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Microbial Ecology

, Volume 71, Issue 2, pp 505–517 | Cite as

A House for Two—Double Bacterial Infection in Euplotes woodruffi Sq1 (Ciliophora, Euplotia) Sampled in Southeastern Brazil

  • Marcus V. X. Senra
  • Roberto J. P. Dias
  • Michele Castelli
  • Inácio D. Silva-Neto
  • Franco Verni
  • Carlos A. G. SoaresEmail author
  • Giulio PetroniEmail author
Host Microbe Interactions
First Online:

Abstract

Several ciliated protists form symbiotic associations with a diversity of microorganisms, leading to drastic impact on their ecology and evolution. In this work, two Euplotes spp. sampled in Rio de Janeiro, Brazil, were identified based on morphological and molecular features as Euplotes woodruffi strain Sq1 and E. encysticus strain Sq2 and investigated for the presence of endosymbionts. While E. woodruffi Sq1 stably hosts two bacterial populations, namely Polynucleobacter necessarius (Betaproteobacteria) and a new member of the family “Candidatus Midichloriaceae” (Alphaproteobacteria, Rickettsiales), here described as “Candidatus Bandiella woodruffii,” branching with a broad host range bacterial group found in association with cnidarians, sponges, euglenoids, and some arthropods; in E. encysticus Sq2 no symbiotic bacterium could be detected. The dispersion ability of this novel bacterium was tested by co-incubating E. woodruffi Sq1 with three different ciliate species. Among the tested strains “Ca. B. woodruffii” could only be detected in association with E. encysticus Sq2 with a prevalence of 20 % after 1 week and 40 % after 2 weeks, maintaining this level for up to 6 months. Nevertheless, this apparent in vitro association was abolished when E. woodruffi Sq1 donor was removed from the microcosm, suggesting that this bacterium has the capacity for at least a short-term survival outside its natural host and the aptitude to ephemerally interact with other organisms. Together, these findings strongly suggest the need for more detailed investigations to evaluate the host range for “Ca. B. woodruffii” and any possible pathogenic effect of this bacterium on other organisms including humans.

Keywords

Ciliates Bacterial symbionts Molecular phylogeny Symbiont dispersion 
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Notes

Acknowledgements

The authors thank for their financial support the Brazilian agencies Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (projects 562366/2010-5 and 484005/2013-8), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) (E-26/110.022/2011), and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG); the Marie Curie Actions, European Commission FP7-PEOPLE-2009-IRSES project CINAR PATHOBACTER (project 247658) and the PRIN fellowship (protocol 2012A4F828_002) from the Italian Research Ministry (MIUR). During the period of development of this work, MS was also supported with Post-Doctoral fellowship by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), PNDP Institucional (project 006995/2011-51). S. Gabrielli is gratefully acknowledged for technical assistance in graphic artwork.

Supplementary material

248_2015_668_MOESM1_ESM.zip (340 kb)
ESM 1 Table S1-S3 Inventory of all sequences used on the phylogenetic analyses. Datasets: (S1) Euplotes; (S2) Polynucleobacter; and (S3) “Ca. Midichloriaceae”. (ZIP 339 kb)

