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Diversity of Endosymbiotic Bacteria inParamecium

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Book cover Endosymbionts in Paramecium

Part of the book series: Microbiology Monographs ((MICROMONO,volume 12))

Abstract

For about one and a half centuries now microbial symbioses in Paramecium have been observed and investigated. Meanwhile a great diversity of endosymbiotic bacteria is known in many of the different species of Paramecium. Paramecium is a unicellular but complete eukaryotic organism. For microbial symbionts, the large cells offer plenty of space and a variety of niches of different metabolic conditions. Bacteria living in the cytoplasm, in micronuclei or macronuclei, or even in the perinuclear space show quite different life strategies. Peculiar adaptations to the symbiotic mode of life have stimulated research in different fields, such as microbiology, cell biology, physiology, ecology, and ­phylogenetics. The symbionts of Paramecium not only turn out to belong to different taxa of Eubacteria, but some appear to be related to human pathogens. As a special highlight, an endonuclear symbiont of Paramecium, Holospora obtusa, may be the closest relative of mitochondria known to date.

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References

  • Allen RD (1988) Cytology. In: Görtz H-D (ed) Paramecium. Springer, Berlin, pp 4–40

    Google Scholar 

  • Amann R, Springer N, Ludwig W, Görtz H-D, Schleifer K-H (1991) Identification in situ and phylogeny of uncultured bacterial endosymbionts. Nature 351:161–164

    PubMed  CAS  Google Scholar 

  • Beale GH (1954) The genetics of Paramecium aurelia. Cambridge University Press, Cambridge

    Google Scholar 

  • Beale GH, Preer JR Jr (2008) Paramecium: Genetics and epigenetics. Taylor and Francis, Boca Raton

    Google Scholar 

  • Beale GH, Jurand A, Preer JR Jr (1969)The classes of endosymbiont of Paramecium aurelia. J Cell Sci 5:65–91

    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

    PubMed  CAS  Google Scholar 

  • Berger JD (1988) The cell cycle and regulation of cell mass and macronuclear DNA content. In: Görtz H-D (ed) Paramecium. Springer, Berlin, pp 97–119

    Google Scholar 

  • Blackburn EH (1991) Structure and function of telomeres. Nature 350:569–573

    PubMed  CAS  Google Scholar 

  • Boss AO-L, Borchsenius ON, Ossipov DV (1987) Pseudolyticum multiflagellatum n. g., n. sp. – a new symbiotic bacterium in the cytoplasm of Paramecium caudatum (Ciliata, Protozoa). Cytologia (Sankt-Petersburg) 29:94–99 (in Russian with English summary)

    Google Scholar 

  • Chen TT (1955) Paramecin 34, a killer substance produced by Paramecium bursaria. Proc Soc Exp Biol Med 88:541–543

    PubMed  CAS  Google Scholar 

  • Chen TT (1956) Varieties and mating types in Paramecium bursaria. II. Variety and mating types found in China. J Exp Zool 132:255–268

    Google Scholar 

  • Cohen J, Beisson J (1988) The cytoskeleton. In: Görtz H-D (ed) Paramecium. Springer, Berlin, pp 363–392

    Google Scholar 

  • Dieckmann J (1977) An infectious bacterium in the cytoplasm of Paramecium caudatum. In Abstract Volume. International Congress of Protozoology, Warzawa, p 77

    Google Scholar 

  • Dohra H, Fujishima M (1999) Effect of antibiotics on the early infection process of a macronuclear endosymbiotic bacterium Holospora obtusa of Paramecium caudatum. FEMS Microbiol Lett 179:473–477

    PubMed  CAS  Google Scholar 

  • Dohra H, Fujishima M, Ishikawa H (1998) Structure and expression of a GroE-homologous operon of a macronucleus-specific symbiont Holospora obtusa of the ciliate Paramecium caudatum. J Eukaryot Microbiol 45:471–479

    Google Scholar 

  • DuBois M, Prescott DM (1995) Scrambling of the actin 1 gene in two Oxytricha species. Proc Natl Acad Sci U S A 92:3888–3892

    PubMed  CAS  Google Scholar 

  • Estève J-C (1978) Une population de type “killer” chez Paramecium caudatum (Ehrenberg). Protistologica 14:201–207

    Google Scholar 

  • Euzeby JP (1997) Revised nomenclature of specific or subspecific epithets that do not agree in gender with generic names that end in -bacter. Int J Syst Bacteriol 47:584

