Skip to main content

Towards an Understanding of the Killer Trait: Caedibacter endocytobionts in Paramecium

  • Chapter
Book cover Molecular Basis of Symbiosis

Part of the book series: Progress in Molecular and Subcellular Biology ((PMSB,volume 41))

5 Conclusions

In conclusion of old and new observations, the old killer symbionts of Paramecium may rather be parasites than mutualists. However, this view does not completely do justice to the system. By coding for R bodies and presumably also for toxins, plasmids and phage genomes ensure the persistence of Caedibacter and of the plasmids / phages themselves in paramecia populations. Caedibacter-free populations of Paramecium may develop under unfavorable conditions, e.g., in case of poor nutrients being the reason for low abundance of the ciliates. Only then paramecia without endocytobionts would survive, not being threatened by R body-bearing Caedibacter that are released by host cells. Caedibacter-free paramecia need less food and grow faster. Since, however, in many habitats the conditions are favorable for bacterial feeders like Paramecium, R body-coding plasmids or phages ensure persistence of the killer symbioses, no matter whether Caedibacter is a mutualist or parasite. As always in microbially infected protozoa, host and endocytobiont are forming an entirely new unit facing selection.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Anderson RM, May RM (1982) Coevolution of hosts and parasites. Parasitology 85:411–426

    PubMed  Google Scholar 

  • Anderson RM, May RM (1991) Infectious diseases of humans. Oxford Univ Press, Oxford

    Google Scholar 

  • Atlas RM (1999) Legionella: from environmental habitats to disease pathology, detection and control. Environ Microbiol 1:283–293

    Article  PubMed  CAS  Google Scholar 

  • Balsley M (1967) Dependence of the kappa particles of stock 7 of Paramecium aurelia on a single gene. Genetics 56:125–131

    PubMed  CAS  Google Scholar 

  • Barker J, Brown MRW (1994) Trojan Horses of the microbial world: protozoa and the survival of bacterial pathogens in the environment. Microbiology 140:1253–1259

    Article  PubMed  CAS  Google Scholar 

  • Beier CL, Horn M, Michel R, Schweikert M, Görtz H-D, Wagner M (2002) The genus Caedibacter comprises endobionts of Paramecium spp. related to the Rickettsiales (Alphaproteobacteria) and to Francisella tularensis (Gammaproteobacteria). Appl Environ Microbiol 68:6043–6050

    Article  PubMed  CAS  Google Scholar 

  • Bradley DE (1967) Ultrastructure of bacteriophage and bacteriocins. Bacteriol Rev 31:230–314

    PubMed  CAS  Google Scholar 

  • Butzel HM, Pagliara A (1962) The effect of biochemicals inhibitors upon the killer sensitive system in Paramecium aurelia. Exp Cell Res 27:382–395

    Article  PubMed  CAS  Google Scholar 

  • Casjens SR, Gilcrease EB, Huang WM, Bunny KL, Pedulla ML, Ford ME, Houtz JM, Hatfull GF, Hendrix RW (2004) The PKO2 linear plasmid prophage of Klebsiella oxytoca. J Bacteriol 186:1818–1832

    Article  PubMed  CAS  Google Scholar 

  • Daw MA, Falkiner FR (1996) Bacteriocins: nature, function and structure. Micron 27:467–479

    Article  PubMed  CAS  Google Scholar 

  • Dilts JA (1976) Covalently closed, circular DNA in kappa endobionts of Paramecium. Genet Res 27:161–170

    Article  PubMed  CAS  Google Scholar 

  • Dilts JA, Quackenbush RL (1986) A mutation in the R-body-coding sequences destroys expression of the killer trait in P. tetraurelia. Science 232:641–643

    PubMed  CAS  Google Scholar 

  • Dippel RV (1958) The fine structure of kappa in killer stock 51 of Paramecium aurelia. Preliminary observations. J Biophys Biochem Cytol 4:125–128

    Google Scholar 

  • Dybdahl MF, Storfer A (2003) Parasite local adaptation: Red Queen versus Suicide King. TREE 18:523–530

    Google Scholar 

  • Easter J, Gober JW (2002) ParB-stimulated nucleotide exchange regulates a switch in functionally distinct ParA activities. Mol Cell 10:427–434

    Article  PubMed  CAS  Google Scholar 

  • Fokin SI, Görtz H-D (1993) Caedibacter macronucleorum sp. nov., a bacterium in-habiting the macronucleus of Paramecium duboscqui. Arch Protistenkd 143:319–324

    Google Scholar 

  • Fokin SI, Skovorodkin IN, Schweikert M, Görtz H-D (2004) Co-infection of the macronucleus of Paramecium caudatum by free-living bacteria together with the infectious Holospora obtusa. J Eukaryot Microbiol 51:417–424

    Article  PubMed  Google Scholar 

  • Fritsche TR, Horn M, Seyedirashti S, Gautom RK, Schleifer K-H, Wagner M (1993) In situ detection of novel bacterial endosymbionts of Acanthamoeba spp. phylogenetically related to members of the order Rickettsiales. Appl Environ Microbiol 65:206–212