References

  1. 1.
    Fokin SI (2004) Bacterial endocytobionts of Ciliophora and their interactions with the host cell. Int Rev Cytol 236:181–249, doi: http://dx.doi.org/10.1016/S0074-7696(04)36005-5
  2. 2.
    Görtz H-D (1996) Symbiosis in ciliates. In: Hausmann KBP (ed) Ciliates cells as Org. Gustav Fischer, Stuttgart, pp 441–462Google Scholar
  3. 3.
    Müller J (1856) Einige Beobachtungen an Infusorien. Monatsber Preuss Akad Wissensch 389–93Google Scholar
  4. 4.
    Fokin SI (2012) Frequency and biodiversity of symbionts in representatives of the main classes of Ciliophora. Eur J Protistol 48:138–148. doi: 10.1016/j.ejop.2011.12.001 CrossRefPubMedGoogle Scholar
  5. 5.
    Görtz HD (2006) Symbiotic associations between ciliates and prokaryotes. The prokaryotes 1:364–402. doi: 10.1007/0-387-30741-9_15 CrossRefGoogle Scholar
  6. 6.
    Dziallas C, Allgaier M, Monaghan MT, Grossart HP (2012) Act together—implications of symbioses in aquatic ciliates. Front Microbiol 3:288. doi: 10.3389/fmicb.2012.00288 PubMedCentralCrossRefPubMedGoogle Scholar
  7. 7.
    Görtz HD (2001) Intracellular bacteria in ciliates. Int Microbiol 4:143–150. doi: 10.1007/s10123-001-0029-9 PubMedGoogle Scholar
  8. 8.
    Amann R, Springer N, Ludwig W et al (1991) Identification in situ and phylogeny of uncultured bacterial endosymbionts. Nature 351:161–164. doi: 10.1038/351161a0 CrossRefPubMedGoogle Scholar
  9. 9.
    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. doi: 10.2323/jgam.50.203 CrossRefPubMedGoogle Scholar
  10. 10.
    Sun HY, Noe J, Barber J et al (2009) Endosymbiotic bacteria in the parasitic ciliate Ichthyophthirius multifiliis. Appl Environ Microbiol 75:7445–7452. doi: 10.1128/AEM.00850-09 PubMedCentralCrossRefPubMedGoogle Scholar
  11. 11.
    Schrallhammer M, Ferrantini F, Vannini C et al (2013) “Candidatus Megaira polyxenophila” gen. nov., sp. nov.: considerations on evolutionary history, host range and shift of early divergent rickettsiae. PLoS One 8, e72581. doi: 10.1371/journal.pone.0072581 PubMedCentralCrossRefPubMedGoogle Scholar
  12. 12.
    Boscaro V, Petroni G, Ristori A et al (2013) Candidatus Defluviella procrastinata” and “Candidatus Cyrtobacter zanobii”, two novel ciliate endosymbionts belonging to the “Midichloria clade”. Microb Ecol 65:302–310. doi: 10.1007/s00248-012-0170-3 CrossRefPubMedGoogle Scholar
  13. 13.
    Vannini C, Ferrantini F, Ristori A et al (2012) Betaproteobacterial symbionts of the ciliate Euplotes: origin and tangled evolutionary path of an obligate microbial association. Environ Microbiol 14:2553–2563. doi: 10.1111/j.1462-2920.2012.02760.x CrossRefPubMedGoogle Scholar
  14. 14.
    Vannini C, Pöckl M, Petroni G et al (2007) Endosymbiosis in statu nascendi: close phylogenetic relationship between obligately endosymbiotic and obligately free-living Polynucleobacter strains (Betaproteobacteria). Environ Microbiol 9:347–359. doi: 10.1111/j.1462-2920.2006.01144.x CrossRefPubMedGoogle Scholar
  15. 15.
    Schrallhammer M, Schweikert M, Vallesi A et al (2011) Detection of a novel subspecies of Francisella noatunensis as endosymbiont of the ciliate Euplotes raikovi. Microb Ecol 61:455–464. doi: 10.1007/s00248-010-9772-9 CrossRefPubMedGoogle Scholar
  16. 16.
    Boscaro V, Vannini C, Fokin SI et al (2012) Characterization of “Candidatus Nebulobacter yamunensis” from the cytoplasm of Euplotes aediculatus (Ciliophora, Spirotrichea) and emended description of the family Francisellaceae. Syst Appl Microbiol 35:432–440. doi: 10.1016/j.syapm.2012.07.003 CrossRefPubMedGoogle Scholar
