Revised Systematics of Holospora-Like Bacteria and Characterization of "Candidatus Gortzia infectiva", a Novel Macronuclear Symbiont of Paramecium jenningsi

Microbial Ecology

Volumn 65, Issue 1, 2013, Pages 255-267

  Boscaro, Vittorio ^a   Fokin, Sergei I ^a   Schrallhammer, Martina ^b   Schweikert, Michael ^c   Petroni, Giulio ^a  

^a UNIVERSITY OF PISA   (Italy)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF STUTTGART   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); CILIOPHORA; HOLOSPORA; HOLOSPORA OBTUSA; HOLOSPORA UNDULATA; HOLOSPORACEAE; PARAMECIUM; PARAMECIUM JENNINGSI; RICKETTSIALES;

EID: 84872317688     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-012-0110-2     Document Type: Article

References (91)

1. Eschbach E, Pfannkuchen M, Schweikert M, Drutschmann D, Brümmer F, Fokin SI, Ludwig W, Görtz HD (2009) "Candidatus Paraholospora nucleivisitans", an intracellular bacterium in Paramecium sexaurelia shuttles between the cytoplasm and the nucleus of its host. Syst Appl Microbiol 32: 490-500.
2. Ferrantini F, Fokin SI, Modeo L, Andreoli I, Dini F, Görtz HD, Verni F, Petroni G (2009) "Candidatus Cryptoprodotis polytropus", a novel Rickettsia-like organism in the ciliated protist Pseudomicrothorax dubius (Ciliophora, Nassophorea). J Eukaryot Microbiol 56: 119-129.
3. Fokin SI (2012) Frequency and biodiversity of symbionts in representatives of the main classes of Ciliophora. Eur J Protistol 48: 138-148.
4. Irbis C, Ushida K (2004) Detection of methanogens and proteobacteria from a single cell of rumen ciliate protozoa. J Gen Appl Microbiol 50: 203-212.
5. Petroni G, Spring S, Schleifer KH, Verni F, Rosati G (2000) Defensive extrusive ectosymbionts of Euplotidium (Ciliophora) that contain microtubule-like structures are bacteria related to Verrucomicrobia. Proc Natl Acad Sci U S A 97: 1813-1817.
6. Rinke C, Schmitz-Esser S, Loy A, Horn M, Wagner M, Bright M (2009) High genetic similarity between two geographically distinct strains of the sulfur-oxidising symbiont "Candidatus Thiobios zoothamnicoli". FEMS Microbiol Ecol 67: 229-241.
7. Rinke C, Schmitz-Esser S, Stoecker K, Nussbaumer AD, Molnár DA, Vanura K, Wagner M, Horn M, Ott JA, Bright M (2006) "Candidatus Thiobios zoothamnicoli", an ectosymbiotic bacterium covering the giant marine ciliate Zoothamnium niveum. Appl Environ Microbiol 72: 2014-2021.
8. Schrallhammer M, Fokin SI, Schleifer KH, Petroni G (2006) Molecular 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.
9. Schrallhammer M, Schweikert M, Vallesi A, Verni F, Petroni G (2011) Detection of a novel subspecies of Francisella noatunensis as endosymbiont of the ciliate Euplotes raikovi. Microb Ecol 61: 455-464.
10. Shinzato N, Watanabe I, Meng XY, Sekiguchi Y, Tamaki H, Matsui T, Kamagata Y (2007) Phylogenetic analysis and fluorescence in situ hybridization detection of archaeal and bacterial endosymbionts in the anaerobic ciliate Trimyema compressum. Microb Ecol 54: 627-636.
11. Sun HY, Noe J, Barber J, Coyne RS, Cassidy-Hanley D, Clark TG, Findly RC, Dickerson HW (2009) Endosymbiotic bacteria in the parasitic ciliate Ichthyophthirius multifiliis. Appl Environ Microbiol 75: 7445-7452.
12. Vannini C, Ferrantini F, Ristori A, Verni F, Petroni G (2012) Betaproteobacterial symbionts of the ciliate Euplotes: origin and tangled evolutionary path of an obligate microbial association. Environ Microbiol. doi: 10. 1111/j. 1462-2920. 2012. 02760. x.
13. Vannini C, Ferrantini F, Schleifer KH, Ludwig W, Verni F, Petroni G (2010) "Candidatus Anadelfobacter veles" and "Candidatus Cyrtobacter comes", two new Rickettsiales species hosted by the protist ciliate Euplotes harpa (Ciliophora, Spirotrichea). Appl Environ Microbiol 76: 4047-4054.
14. Vannini C, Petroni G, Verni F, Rosati G (2005) A bacterium belonging to the Rickettsiaceae family inhabits the cytoplasm of the marine ciliate Diophrys appendiculata (Ciliophora, Hypotrichia). Microb Ecol 49: 434-442.