    Google Scholar 

  • Galibert F, Finan TM, Long SR, Puhler A, Abola P, Ampe F, Barloy-Hubler F, Barnett MJ, Becker A, Boistard P, Bothe G, Boutry M, Bowser L, Buhrmester J, Cadieu E et al (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672

    Article  PubMed  CAS  Google Scholar 

  • Gause GF (1934) The struggle for existence. Hafner Publ, New York

    Google Scholar 

  • Görtz H-D (2002) Bacterial symbionts of protozoa in aqueous environments — potential pathogens? In: Greenblatt C, Spigelman M (eds) Emerging pathogens. Oxford Univ Press, Oxford, pp 25–37

    Google Scholar 

  • Görtz H-D, Michel R (2003) Bacterial symbionts of protozoa in aqueous environments — potential pathogens? In: Greenblatt C, Spigelman M (eds) Emerging pathogens. Oxford Univ Press, Oxford, pp 25–37

    Google Scholar 

  • Görtz H-D, Schmidt HJ (2004) Caedibacter, Holosporaceae, Lyticum, Paracaedibacter, Pseudocaedibacter, Pseudolyticum, Tectibacter and Polynucleobacter. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology, vol 2. Springer, Berlin Heidelberg New York (in press)

    Google Scholar 

  • Hamilton LD, Gettner ME (1958) Fine structure of kappa in Paramecium aurelia. J Biophys Biochem Cytol 4:122–123

    PubMed  CAS  Google Scholar 

  • Heckmann K (1983) Endosymbionts of Euplotes. In: Jeon KW (ed) Intracellular symbiosis. Academic Press, New York, pp 111–144

    Google Scholar 

  • Heruth DC, Pond FR, Dilts JA, Quackenbush RL (1994) Characterization of genetic determinants for R body synthesis and assembly in Caedibacter taeniospiralis 47 and 166. J Bacteriol 176:3559–3567

    PubMed  CAS  Google Scholar 

  • Horn M, Fritsche TR, Gautom RK, Schleifer K-H, Wagner M (1999) Novel bacterial endosymbionts of Acanthamoeba spp. Related to the Paramecium caudatum symbiont Caedibacter caryophilus. Environ Microbiol 1:357–367

    Article  PubMed  CAS  Google Scholar 

  • Ikeda H, Tomizawa J (1968) Phage P1, an extrachromosomal replicator unit. Cold Spring Harbor Symp Quant Biol 33:791–798

    PubMed  CAS  Google Scholar 

  • Jabrane A, Sabri A, Compère P, Jacques P, Vandenberghe I, van Beeumen J, Thonart P (2002) Characterization of Serracin P, a phage-tail-like bacteriocin, and its activity against Erwinia amylovora, the fire blight pathogen. Appl Environ Microbiol 68:5704–5710

    Article  PubMed  CAS  Google Scholar 

  • Jeblick J, Kusch J (2005) Sequence, transcription activity and evolutionary origin of the R-body coding plasmid pKAP298 from the intracellular parasitic bacterium Caedibacter taeniospiralis. J Mol Evol 60:164 173

    Article  PubMed  CAS  Google Scholar 

  • Jeon WP, Jeon KW (1997) A symbiont-produced protein and bacterial symbiosis in Amoeba proteus. J Euk Microbiol 44:614–619

    PubMed  Google Scholar 

  • Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, Sasamoto S, Watanabe A, Idesawa K, Iriguchi M, Kawashima K, Kohara M, Matsumoto M, Shimpo S, Tsuruoka H, Wada T, Yamada M, Tabata S (2002) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9:189–197

    Article  PubMed  Google Scholar 

  • Kusch J, Stremmel M, Schweikert M, Adams V, Schmidt HJ (2000) The toxic symbiont Caedibacter caryophila in the cytoplasm of Paramecium novaurelia. Microb Ecol 40:330–335

    PubMed  CAS  Google Scholar 

  • Kusch J, Czubatinski L, Wegmann S, Hübner M, Alter M, Albrecht P (2002) Competitive advantages of Caedibacter-infected Paramecia. Protist 153:47–58

    Article  PubMed  Google Scholar 

  • Landis WG (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

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Landis W (1988) Ecology. In: Görtz H-D (ed) Paramecium. Springer, Berlin Heidelberg New York, pp 419–436

    Google Scholar 

  • Linka N, Hurka H, Lang BF, Burger G, Winkler HH, Stamme C, Urbany C, Seil I, Kusch J, Neuhaus HE (2003) Phylogenetic relationships of non-mitochondrial nucleotide transport proteins in bacteria and eukaryotes. Gene 306:27–35

    Article  PubMed  CAS  Google Scholar 

  • Marrs BL (1974) Genetic recombination in Rhodopseudomonas capsulata. Proc Natl Acad Sci USA 71:971–973

    PubMed  CAS  Google Scholar 

  • Maruyama C, Fujisawa H, Takagi Y (2001) Age-associated survival and extinction in mixed cultures of Paramecium. Eur J Protistol 37:303–312