  17. 17.
    Beier CL, Horn M, Michel R et al (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. doi: 10.1128/AEM.68.12.6043 PubMedCentralCrossRefPubMedGoogle Scholar
  18. 18.
    Rinke C, Schmitz-Esser S, Stoecker K et al (2006) “Candidatus Thiobios zoothamnicoli”, an ectosymbiotic bacterium covering the giant marine ciliate Zoothamnium niveum. Appl Environ Microbiol 72:2014–2021. doi: 10.1128/AEM.72.3.2014-2021.2006 PubMedCentralCrossRefPubMedGoogle Scholar
  19. 19.
    Nowack ECM, Melkonian M (2010) Endosymbiotic associations within protists. Philos Trans R Soc Lond B Biol Sci 365:699–712. doi: 10.1098/rstb.2009.0188 PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    Sachs JL (2013) Origins, evolution, and breakdown of bacterial symbiosis, second edi. Encycl Biodivers 5:637–644. doi: 10.1016/B978-0-12-384719-5.00382-8 CrossRefGoogle Scholar
  21. 21.
    Sachs JL, Skophammer RG, Bansal N, Stajich JE (2014) Evolutionary origins and diversification of proteobacterial mutualists. Proc R Soc B 281:20132146. doi: 10.1098/rspb.2013.2146 PubMedCentralCrossRefPubMedGoogle Scholar
  22. 22.
    Heckmann K (1975) Omikron, ein essentieller Endosymbiont von Euplotes aediculatus. J Protozool 22:97–104. doi: 10.1111/j.1550-7408.1975.tb00949.x CrossRefGoogle Scholar
  23. 23.
    Heckmann K, Ten Hagen R, Görtz HD (1983) Freshwater Euplotes species with a 9 Type 1 cirrus pattern depend upon endosymbionts. J Protozool 30:284–289. doi: 10.1111/j.1550-7408.1983.tb02917.x CrossRefGoogle Scholar
  24. 24.
    Vannini C, Petroni G, Verni F, Rosati G (2005) Polynucleobacter bacteria in the brackish-water species Euplotes harpa (Ciliata Hypotrichia). J Eukaryot Microbiol 52:116–122. doi: 10.1111/j.1550-7408.2005.04-3319.x CrossRefPubMedGoogle Scholar
  25. 25.
    Boscaro V, Felletti M, Vannini C et al (2013) Polynucleobacter necessarius, a model for genome reduction in both free-living and symbiotic bacteria. Proc Natl Acad Sci. doi: 10.1073/pnas.1316687110 PubMedCentralPubMedGoogle Scholar
  26. 26.
    Vannini C, Boscaro V, Ferrantini F et al (2014) Flagellar movement in two bacteria of the family Rickettsiaceae: a re-evaluation of motility in an evolutionary perspective. PLoS ONE 9, e87718. doi: 10.1371/journal.pone.0087718 PubMedCentralCrossRefPubMedGoogle Scholar
  27. 27.
    Ferrantini F, Fokin SI, Modeo L et al (2009) “Candidatus Cryptoprodotis polytropus”, a novel Rickettsia-like organism in the ciliated protist Pseudomicrothorax dubius (Ciliophora, Nassophorea). J Eukaryot Microbiol 56:119–129CrossRefPubMedGoogle Scholar
  28. 28.
    Yu X, Walker D (2005) Rickettsiaceae Pinkerton 1936, 186AL emend. Dumler, Barbet, Bekker, Dasch, Palmer, Ray, Rikihisa and Rurangirwa 2001. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s Man. Syst. Bacteriol, vol III, 2nd edn. Springer-Verlag, New York, NY, pp 96–116CrossRefGoogle Scholar
  29. 29.
    Görtz HD, Schmidt H (2005) Holosporaceae fam. nov. In: Garrity G, Brenner D, Staley J, Krieg N (eds) Bergey’s Man. Syst. Bacteriol, vol 2 part C, 2nd edn. Springer, New York, NY, pp 146–160Google Scholar
  30. 30.
    Boscaro V, Fokin SI, Schrallhammer M et al (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. doi: 10.1007/s00248-012-0110-2 CrossRefPubMedGoogle Scholar
  31. 31.
    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. doi: 10.1099/00207713-32-1-140 CrossRefGoogle Scholar
  32. 32.
    Schrallhammer M, Schweikert M (2009) The killer effect of Paramecium and its causative agents. In: Fujishima M (ed) Endosymbionts in Paramecium. Microbiology Monographs 12, Berlin Heidelberg, pp 227–246CrossRefGoogle Scholar