15. Vannini C, Rosati G, Verni F, Petroni G (2004) Identification of the bacterial endosymbionts of the marine ciliate Euplotes magnicirratus (Ciliophora, Hypotrichia) and proposal of "Candidatus Devosia euplotis". Int J Syst Evol Microbiol 54: 1151-1156.
16. Fokin SI (2004) Bacterial endocytobionts of Ciliophora and their interactions with the host cell. Int Rev Cytol 236: 181-249.
17. Görtz HD (1996) Symbiosis in ciliates. In: Hausmann K, Bradbury PS (eds) Ciliates. Cells as organisms. Fisher, Stuttgart, pp 441-462.
18. Görtz HD (2006) Symbiotic associations between ciliates and prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes, vol 1, 3rd edn. Springer, New York, pp 364-402.
19. Görtz HD, Fokin SI (2009) Diversity of endosymbiotic bacteria in Paramecium. In: Fujishima M (ed) Endosymbionts in Paramecium. Microbiology Monograph, Münster, pp 131-160.
20. Vannini C, Petroni G, Schena A, Verni F, Rosati G (2003) Well-established mutualistic associations between ciliates and prokaryotes might be more widespread and diversified than so far supposed. Eur J Protistol 39: 481-485.
21. Duncan AB, Fellous S, Kaltz O (2011) Temporal variation in temperature determines disease spread and maintenance in Paramecium microcosm populations. Proc R Soc B 278: 3412-3420.
22. Fellous S, Quillery E, Duncan AB, Kaltz O (2011) Parasitic infection reduces dispersal of ciliate host. Biol Lett 7: 327-329.
23. 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 B 273: 1031-1038.
24. Kusch J, Czubatinsky L, Wegmann S, Hübner M, Alter M, Albrecht P (2002) Competitive advantages of Caedibacter-infected paramecia. Protist 153: 47-58.
25. Vannini C, Lucchesi S, Rosati G (2007) Polynucleobacter: symbiotic bacteria in ciliates compensate for a genetic disorder in glycogenolysis. Symbiosis 44: 85-91.
26. Vannini C, Pöckl M, Petroni G, Wu QL, Lang E, Stackebrandt E, Schrallhammer M, Richardson PM, 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.
27. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59: 143-169.
28. Amann RI, Springer N, Ludwig W, Görtz HD, Schleifer KH (1991) Identification in situ and phylogeny of uncultured bacterial endosymbionts. Nature 351: 161-164.
29. Fokin SI, Görtz HD (2009) Diversity of Holospora bacteria in Paramecium and their characterization. In: Fujishima M (ed) Endosymbionts in Paramecium. Microbiology Monograph, Münster, pp 161-199.
30. Görtz HD, Schmidt HJ (2005) Holosporaceae fam. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT (eds) Bergey's manual of systematic bacteriology, 2nd edn, vol II, part C. Springer, New York, pp 146-160.
31. Gromov BV, Ossipov DV (1981) Holospora (ex Hafkine 1890) nom. rev., a genus of bacteria inhabiting the nuclei of paramecia. Int J Syst Bacteriol 31: 348-352.
32. Hafkine MW (1890) Maladies infectieuses des paramécies. Ann Inst Pasteur Paris 4: 363-379.
33. 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.
34. Fokin SI (2000) Host specificity of Holospora and its relationships with Paramecium phylogeny. Jpn J Protozool 33: 94.
35. Hori M, Fujii K, Fujishima M (2008) Micronucleus-specific bacterium Holospora elegans irreversibly enhances stress gene expression of the host Paramecium caudatum. J Eukaryot Microbiol 55: 515-521.
36. Hori M, Fujishima M (2003) The endosymbiotic bacterium Holospora obtusa enhances heat-shock gene expression of the host Paramecium caudatum. J Eukaryot Microbiol 50: 293-298.
37. Smurov AO, Fokin SI (1998) Resistance of some stocks of ciliate Paramecium caudatum infected with endonuclear bacteria Holospora against salinity impact. Proc Zool Inst RAS 276: 175-178.
38. Fujishima M, Hoshide K (1988) Light and electron microscopic observations of Holospora obtusa: a macronucleus-specific bacterium of the ciliate Paramecium caudatum. Zool Sci 5: 791-799.
39. Fujishima M, Sawabe H, Iwatsuki K (1990) Scanning electron microscopic observations of differentiation from the reproductive short form to the infectious long form of Holospora obtusa. J Protozool 37: 123-128.