    Google Scholar 

  • Fels D, Kaltz O (2006) Temperature-dependent transmission and latency of Holospora undulata, a micronucleus-specific parasite of the ciliate Paramecium caudatum. Proc R Soc Lond B 273:1031–1038

    Google Scholar 

  • Ferrantini F, Fokin SI, Vannini C, Modeo L, Verni F, Petroni G (2007) Ciliates as natural hosts of many novel Rickettsia-like bacteria. Protistology 5:28–29

    Google Scholar 

  • Fok AK, Allen RD (1988) The lysosome system. In: Görtz H-D (ed) Paramecium. Springer, Berlin, pp 301–324

    Google Scholar 

  • Fokin SI (1988) A bacterial symbiont of the macronucleus perinuclear space in the ciliate Paramecium duboscqui. Cytologia 30:632–635

    Google Scholar 

  • Fokin SI (1989a) Bacterial endobionts of the ciliate Paramecium woodruffi. II. Endobionts of the perinuclear space. Cytology (Sankt-Petersburg) 31:845–850 (in Russian with English summary)

    Google Scholar 

  • Fokin SI (1989b) Bacterial endobionts of the ciliate Paramecium woodruffi. III. Endobionts of the cytoplasm. Cytology (Sankt-Petersburg) 31:964–969 (in Russian with English summary)

    Google Scholar 

  • Fokin SI (1989c) Mate-killer effect caused by endobionts of the ciliate Paramecium woodruffi. Cytology (Sankt-Petersburg) 31:1085–1089 (in Russian with English summary)

    Google Scholar 

  • Fokin SI (1997) Morphological diversity of the micronuclei in Paramecium. Arch Protistenkd 148:375–387

    Google Scholar 

  • Fokin SI (2004)Bacterial endocytobionts of Ciliophora and their interactions with the host cell. Int Rev Cytol 236:181–249

    PubMed  Google Scholar 

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

    Google Scholar 

  • Fokin SI, Karpov SA (1995) Bacterial endocytobionts inhabiting the perinuclear space of Protista. Endocytobiosis Cell Res 11:81–94

    Google Scholar 

  • Fokin SI, Ossipov DV (1986) Pseudocaedibacter glomeratus sp. n. – a cytoplasmic symbiont of the ciliate Paramecium pentaurelia. Cytologia 28:1000–1004

    Google Scholar 

  • Fokin SI, Boss AO-L, Ossipov DV (1987a)Virus-containing cytoplasmic symbiont of the ciliate Paramecium woodruffi. Cytologia 29:1303–1306

    Google Scholar 

  • Fokin SI, Sabaneyeva EV (1993) Bacterial endocytobionts of the ciliate Paramecium calkinsi. Eur J Protistol 29:390–395

    Google Scholar 

  • Fokin SI, Ossipov DV, Skoblo II, Rautian MS, Sabaneyeva EV (1987b) Nonospora macronucleata g.n., sp. n. – a vegetative nucleus symbiont of the ciliate Paramecium caudatum. Cytology (Sankt-Petersburg) 29:963–970 (in Russian with English summary)

    Google Scholar 

  • Fokin SI, Stoeck T, Schmidt HJ (1999) Rediscovery of Paramecium nephridiatum Gelei, 1925 and its characteristics. J Euk Microbiol 46:416–426

    Google Scholar 

  • Fokin SI, Sabaneyeva EV, Borkchsenius ON, Schweikert M, Görtz H-D (2000) Paramecium calkinsi and Paramecium putrinum (Ciliaphora, Protista) harboring alpha-subgroup bacteria in the cytoplasm. Protoplasma 213:176–183

    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

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  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 

  • Fujishima M, Fujita M (1985) Infection and maintenance of Holospora obtusa, a macronuclear-specific bacterium of the ciliate Paramecium caudatum. J Cell Sci 76:179–187

    PubMed  CAS  Google Scholar 

  • Gibson I (1974) The endosymbionts of Paramecium. Crit Rev Microbiol 3: 243–273

    CAS  Google Scholar 

  • Gibson I, Beale GH (1961) Genie basis of the mate-killer trait in Paramecium aurelia, stock 540. Genet Res 2:82–91

    Google Scholar 

  • Godiska R, Aufderheide KJ, Gilley D, Hendrie P, Fitzwater T, Preer LB, Polisky, B, Preer JR Jr (1987) Transformation of Paramecium by microinjection of a cloned serotype gene. Proc Natl Acad Sci U S A 84:7590–7594