  33. 33.
    Springer N, Ludwig W, Amann R et al (1993) Occurrence of fragmented 16S rRNA in an obligate bacterial endosymbiont of Paramecium caudatum. Proc Natl Acad Sci U S A 90:9892–9895PubMedCentralCrossRefPubMedGoogle Scholar
  34. 34.
    Montagna M, Sassera D, Epis S et al (2013) “Candidatus Midichloriaceae” fam. nov. (Rickettsiales), an ecologically widespread clade of intracellular Alphaproteobacteria. Appl Environ Microbiol 79:3241–3248. doi: 10.1128/AEM.03971-12 PubMedCentralCrossRefPubMedGoogle Scholar
  35. 35.
    Boscaro V, Schrallhammer M, Benken K et al (2013) Rediscovering the genus Lyticum, multiflagellated symbionts of the order Rickettsiales. Sci Rep 3:3305. doi: 10.1038/srep03305 PubMedCentralCrossRefPubMedGoogle Scholar
  36. 36.
    Vannini C, Ferrantini F, Schleifer KH et al (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. doi: 10.1128/AEM.03105-09 PubMedCentralCrossRefPubMedGoogle Scholar
  37. 37.
    Matsuura Y, Kikuchi Y, Meng XY et al (2012) Novel clade of alphaproteobacterial endosymbionts associated with stinkbugs and other arthropods. Appl Environ Microbiol 78:4149–4156. doi: 10.1128/AEM.00673-12 PubMedCentralCrossRefPubMedGoogle Scholar
  38. 38.
    Beninati T, Lo N, Sacchi L et al (2004) A novel alpha-proteobacterium resides in the mitochondria of ovarian cells of the tick Ixodes ricinus. Appl Environ Microbiol 70:2596–2602. doi: 10.1128/AEM.70.5.2596 PubMedCentralCrossRefPubMedGoogle Scholar
  39. 39.
    Epis S, Sassera D, Beninati T et al (2008) Midichloria mitochondrii is widespread in hard ticks (Ixodidae) and resides in the mitochondria of phylogenetically diverse species. Parasitology 135:485–494. doi: 10.1017/S0031182007004052 CrossRefPubMedGoogle Scholar
  40. 40.
    Hornok S, Földvári G, Elek V et al (2008) Molecular identification of Anaplasma marginale and rickettsial endosymbionts in blood-sucking flies (Diptera: Tabanidae, Muscidae) and hard ticks (Acari: Ixodidae). Vet Parasitol 154:354–359. doi: 10.1016/j.vetpar.2008.03.019 CrossRefPubMedGoogle Scholar
  41. 41.
    Richard S, Seng P, Parola P et al (2009) Detection of a new bacterium related to “Candidatus Midichloria mitochondrii” in bed bugs. Clin Microbiol Infect 15:84–85. doi: 10.1111/j.1469-0691.2008.02244.x CrossRefPubMedGoogle Scholar
  42. 42.
    Mediannikov O, Ivanov L, Nishikawa M et al (2004) Microorganism “Montezuma” of the order Rickettsiales: the potential causative agent of tick-borne disease in the Far East of Russia. Zh Mikrobiol Epidemiol Immunobiol 1:7–13PubMedGoogle Scholar
  43. 43.
    Fritsche TR, Horn M, Seyedirashti S et al (1999) In situ detection of novel bacterial endosymbionts of Acanthamoeba spp. phylogenetically related to members of the order Rickettsiales. Appl Environ Microbiol 65:206–212PubMedCentralPubMedGoogle Scholar
  44. 44.
    Kuo RC, Lin S (2013) Ectobiotic and endobiotic bacteria associated with Eutreptiella sp. isolated from Long Island Sound. Protist 164:60–74. doi: 10.1016/j.protis.2012.08.004 CrossRefPubMedGoogle Scholar
  45. 45.
    Longford SR, Tujula NA, Crocetti GR et al (2007) Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquat Microb Ecol 48:217–229CrossRefGoogle Scholar
  46. 46.
    Sipkema D, Holmes B, Nichols SA, Blanch HW (2009) Biological characterisation of Haliclona (?gellius) sp.: sponge and associated microorganisms. Microb Ecol 58:903–920. doi: 10.1007/s00248-009-9534-8 PubMedCentralCrossRefPubMedGoogle Scholar
  47. 47.
