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The Family Holosporaceae

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The Prokaryotes

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The Holosporaceae family (Görtz H-D, Schmidt HJ (2005) Genus Holospora. In: Garrity et al. (eds) Bergey’s manual of systematic of bacteriology, vol 2, part C, 2nd edn. Springer, New York, pp 149–151) in the Rickettsiales order (Gieszczykiewicz 1939) includes a group of gram-negative bacteria without motility and obligatory symbionts. Routinely, these bacteria occupy specific compartments in their host cells, which are generally rich in metabolites (Heckmann, K. Görtz H-D (1991) Procaryotic symbionts of ciliates. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds) The prokaryotes, 2nd edn. Springer, Berlin/Heidelberg/New York, pp 3865–3890; Fokin and Karpov, Endocyt Cell Res 11:81–94, 1995). Individuals of this family are mostly endosymbionts of ciliated protozoa of the genus Paramecium (Müller 1772) that parasitize, according to the species, the macronucleus and micronucleus. The family has only one consolidated genus, Holospora, and others seven genera considered to be incertae sedis in this family, including Caedibacter, Lyticum, Odyssella, Paracedibacter, Pseudocaedibacter, Pseudolyticum, and Tectibacter (Fujishima and Fujita, J Cell Sci 76:179–187, 1985). However, Lyticum was recently moved to the Midichloriaceae family (Boscaro et al., Microb Ecol 65:255–267, 2013). Among those cited, Holospora and Caedibacter are commonly studied. Thus, H. obtusa, H. caryophila, and H. curviuscula are parasitize the macronucleus of P. caudatum and P. biaurelia; H. elegans, H. undulate, and H. accuminata can be found in micronucleus of P. caudatum and P. bursaria. The specificity for the host does not occur only by the success of cell penetration, which demonstrates that the specificity for a habitat is influenced by nuclear genes (Fujishima and Fujita, J Cell Sci 76:179–187, 1985). Its distribution is still not clearly defined, but it is believed to be associated with the distribution of its host (Fokin et al., Eur J Protistol 32:19–24, 1996).

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References

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Andersson GE, Zomorodipour A, Andersson JO, Sicheritz-Ponten T, Ismark UCM, Podowski RM, Na¨slund AK, Eriksson A-S, Winkler HH, Kurland CG (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133–140

    Article  CAS  PubMed  Google Scholar 

  • Baker BJ, Hugenholtz P, Dawson SC, Banfield JF (2003) Extremely acidophilic protists from acid mine drainage host Rickettsiales-lineage endosymbionts that have intervening sequences in their 16S rRNA genes. Appl Environ Microbiol 69:5512–5518

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Beier CL, Horn M, Michel R, Schweikert M, Görtz H-D, 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bishop R (2010) Applications of fluorescence in situ hybridization (FISH) in detecting genetic aberrations of medical significance. Biohorizons 3:85–95

    CAS  Google Scholar 

  • Boscaro V, Fokin SI, Schrallhammer M, Schweikert M, Petroni G (2013) Revised systematics of Holospora-like bacteria and characterization of “Candidatus Gortzia infectiva”, a novel macronuclear symbiont of Paramecium jenningsi. Microb Ecol 65:255–267

    Article  CAS  PubMed  Google Scholar 

  • Burger G, Lang BF (2003) Parallels in genome evolution in mitochondria and bacterial symbionts. IUBMB Life 55:205–212

    Article  CAS  PubMed  Google Scholar 

  • Darriba S, Ruiz M, López C (2012) Phage particles infecting branchial Rickettsiales-like organisms in banded carpet shell Polititapes virgineus (Bivalvia) from Galicia (NW Spain). Dis Aquat Organ 100:269–272

    Article  CAS  PubMed  Google Scholar 

  • Dohra H, Fujishima M (1999) Cell Structure of the infectious form of Holospora, an endonuclear symbiotic bacterium of the ciliate Paramecium. Zoolog Sci 16:93–98

    Article  Google Scholar 

  • Dohra H, Suzuki H, Suzuki T, Tanaka K, Fujishima M (2013) Draft genome sequence of Holospora undulata strain HU1, a micronucleus-specific symbiont of the ciliate Paramecium caudatum. Genome Announc 1:664-13

    Article  Google Scholar 

  • Dorah H, Suzuki H, Suzuki T, Tanaka K, Fujishima M (2013) Draft genome sequence of Holospora undulata strain HU1, a micronucleus-specific symbiont of the ciliate Paramecium caudatum. Genome Announc 1:1–2

    Google Scholar 

  • Dumler JS, Barbet AF, Bekker CPJ, Dasch GA, Palmer GH, Ray SC, Rikihisa Y, Rurangirwa FR (2001) Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: Unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ‘HE agent’ as subjective synonyms of Ehrlichia phagocytophila. Int J Syst Evol Microbiol 51:2145–2165