    PubMed  CAS  Google Scholar 

  • Görtz H-D (1981) Ein neues symbiontisches Bakterium in Paramecium sexaurelia. Verh Dtsch Zool Ges 74:227

    Google Scholar 

  • Görtz HD (1982) Infection of Paramecium bursaria with bacteria and a yeast. J Cell Sci 58:445–453

    PubMed  Google Scholar 

  • Görtz H-D (1983) Endonuclear symbionts in Ciliates. Int Rev Cytol Suppl 14:145–176

    Google Scholar 

  • Görtz H-D (1987) Different endocytobionts simultaneously colonizing ciliate cells. Ann N Y Acad Sci 503:261–268

    Google Scholar 

  • Görtz, H-D (2007) Symbiotic associations between ciliates and prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The orokaryotes, 3rd edn, vol 1. Springer, East Lansing, pp 403–438

    Google Scholar 

  • Görtz HD (2008) Towards an understanding of the distribution, dynamics and ecological significance of bacterial symbioses in protists. Denisia 23:307–311

    Google Scholar 

  • Görtz H-D, Freiburg M (1984) Bacterial symbionts in the micronucleus of Paramecium bursaria. Endocytobiosis Cell Res 1:37–46

    Google Scholar 

  • Görtz H-D, Fujishima M (1983) Conjugation and meiosis of Paramecium caudatum infected with the micronucleus-specific bacterium Holospora elegans. Eur J Cell Biol 32:86–91

    PubMed  Google Scholar 

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

    Google Scholar 

  • Görtz H-D, Schmidt HJ (2005) Family III. Holosporaceae fam.nov. In: Garrity et al., (eds) Bergey’s manual of systematic bacteriology, part C, 2nd edn. Springer, New York, pp 146–160

    Google Scholar 

  • Görtz H-D, Wiemann M (1989) Route of infection of the bacteria Holospora elegans and Holospora obtusa into the nuclei of Paramecium caudatum. Eur J Protistol 24:101–109

    Google Scholar 

  • Görtz H-D, Rosati G, Schweikert M, Schrallhammer M, Omura G, Suzaki T (2009) In: White JF Jr, Torres MS (eds) Defensive mutualism in microbial symbiosis. Taylor and Francis, Boca Raton

    Google Scholar 

  • Hausmann K, Hülsmann N, Radek R (2003) Protistology, 3rd edn. Schweizerbart, Stuttgart

    Google Scholar 

  • Heckmann K, Görtz H-D (1991) Prokaryotic symbionts of ciliates. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-D (eds) The prokaryotes, 2nd edn. Springer, Berlin, pp 3865–3890

    Google Scholar 

  • Heckmann K, Schmidt HJ (1987) Polynucleobacter necessarius gen. nov., sp. nov., an obligately endosymbiotic bacterium living in the cyotplasm of Euplotes aediculatus. Int J Syst Bacteriol 37:456–457

    Google Scholar 

  • Holtzman HE (1959) A kappa-like particle in a non-killer stock of Paramecium aurelia, syngen 5. J Protozool 6(Suppl):26

    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

    PubMed  CAS  Google Scholar 

  • Jenkins RA (1970) The fine structure of a nuclear envelope associated endosymbiont of Paramecium. J Gen Microbiol 61: 355–359

    Google Scholar 

  • Jurand A, Rudman BM, Preer JR Jr (1971) Prelethal effects of killing action by stock 7 of Paramecium aurelia. J Exp Zool 177:365–388

    PubMed  CAS  Google Scholar 

  • Katz LA (2001) Evolution of nuclear dualism ciliates: a reanalysis in light of molecular data. Int J Syst Evol Microbiol 51:1587–1592

    PubMed  CAS  Google Scholar 

  • Kusch J, Görtz H-D (2006) Towards an understanding of the killer trait: Caedibacter endocytobionts in Paramecium. Prog Mol Subcell Biol 41:61–76

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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

    Google Scholar 

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

    Google Scholar 

  • Lang BF, Brinkmann H, Koski LB, Fujishima M, Görtz H-D, Burger G (2005) On the origin of mitochondria and Rickettsia-related eukaryotic endosymbionts. Jpn J Protozool 38:171–183

    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

    PubMed  CAS  Google Scholar 

  • Lohse K, Gutierrez A, Kaltz O (2006) Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata. Evol Int J Org Evol 60:1177–1186