    Fraune S, Bosch TCG (2007) Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc Natl Acad Sci U S A 104:13146–13151. doi: 10.1073/pnas.0703375104 PubMedCentralCrossRefPubMedGoogle Scholar
  48. 48.
    Sunagawa S, Woodley CM, Medina M (2010) Threatened corals provide underexplored microbial habitats. PLoS One 5, e9554. doi: 10.1371/journal.pone.0009554 PubMedCentralCrossRefPubMedGoogle Scholar
  49. 49.
    Lloyd SJ, LaPatra SE, Snekvik KR et al (2008) Strawberry disease lesions in rainbow trout from southern Idaho are associated with DNA from a Rickettsia-like organism. Dis Aquat Organ 82:111–118. doi: 10.3354/dao01969 CrossRefPubMedGoogle Scholar
  50. 50.
    Mariconti M, Epis S, Gaibani P et al (2012) Humans parasitized by the hard tick Ixodes ricinus are seropositive to Midichloria mitochondrii: is Midichloria a novel pathogen, or just a marker of tick bite? Pathog Glob Health 106:391–396. doi: 10.1179/2047773212Y.0000000050 PubMedCentralCrossRefPubMedGoogle Scholar
  51. 51.
    Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491–499. doi: 10.1016/0378-1119(88)90066-2 CrossRefPubMedGoogle Scholar
  52. 52.
    Petroni G, Dini F, Verni F, Rosati G (2002) A molecular approach to the tangled intrageneric relationships underlying phylogeny in Euplotes (Ciliophora, Spirotrichea). Mol Phylogenet Evol 22:118–130. doi: 10.1006/mpev.2001.1030 CrossRefPubMedGoogle Scholar
  53. 53.
    Modeo L, Rosati G, Andreoli I et al (2006) Molecular systematics and ultrastructural characterization of a forgotten species: Chattonidium setense (Ciliophora, Heterotrichea). Proc Japan Acad Ser B 82:359–374. doi: 10.2183/pjab.82.359 CrossRefGoogle Scholar
  54. 54.
    Don RH, Cox PT, Wainwright BJ et al (1991) “Touchdown” PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res 19:4008. doi: 10.1093/nar/19.14.4008 PubMedCentralCrossRefPubMedGoogle Scholar
  55. 55.
    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. doi: 10.1099/ijs.0.02759-0 CrossRefPubMedGoogle Scholar
  56. 56.
    Vannini C, Schena A, Verni F, Rosati G (2004) Euplotes magnicirratus (Ciliophora, Hypotrichia) depends on its bacterial endosymbiont “Candidatus Devosia euplotis” for food digestion. Aquat Microb Ecol 36:19–28. doi: 10.3354/ame036019 CrossRefGoogle Scholar
  57. 57.
    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. doi: 10.1111/j.1550-7408.2006.00133.x CrossRefPubMedGoogle Scholar
  58. 58.
    Stahl DA, Amann R (1991) Development and application of nucleic acid probes in bacterial systematics. In: Stackebrandt E, Goodfellow M (eds) Nucleic acids techniques in bacterial systematics. John Wiley & Sons, Inc, Hoboken, NJ, USA, pp 205–248Google Scholar
  59. 59.
    Klindworth A, Pruesse E, Schweer T et al (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41, e1. doi: 10.1093/nar/gks808 PubMedCentralCrossRefPubMedGoogle Scholar
  60. 60.
    Pruesse E, Quast C, Knittel K et al (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. doi: 10.1093/nar/gkm864 PubMedCentralCrossRefPubMedGoogle Scholar
  61. 61.
    Cole JR, Wang Q, Cardenas E et al (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145. doi: 10.1093/nar/gkn879 PubMedCentralCrossRefPubMedGoogle Scholar
  62. 62.
    Ludwig W, Strunk O, Westram R et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371. doi: 10.1093/nar/gkh293 PubMedCentralCrossRefPubMedGoogle Scholar
  63. 63.
    Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. doi: 10.1038/nmeth.2109 PubMedCentralCrossRefPubMedGoogle Scholar
  64. 64.
    Ronquist F, Teslenko M, van der Mark P et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. doi:  10.1093/sysbio/sys029.