40. Görtz HD, Ahlers N, Robenek H (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.
41. Görtz HD, Dieckmann J (1980) Life cycle and infectivity of Holospora elegans Haffkine, a micronucleus-specific symbiont of Paramecium caudatum (Ehrenberg). Protistologica 16: 591-603.
42. Dohra H, Fujishima M (1999) Cell structure of the infectious form of Holospora, an endonuclear symbiotic bacterium of the ciliate Paramecium. Zool Sci 16: 93-98.
43. Iwatani K, Dohra H, Lang BF, Burger G, Hori M, Fujishima M (2005) Translocation of an 89-kDa periplasmic protein is associated with Holospora infection. Biochem Biophys Res Commun 337: 1198-1205.
44. Fujishima M (2009) Infection and maintenance of Holospora species in Paramecium caudatum. In: Fujishima M (ed) Endosymbionts in Paramecium. Microbiology Monograph, Münster, pp 201-225.
45. Wiemann M, Görtz HD (1989) Release of the endonucleobiotic bacterium Holospora elegans from its host cell Paramecium caudatum. Eur J Protistol 25: 100-108.
46. Fujishima M, Kawai M (1997) Acidification in digestive vacuoles is an early event required for Holospora infection of Paramecium nucleus. In: Achenk HEA, Herrmann RG, Jeon KW, Müller NE, Schwemmler W (eds) Eukaryotism and symbiosis. Springer, Berlin, pp 367-370.
47. Sabaneyeva EV, Derkacheva ME, Benken KA, Fokin SI, Vainio S, Skovorodkin IN (2009) Actin-based mechanism of Holospora obtusa trafficking in Paramecium caudatum. Protist 160: 205-219.
48. Sabaneyeva EV, Fokin SI, Gavrilova EV, Kornilova ES (2005) Nocodazole inhibits macronuclear infection with Holospora obtusa in Paramecium caudatum. Protoplasma 226: 147-153.
49. Fokin SI, Brigge T, Brenner J, Görtz HD (1996) Holospora species infecting the nuclei of Paramecium appear to belong into two groups of bacteria. Eur J Protistol 32: 19-24.
50. Fokin SI, Sabaneyeva EV (1997) Release of endonucleobiotic bacteria Holospora bacillata and Holospora curvata from the macronucleus of their host cells Paramecium woodruffi and Paramecium calkinsi. Endocyt Cell Res 12: 49-55.
51. Vakkerov-Kouzova ND, Rautian MS (2011) Obtaining and characterization of "Holospora curviuscula" and Holospora obtusa, bacterial symbionts of the macronuclei of Paramecium bursaria and Paramecium caudatum. Microbiology 80: 728-732.
52. Schrallhammer M, Schweikert M (2009) The killer effect of Paramecium and its causative agents. In: Fujishima M (ed) Endosymbionts in Paramecium. Microbiology Monograph, Münster, pp 227-246.
53. Birtles RJ, Rowbotham TJ, Michel R, Pitcher DG, Lascola B, Alexiou-Daniel S, Raoult D (2000) "Candidatus Odyssella thessalonicensis" gen. nov., sp. nov., an obligate intracellular parasite of Acanthamoeba species. Int J Syst Evol Microbiol 50: 63-72.
54. Horn M, Fritsche TR, Gautom RK, Schleifer KH, Wagner M (1999) Novel bacterial endosymbionts of Acanthamoeba spp. related to the Paramecium caudatum symbiont Caedibacter caryophilus. Environ Microbiol 1: 357-367.
55. Przyboś E, Fokin S, Stoeck T, Schmidt HJ (1999) Occurrence and ecology of Paramecium jenningsi strains. Folia Biol-Krakow 47: 53-59.
56. Wichterman R (1953) The biology of Paramecium. McGraw-Hill, New York, p 527.
57. Skovorodkin IN (1990) A device for immobilizing biological objects in the light microscope studies. Tsitologiya 32: 301-302, In Russian with English summary.
58. Fokin SI (1997) Morphological diversity of the micronuclei in Paramecium. Arch Protistenkd 148: 375-387.
59. Fokin SI (2010/2011) Paramecium genus: biodiversity, some morphological features and the key to the main morphospecies discrimination. Protistology 6: 227-235.
60. Preer LB (1969) Alpha, an infectious macronuclear symbiont of Paramecium aurelia. J Protozool 16: 570-578.
61. Don RH, Cox PT, Wainwright BJ, Baker K, Mattick JS (1991) "Touchdown" PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res 19: 4008.
62. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
63. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
64. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
65. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
66. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
67. Felsenstein J (1989) PHYLIP-phylogeny inference package (version 3. 2). Cladistics 5: 164-166.
68. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
69. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
70. Miyake A (1981) Cell-cell interaction by gamones in Blepharisma. In: O'Day DH, Horgen PA (eds) Sexual interactions in eukaryotic microbes. Academic, New York, pp 95-129.
71. Manz W, Amann RI, Ludwig W, Wagner M, Schleifer KH (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst Appl Microbiol 15: 593-600.
72. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-D145.
73. Loy A, Maixner F, Wagner M, Horn M (2007) probeBase-an online resource for rRNA-targeted oligonucleotide probes: new features 2007. Nucleic Acids Res 35: D800-D804.
74. Wang Y, Stingl U, Anton-Erxleben F, Zimmer M, Brune A (2004) "Candidatus Hepatincola porcellionum" gen. nov., sp. nov., a new, stalk-forming lineage of Rickettsiales colonizing the midgut glands of a terrestrial isopod. Arch Microbiol 181: 299-304.
75. Ludwig W, Strunk O, Klugbauer S, Klugbauer N, Weizenegger M, Neumaier J, Bachleitner M, Schleifer KH (1998) Bacterial phylogeny based on comparative sequence analysis. Electrophoresis 19: 554-568.
76. Murray RGE, Schleifer KH (1994) A proposal for recording the properties of putative taxa of procaryotes. Int J Syst Bacteriol 44: 174-176.
77. Murray RGE, Stackebrandt E (1995) Implementation of the provisional status Candidatus for incompletely described prokaryotes. Int J Syst Bacteriol 45: 186-187.
78. Borchsenius ON, Skoblo II, Ossipov DV (1983) Holospora curviuscula-a new species of macronuclear symbiotic bacteria of Paramecium bursaria. Tsitologiya 25: 91-97, In Russian with English summary.
79. Landis WG (1981) The ecology, role of the killer trait, and interactions of five species of Paramecium aurelia complex inhabiting the littoral zone. Can J Zool 59: 1734-1743.
80. Landis WG (1987) Factors determining the frequency of the killer trait within populations of the Paramecium aurelia complex. Genetics 115: 197-205.
81. Preer JR, Stark PS (1953) Cytological observations on the cytoplasmic factor "kappa" in Paramecium aurelia. Exp Cell Res 5: 478-491.
82. Schrallhammer M, Galati S, Altenbuchner J, Schweikert M, Görtz HD, Petroni G (2012) Tracing the role of R-bodies in the killer trait: absence of toxicity of R-body producing recombinant E. coli on paramecia. Eur J Protistol. doi: 10. 1016/j. ejop. 2012. 01. 008.
83. Preer JR, Preer LB, Jurand A (1974) Kappa and other endosymbionts in Paramecium aurelia. Bacteriol Rev 38: 113-163.
84. Kusch J, Stremmel M, Breiner HW, Adams V, Schweikert M, Schmidt HJ (2000) The toxic symbiont Caedibacter caryophila in the cytoplasm of Paramecium novaurelia. Microb Ecol 40: 330-335.
85. Beier CL, Horn M, Michel R, Schweikert M, Görtz HD, Wagner M (2002) The genus Caedibacter comprises endosymbionts of Paramecium spp. related to the Rickettsiales (Alphaproteobacteria) and to Francisella tularensis (Gammaproteobacteria). Appl Environ Microbiol 68: 6043-6050.
86. Springer N, Ludwig W, Amann R, Schmidt HJ, Görtz HD, Schleifer KH (1993) Occurrence of fragmented 16S rRNA in an obligate bacterial endosymbiont of Paramecium caudatum. Proc Natl Acad Sci U S A 90: 9892-9895.
87. Jones RT, McCormick KF, Martin AP (2008) Bacterial communities of Bartonella-positive fleas: diversity and community assembly patterns. Appl Environ Microbiol 74: 1667-1670.
88. 2 affects soil microbial diversity associated with trembling aspen. Environ Microbiol 10: 926-941.
89. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Kumar Y, Buchner A, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüßmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
90. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115-147.
91. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56: 1919-1925.