    Article  Google Scholar 

  • Motallebi-Veshareh M, Rouch DA, Thomas CM (1990) A family of ATPases involved in active partitioning of diverse bacterial plasmids. Mol Microbiol 4:1455–1463

    PubMed  CAS  Google Scholar 

  • Pond F, Gibson I, Lalucat J, Quackenbush RL (1989) R-body-producing bacteria. Bacteriol Rev 53:25–67

    CAS  Google Scholar 

  • Poulin R (1998) Evolutionary ecology of parasites — from individuals to communities. Chapman and Hall, London

    Google Scholar 

  • Preer JR (1950) Microscopically visible bodies in the cytoplasm of the ‘killer’ strains of Paramecium aurelia. Genetics 35:344–362

    PubMed  Google Scholar 

  • Preer JRJr, Preer LB (1982) Revival of names of protozoan endosymbionts and proposal of Holospora caryophila nom. nov. Int J Syst Bacteriol 32:140–141

    Article  Google Scholar 

  • Preer LB, Jurand A, Preer JR, Rudman BM (1972) The classes of kappa in Paramecium aurelia. J Cell Sci 11:581–600

    PubMed  CAS  Google Scholar 

  • Preer JR Jr, Preer LB, Jurand A (1974) Kappa and other endobionts in Paramecium aurelia. Bacteriol Rev 38:113–163

    PubMed  CAS  Google Scholar 

  • Quackenbush RL (1977) Phylogenetic relationships of bacterial endobionts of Paramecium aurelia: deoxyribonucleotide sequence relationship of 51 kappa and its mutants. J Bacteriol 129:895–900

    PubMed  CAS  Google Scholar 

  • Quackenbush RL (1978) Genetic relationships among bacterial endobionts of Paramecium aurelia: polynucleotide sequence relationships among members of Caedibacter. J Gen Microbiol 108:181–187

    CAS  Google Scholar 

  • Quackenbush RL (1988) Endosymbionts of killer paramecia. In: Görtz H-D (ed) Paramecium. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Quackenbush RL (1983) Plasmids from bacterial endobionts of hump-killer paramecia. Plasmid 9:298–306

    PubMed  CAS  Google Scholar 

  • Quackenbush RL, Burbach JA (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

    PubMed  CAS  Google Scholar 

  • Quackenbush RL, Cox BJ, Kanabrocki JA (1986a) Extrachromosomal elements of extrachromosomal elements of paramecia, and their extrachromosomal elements. In: Wickner RB, Hinnebusch A, Lambowitz AM, Gunsalus IC, Hollaender A (eds) Extrachromosomal elements in lower eukaryotes. Plenum Press, New York, pp 265–278

    Google Scholar 

  • Quackenbush RL, Dilts JA, Cox BJ (1986b) Transposonlike elements in Caedibacter taeniospiralis. J Bacteriol 166:349–352

    PubMed  CAS  Google Scholar 

  • Ravin VK, Shulga MG (1970) Evidence for extrachromosomal location of prophage N15. Virology 40:800–807

    Article  PubMed  CAS  Google Scholar 

  • Reisser W, Meier R, Görtz H-D, Kwang WJ (1985) Establishment, maintenance, and integration mechanisms of endosymbionts in protozoa. J Protozool 32:383–390

    CAS  Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sonneborn TM (1938) Mating types in P. aurelia: diverse conditions for mating in different stocks; occurrence, number and interrelations of the type. Proc Am Phil Soc 79:411–434

    Google Scholar 

  • Sonneborn TM (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 Nat Acad Sci USA 29:329–343

    PubMed  CAS  Google Scholar 

  • Strauch E, Kaspar H, Schaudinn C, Dersch P, Madela K, Gewinner C, Hertwig S, Wecke J, Appel B (2001) Characterization of Enterocoliticin, a phage tail-like bacteriocin, and its effect on pathogenic Yersinia enterocolitica strains. Appl Environ Microbiol 67:5634–5642

    Article  PubMed  CAS  Google Scholar 

  • Walker DH Jr, Walker JT (1975) Genetic studies of coliphage P1. I. Mapping by use of prophage deletions. J Virol 16:525–534

    PubMed  Google Scholar 

  • Yen HC, Hu NT, Marrs BL (1979) Characterization of the gene transfer agent made by an overproducer mutant of Rhodopseudomonas capsulata. J Mol Biol 131:157–168

    Article  PubMed  CAS  Google Scholar 

  • Zhou T, Radaev S, Rosen BP, Gatti DL (2000) Structure of the ArsA ATPase: the catalytic subunit of a heavy metal resistance pump. EMBO J 19:4838–4845

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2005 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Kusch, J., Görtz, HD. (2005). Towards an Understanding of the Killer Trait: Caedibacter endocytobionts in Paramecium . In: Overmann, J. (eds) Molecular Basis of Symbiosis. Progress in Molecular and Subcellular Biology, vol 41. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-28221-1_4

Download citation

Publish with us

Policies and ethics