat 82:51–59

    Article  PubMed  CAS  Google Scholar 

  2. Austin ML (1948) The killing action and rate of production of single particles of paramecin 51. Physiol Zool 21:69–86

    PubMed  CAS  Google Scholar 

  3. Görtz, H-D (1996) Symbiosis in ciliates. In: Hausmann, K, Bradbury PC (eds) Ciliates: Cells as organisms. Gustav Fischer Verlag, Stuttgart, pp. 441–462

    Google Scholar 

  4. Görtz H-D, Wiemann M (1989) Route of infection of the bacteriaHolospora elegans andHolospora obtusa into the nuclei ofParamecium caudatum. Europ J Protistol 24:101–109

    Google Scholar 

  5. Heruth DP, Pond FR, Dilts JA, Quackenbush RL (1994) Characterization of genetic determinants for R body synthesis and assembly inCaedibacter taeniospiralis 47 and 116. J Bacteriol 176:3559–3567

    PubMed  CAS  Google Scholar 

  6. Kusch J (1998) Local and temporal distribution of different genotypes of pond-dwellingStentor coeruleus. Protist 149:147–154

    Article  Google Scholar 

  7. Kusch J, Heckmann K (1996) Population-structure ofEuplotes cilites revealed by RAPD-fingerprinting. Écoscience 3:378–384

    Google Scholar 

  8. Landis WG (1981) The ecology, role of the killer trait, and interactions of five species of theParamecium aurelia complex inhabiting the littoral zone. Can J Zool 59:1734–1743

    Article  Google Scholar 

  9. Landis WG (1986) The interplay among ecology, breeding systems, and genetics in theParamecium aurelia andParamecium bursaria complexes. In: Corliss JO, Patterson DJ (eds) Progress in Protistology, vol. 1. Biopress Ltd, Bristol, pp 287–307

    Google Scholar 

  10. Landis WG (1987) Factors determining the frequency of the killer trait within populations of theParamecium aurelia complex. Genetics 115:197–205

    PubMed  CAS  Google Scholar 

  11. Landis WG (1988) Ecology. In: Görtz H-D (ed)Paramecium. Springer Verlag, Berlin, pp 419–436

    Google Scholar 

  12. Mueller JA (1963) Separation of kappa particles with infective activity from those with killing activity and identification of the infective particles inParamecium aurelia. Exp Cell Res 30:492–508

    Article  Google Scholar 

  13. Pond FR, Gibson I, Lalucat, J, Quackenbush RL (1989) Rbody-producing bacteria. Microbiol Rev 53:25–67

    PubMed  CAS  Google Scholar 

  14. Preer Jr JR, Preer LB, Jurand A (1974) Kappa and other endosymbionts inParamecium aurelia. Bacteriol Rev 38:113–163

    PubMed  CAS  Google Scholar 

  15. Quackenbush RL (1988) Endosymbionts of killerParamecia. In: Görtz H-D (ed)Paramecium. Springer Verlag, Berlin, pp 406–418

    Google Scholar 

  16. Quackenbush RL, Burbach JA (1983) Cloning and expression of DNA sequences associated with the killer trait ofParamecium tetraurelia stock 47. Proc Natl Acad Sci USA 80:250–254

    Article  PubMed  CAS  Google Scholar 

  17. Schmidt HJ, Görtz H-D, Quackenbush RL (1987)Caedibacter caryophila sp nov, a killer symbiont inhabiting the macronucleus ofParamecium caudatum. Int J Syst Bacteriol 37:459–462

    Article  Google Scholar 

  18. Schmidt HJ, Pond FR, Görtz H-D (1987) Refractile bodies (R bodies) from the macronuclear killer particleCaedibacter caryophila. J Cell Sci 88:177–184

    Google Scholar 

  19. Schmidt HJ, Görtz H-D, Pond FR, Quackenbush RL (1988) Characterization ofCaedibacter endonucleobionts from the macronucleus ofParamecium caudatum and the identification of a mutant with blocked R-body synthesis. Exp Cell Res 174:49–57

    Article  PubMed  CAS  Google Scholar 

  20. Sonneborn TM (1943) Gene and cytoplasm. I. The determination and inheritance of the killer character in variety 4 ofParamecium aurelia. Proc Natl Acad Sci USA 29:329–338

    Article  PubMed  CAS  Google Scholar 

  21. Sonneborn TM (1959)Kappa and related particles inParamecium. Adv Virus Res 6:229–359

    Article  Google Scholar 

  22. Springer N, Ludwig W, Amann R, Schmidt HJ, Görtz H-D, Schleifer K-H (1993) Occurrence of fragmented 16S rRNA in an obligate bacterial endosymbiont ofParamecium caudatum. Proc Natl Acad Sci USA 90:9892–9895

    Article  PubMed  CAS  Google Scholar 

  23. Stoeck T, Schmidt HJ (1997) Fast and accurate identification of European species of theParamecium aurelia complex by RAPD-fingerprints. Microb Ecol 35:311–317

    Article  Google Scholar 

  24. Tallan I (1959) Factors involved in infection by the kappa particles inParamecium aurelia, syngen 4. Physiol Zool 32:78–89

    Google Scholar 

  25. Tallan I (1961) A cofactor required by kappa in the infection ofParamecium aurelia and its possible action. Physiol Zool 34:1–13

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Kusch.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kusch, J., Stremmel, M., Breiner, H.W. et al. The toxic symbiontCaedibacter caryophila in the cytoplasm ofParamecium novaurelia . Microb Ecol 40, 330–335 (2000). https://doi.org/10.1007/s002480000034

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s002480000034

Keywords

Navigation