    Article  CAS  PubMed  Google Scholar 

  • Eschbach E, Pfannkuchena M, Schweikerta M, Drutschmannb D, Brümmera F, Fokin S, Ludwigd W, Görtz H-D (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

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Smouse PE Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ferla MP, Thrash JC, Giovannoni SJ, Patrick WM (2013) New rRNA gene-based phylogenies of the Alphaproteobacteria provide perspective on major groups, mitochondrial ancestry and phylogenetic instability. PLos One 8:1–14

    Article  Google Scholar 

  • Fok AK, Allen RD (1988) The lysosome system. In: Gortz HD (ed) Paramecium. Springer, Berlin, pp 301–324

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Fokin SI, Karpov S (1995) Bacterial endocytobionts inhabiting the perinuclear space of protista. Endocyt Cell Res 11:81–94

    Google Scholar 

  • Fokin SI, Bridge T, Brenner J, Görtz H-D (1996) Holospora species infecting the nuclei of Paramecium appear to belong into two groups of bacteria. Eur J Protistol 32:19–24

    Article  Google Scholar 

  • Fujisawa T, Barraclough TG (2013) Delimiting species using single-locus data and the generalized mixed yule coalescent (GMYC) approach: a revised method and evaluation on simulated datasets. Syst Biol 62:707–724

    Article  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Fujishima M, Görtz HD (1983) Infection of macronuclear anlagen of Paramecium caudatum with the macronucleusspecific symbiont Holospora obtusa. J Cell Sci 64:137–146

    CAS  PubMed  Google Scholar 

  • Fujishima K, Horie R, Mochizuki A Kengaku M (2012) Principles of branch dynamics governing shape characteristics of cerebellar Purkinje cell dendrites. Development 139:3442–3455

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fujishima M, Kodama Y (2012) Endosymbionts in Paramecium. Eur J Protistol 48:124–137

    Article  PubMed  Google Scholar 

  • Fujishima M, Nagahara K, Kojima Y, Sayama Y (1991) Sensitivity of the infectious longform of the macronuclear endosymbiont Holospora obtusa of the ciliate Paramecium caudatum against chemical and physical factors. Eur J Protistol 27(2):119–126

    Article  CAS  PubMed  Google Scholar 

  • Garrity GM, Bell JA, Lilburn TG (2004) Taxonomic outline if the prokaryotes Bergey’s manual® of systematic bacteriology, 2nd ed, 401p, Springer, New York

    Google Scholar 

  • Garrity GM, Bell JA, Lilburn T (2005) Phylum XIV. Proteobacteria phyl. nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 2, 2nd edn, The Proteobacteria, part B (the Gammaproteobacteria). Springer, New York, p 1

    Chapter  Google Scholar 

  • Garrity GM, Bell JA, Lilburn T (2006) Class I. Alphaproteobacteria class. nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 2, 2nd edn, The proteobacteria, part C (the alpha-, beta-, delta-, and Epsilonproteobacteria). Springer, New York, p 1

    Google Scholar 

  • Georgiades K, Madoui M-A, Le P, Robert C, Raoult D (2011) Phylogenomic analysis of Odyssella thessalonicensis fortifies the common origin of Rickettsiales, Pelagibacter ubique and Reclimonas americana mitochondrion. Plos One 6:1–8

    Google Scholar 

  • Gieszczykiewicz (1939) Zagadnienie systematihki w bakteriologii – Zur Frage der Bakterien-Systematic. Bull Acad Pol Sci Ser Sci Biol 1:9–27 (in Polish with German Abstract)

    Google Scholar 

  • Görtz HD (1986) Endonucleobiosis in ciliates. Int Rev Cytol 12:63–71

    Google Scholar 

  • Görtz H-D, Schmidt HJ (2005) Genus Holospora. In: Garrity (ed) Bergey’s manual of systematic of bacteriology, vol 2, part C, 2nd edn. Springer, New York, pp 149–151

    Google Scholar 

  • Görtz HD, 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

    Article  PubMed  Google Scholar 

  • GORTZ H-D (1983) Endonuclear symbionts in ciliates. Int Rev Cytol 14(suppl.):145–176

    Google Scholar 

  • Gortz HD (2006) Symbiotic associations between ciliates and prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes. A handbook on the biology of bacteria: symbiotic associations, biotechnology, applied microbiology, 3rd edn. Springer, New York, pp 364–402

    Google Scholar 

  • Gouin E, Gantelet H, Egile GC, Lasa I, Ohayon H, Villiers V, Gounon P, Sansonetti, PJ, Cossart P (1999) A comparative study of the actin-based motilities of the pathogenic bacteria Listeria monocytogenes, Shigella flexneri and Rickettsia conorii. J Cell Sci 112:1697–1708

    CAS  PubMed  Google Scholar 

  • Gower JC (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53:325–338

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Haeckel E (1894) Systematische Phylogenie: Entwuf eines natürlichen Systems der Organismen auf Grund ihrer Stammesgeschichte, 3 v: vol 1. Berlin