    Google Scholar 

  • Meyer GG, Lipps HJ (1980) Chromatin elimination in the hypotrichous ciliate Stylonychia mytilus. Chromosoma 77:284–297

    Google Scholar 

  • Nanney DL (1980) Experimental ciliatology. Wiley, New York

    Google Scholar 

  • Nidelet T, Kaltz O (2007) Direct and correlated responses to selection in a host-parasite system: testing for the emergence of genotype specificity. Evol Int J Org Evol 61:1803–1811

    Google Scholar 

  • Nobili R (1961) Alcune considerazioni sulla liberazione e sull’ azione delle particelle kappa in individui amacronucleati die Paramecium aurelia, stock 51, syngen 4. Atti Soc Tosc Sci Nat Ser B:158–172

    Google Scholar 

  • Nowacki M, Vijayan V, Zhou Y, Schotanus K, Doak T G, Landweber LF (2008) RNA-mediated epigenetic programming of a genome-rearrangement pathway Nature 451:153–158

    PubMed  CAS  Google Scholar 

  • Ossipiv DV (1981) Problems of nuclear heteromorphism in the unicellular organisms. Nauka, Leningrad (in Russian with English summary)

    Google Scholar 

  • Ossipiv DV, Borchsenius ON, Skoblo II, Lebedeva NA (1994) Two new species of symbiotic bacteria in the cytoplasm of the ciliate Paramecium bursaria. Cytology (Sankt-Petersburg) 36:411–426 (in Russian with English summary)

    Google Scholar 

  • Paulin JJ (1996) Morphology and cytology of ciliates. In: Hausmann K, Bradbury PC (eds) Ciliates. Cells as organisms. Fischer, Stuttgart, pp 1–40

    Google Scholar 

  • Preer JR Jr (1948) A sudy of some properties of the cytoplasmic factor “kappa” in P. aurelia, variety 2. Genetics 33:349–404

    CAS  Google Scholar 

  • Preer JR Jr (1977) The killer system in Paramecium – kappa and its viruses. Microbiology 1977:576–578

    Google Scholar 

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

    Google Scholar 

  • Preer JR, Preer LB (1984) Endosymbionts of protozoa. In: Krieg NR (ed) Bergey’s manual of systematic bacteriology, vol. 1. Williams and Wilkins, Baltimore, London, pp 795–813

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Prescott DM (1994) The DNA of ciliated protozoa. Microbiol Mol Biol Rev 58:233–267

    CAS  Google Scholar 

  • Prescott DM, Greslin AF (2005) Scrambled actin I gene in the micronucleus of Oxytricha nova. Dev Genet 13:66–74

    Google Scholar 

  • Przybos E, Fokin SI (1997) Species of the Paramecium aurelia complex Sonneborn in Germany. Arch Protistenkd 148:167–172

    Google Scholar 

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

    CAS  Google Scholar 

  • Quackenbush RL (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 

  • Quackenbush RL (1988) Endosymbionts of killer paramecia. In: Görtz H-D (ed) Paramecium. Springer, Berlin, pp 406–418

    Google Scholar 

  • Raikov IB (1996) Nuclei of ciliates. In: Hausmann K, Bradbury PC (eds) Ciliates. Cells as organisms. Fischer, Stuttgart, pp 221–242

    Google Scholar 

  • Schmidt HJ (1982) Isolation of omikron-endosymbionts from mass cultures of Euplotes aediculatus and characterization of their DNA. Exp Cell Res 140:417–425

    PubMed  CAS  Google Scholar 

  • Schmidt HJ (1984) Studies on protein synthesis in kappa particles. J Gen Microbiol 130:1517–1523

    CAS  Google Scholar 

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

    Google Scholar 

  • Schmitz-Esser S, Link N, Collingro A, Beier CL, Neuhaus HE, Wagner M, Horn M (2004) ATP/ADP translocases: a common feature of obligate intracellular amoebal symbiont related to Chlamydiae and Rickettsiae. J Bacteriol 186:683–691

    PubMed  CAS  Google Scholar 

  • Schneller MV, Sonneborn TM, Mueller JA (1959) The genetic control of kappa-like particles in Paramecium aurelia. Genetics 44:533–534

    Google Scholar 

  • Schrallhammer M, Fokin SI, Schleifer K-H, Petroni G (2006) Characterization of the obligate endosymbiont “Caedibacter macronucleorum” Fokin and Görtz, 1993 and of its host Paramecium duboscqui strain Ku4-8. J Eukaryot Microbiol 53:499–506

    PubMed  CAS  Google Scholar 

  • Schweikert M, Meyer B (2001) Characterization of intracellular bacteria in the freshwater dinoflagellate Peridinium cinctum. Protoplasma 217:177–184

    PubMed  CAS  Google Scholar 

  • Sitte P (1993) Symbiotenic evolution of complex cells and complex plastids. Eur J Protistol 29:131–143

    Google Scholar 

  • Skoblo II, Borchsenius ON, Lebedeva NA, Ossipov DV (1985) A new species of symbiotic bacteria of Paramecium bursaria (Ciliophora, Protozoa). Cytology (Sankt-Petersburg) 27:1292–1297 (in Russian with English summary)

    Google Scholar 

  • Soldo AT (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

    PubMed  CAS  Google Scholar 

  • Soldo AT (1987) Parauronema acutum and its xenosomes: a model system. J Protozool 34:447–451

    PubMed  CAS  Google Scholar 

  • Soldo AT, Godoy GA (1973a) Observations on the production of folic acid by symbiont lambda particles of Paramecium aurelia stock 299. J Protozool 20:502

    Google Scholar 

  • Soldo AT, Godoy GA (1973b) Molecular complexity of Paramecium symbiont lambda deoxyribonucleic acid: evidence for the presence of a multicopy genome. J Mol Biol 73:93–108

    CAS  Google Scholar 

  • Sonneborn TM (1938) Mating types in Paramecium aurelia: diverse conditions for mating in different stocks; occurrence, number and interrelations of the type. Proc Am Philos 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 charcters in P. aurelia on problems of cytoplasmic inheritance, pneumococcus transformations, mutations and development. Proc Nat Acad Sci U S A 29:329–343

    CAS  Google Scholar 

  • 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 of Paramecium caudatum. Proc Natl Acad Sci U S A 90:9892–9895

    PubMed  CAS  Google Scholar 

  • Springer N, Amann R, Ludwig W, Schleifer KH, Schmidt HJ (1996) Polynucleobacter necessarius, an obligate Material endosymbiont of the hypotrichous ciliate Euplotes aediculatus, is a member of the ß-subclass of proteobacteria. FEMS Microbiol Lett 135:333–336

    PubMed  CAS  Google Scholar 

  • Steinbrück G (1983) Overamplification of genes in macronuclei of hypotrichous ciliates. Chromosoma 88:156–163

    Google Scholar 

  • Steinbrück G (1986) Molecular reorganization during nuclear differentiation in ciliates. In: Hennig W (ed) Results and problems in cell differentiation. Springer, Berlin, pp 13:105–174

    Google Scholar 

  • Vannini C, Hahn M, Petroni G, Verni F, Lucchesi S, Rosati G (2005) Recent adaptation to symbiotic lifestyle: the Polynucleobacter – Euplotes system. J Eukaryot Microbiol 52:38S–43S

    Google Scholar 

  • Vannini C, Pöckl M, Petroni G, Wu QL, Lang E, Stackebrandt E, Schrallhammer M, Richardson P, Hahn, MW (2007) Endosymbiosis in statu nascendi: close phylogenetic relationship between obligately endosymbiotic and obligately free-living Polynucleobacter strains (Betaproteobacteria). Environ Microbiol 9:347–359

    PubMed  CAS  Google Scholar 

  • Vishnyakov A, Rodionova G (1999) Motile intranuclear symbionts of ciliate Paramecium multimicronucleatum. In: Wagner et al (eds) From symbiosis to eukaryotism. Endocytobiology VII. University of Geneva, Geneva, pp 169–177

    Google Scholar 

  • Wichterman R (1986) The biology of Paramecium, 2nd edn. Plenum, New York

    Google Scholar 

  • Yao M-C (2008) RNA rules. Nature 451:131–132

    PubMed  CAS  Google Scholar 

  • Yu X-J, Walker DH (2005) Genus I. Rickettsia. In: Garrity et al. (eds) Bergey’s manual of systematic bacteriology, part C, 2nd edn. Springer, New York, pp 96–114

    Google Scholar 

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Görtz, HD., Fokin, S.I. (2009). Diversity of Endosymbiotic Bacteria inParamecium . In: Fujishima, M. (eds) Endosymbionts in Paramecium. Microbiology Monographs, vol 12. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-92677-1_6

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