    Google Scholar 

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

    Google Scholar 

  • Heinzen RA, Hackstadt T, Samuel JE (1999) Developmental biology of Coxiella burnetii. Trends Microbiol 7:149–154

    Article  CAS  PubMed  Google Scholar 

  • Heinzen RA, Hayes SF, Peacock MG Hackstadt T (1993) Directional actin polymerization associated with spotted fever group Rickettsia infection of vero cells. Infect Immun 61:1926–1935

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  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 

  • Lee K-B, Liu C-T, Anzai Y, Kim H, Aono T, Oyaizu H (2005) The hierarchical system of the ‘Alphaproteobacteria’: description of Hyphomonadaceae fam. nov., Xanthobacteraceae fam. nov. and Erythrobacteraceae fam. nov. Int J Syst Evol Microbiol 55:1907–1919

    Article  CAS  PubMed  Google Scholar 

  • Loy JK, Dewhirst FE, Weber W, Frelier PF, Garbar TL, Tasca SI, Templeton JW (1996) Molecular phylogeny and in situ detection of the etiologic agent of necrotizing Hepatopancreatitis in shrimp. Appl Environ Microbiol 62(9):3439–3445

    CAS  PubMed Central  PubMed  Google Scholar 

  • Masahiro F (2009) Endosymbionts in Paramecium. Microbiology monographs, 1 edn, vol 12. Springer, Berlin, pp 201–225

    Google Scholar 

  • Montagna M, Sassera D, Epis S, Bazzocchi C, Vannini C, Lo N, Sacchi L, Fukatsu T, Petroni G, Bandi C (2013) “Candidatus Midichloriaceae” fam. Nov. (Rickettsiales), an ecologically widespread clade of intracellular Alphaproteobacteria. Appl Environ Microbiol 79:3241–3248

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nidelet T, Koella JC, Kaltz O (2009) Effects of shortened host life span on the evolution of parasite life history and virulence in a microbial host-parasite system. BMC Evol Biol 9:1–10

    Article  Google Scholar 

  • Nunan LM, Pantoja CR, Gomez-Jimenez S, Lightner DV (2013) “Candidatus Hepatobacter penaei”, an intracellular pathogenic enteric bacterium in the Hepatopancreas of the Marine Shrimp Penaeus vannamei (Crustacea: Decapoda). Appl Environ Microbiol 79:1407–1409

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pronk LM, Sanderson KE (2001) Intervening sequences in rrn genes and fragmentation of 23S rRNA in genera of the family Enterobacteriaceae. J Bacteriol 183:5782–5787

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rautian MS, Wackerow-Kouzova ND (2013) Phylogenetic placement of two previously described intranuclear bacteria from the ciliate Paramecium bursaria (Protozoa, Ciliophora): ‘Holospora acuminata’ and ‘Holospora curviuscula’. Int J Syst Evol Microbiol 63:1930–1933

    Article  PubMed  Google Scholar 

  • Reid NM, Carstens BC (2012) Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. BMC Evol Biol 12:196

    Article  PubMed Central  PubMed  Google Scholar 

  • Schmidt HJ, Gortz H-D, Quackenbush RL (1987) Caedibacter caryophila sp. nov. a killer symbiont inhabiting the macronucleus of Paramecium caudatum. Int J Syst Evol Microbiol 37(4):459–462

    Google Scholar 

  • Schrallhammer M (2010) The killer trait of Paramecium and its causative agents. Palaeodiversity 3:78–88

    Google Scholar 

  • Springer N, Ludwig TW, Amann R, Schmidtt HJ, Gortz H-D, Schleifer K-H (1993) Occurrence of fragmented 16S rRNA in an obligate bacterial endosymbiont of Paramecium caudatum. Proc Natl Acad Sci USA 90:9892–9895

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical taxonomy. W. H. Freeman and Company, San Francisco

    Google Scholar 

  • Thrash JC, Boyd A, Huggett MJ, Grote J, Carini P, Yoder RJ, Robbertse B, Spatafora JW, Rappé MS, Giovannoni SJ (2011) Phylogenomic evidence for a common ancestor of mitochondria and the SAR11 clade. Nature 13:1–9

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Vannini C, Boscaro V, Ferrantini F, Benken KA, Mironov TI, Schweikert M, Görtz H-D, Fokin SI, Sabaneyeva EV, Petroni G (2014) Flagellar movement in two bacteria of the family Rickettsiaceae: a re-evaluation of motility in an evolutionary perspective. PLoS One 9:1–9

    Google Scholar 

  • Weinert LA, Werren JH, Aebi A, Stone GN, Jiggins FM (2009) Evolution and diversity of Rickettsia bacteria, BMC Biology 7:6. doi:10.1186/1741-7007-7-6

    Google Scholar 

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

    Book  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4579

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Santos, H.A., Massard, C.L. (2014). The Family Holosporaceae. In: Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., Thompson, F. (eds) The Prokaryotes. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30197-1_264

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