  65. 65.
    Guindon S, Dufayard J-F, Lefort V et al (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. doi: 10.1093/sysbio/syq010 CrossRefPubMedGoogle Scholar
  66. 66.
    Tamura K, Peterson D, Peterson N et al (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi: 10.1093/molbev/msr121 PubMedCentralCrossRefPubMedGoogle Scholar
  67. 67.
    Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. doi: 10.1007/BF01731581 CrossRefPubMedGoogle Scholar
  68. 68.
    Amann R, Binder BJ, Olson RJ et al (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microb 56:1919–1925Google Scholar
  69. 69.
    Vannini C, Ferrantini F, Verni F, Petroni G (2013) A new obligate bacterial symbiont colonizing the ciliate Euplotes in brackish and freshwater: “Candidatus Protistobacter heckmanni”. Aquat Microb Ecol 70:233–243. doi: 10.3354/ame01657 CrossRefGoogle Scholar
  70. 70.
    Hahn MW, Pöckl M, Wu QL (2005) Low intraspecific diversity in a polynucleobacter subcluster population numerically dominating bacterioplankton of a freshwater pond. Appl Environ Microbiol 71:4539–4547. doi: 10.1128/AEM.71.8.4539-4547.2005 PubMedCentralCrossRefPubMedGoogle Scholar
  71. 71.
    Manz W, Amann R, Ludwig W et al (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst Appl Microbiol 15:593–600, doi: http://dx.doi.org/10.1016/S0723-2020(11)80121-9
  72. 72.
    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. doi: 10.1093/nar/gkl856 PubMedCentralCrossRefPubMedGoogle Scholar
  73. 73.
    Boscaro V, Fokin SI, Verni F, Petroni G (2012) Survey of Paramecium duboscqui using three markers and assessment of the molecular variability in the genus Paramecium. Mol Phylogenet Evol 65:1004–1013. doi: 10.1016/j.ympev.2012.09.001 CrossRefPubMedGoogle Scholar
  74. 74.
    Curds CR (1975) A guide to the species of the genus Euplotes (Hypotrichida, Ciliatea). Bull Br Museum (Natural Hist Zoo) 28:1–61Google Scholar
  75. 75.
    Fokin SI, Di Giuseppe G, Erra F, Dini F (2008) Euplotespora binucleata n. gen., n. sp. (Protozoa: Microsporidia), a parasite infecting the hypotrichous ciliate Euplotes woodruffi, with observations on microsporidian infections in Ciliophora. J Eukaryot Microbiol 55:214–228. doi: 10.1111/j.1550-7408.2008.00322.x CrossRefPubMedGoogle Scholar
  76. 76.
    Dai R, Xu K, He Y (2013) Morphological, physiological, and molecular evidences suggest that Euplotes parawoodruffi is a junior synonym of Euplotes woodruffi (Ciliophora, Euplotida). J Eukaryot Microbiol 60:70–78. doi: 10.1111/jeu.12007 CrossRefPubMedGoogle Scholar
  77. 77.
    Fan X, Huang J, Lin X et al (2010) Morphological and molecular characterization of Euplotes encysticus (Protozoa: Ciliophora: Euplotida). J Mar Biol Assoc United Kingdom 90:1411–1416. doi: 10.1017/S002531541000038X CrossRefGoogle Scholar
  78. 78.
    Fokin SI, Schrallhammer M, Chiellini C et al (2014) Free-living ciliates as potential reservoirs for eukaryotic parasites: occurrence of a trypanosomatid in the macronucleus of Euplotes encysticus. Parasit Vectors 7:203. doi: 10.1186/1756-3305-7-203 PubMedCentralCrossRefPubMedGoogle Scholar
  79. 79.
    Lynn D (2008) The Ciliated Protozoa, 3rd edn., p 605Google Scholar
  80. 80.
    Achilles-Day U, Pröschold T, Day J (2008) Phylogenetic position of the freshwater ciliate Euplotes daidaleos within the family of Euplotidae obtained from small subunit rDNA gene sequence. Denisia 23:411–416Google Scholar
  81. 81.
    Jiang J, Zhang Q, Hu X et al (2010) Two new marine ciliates, Euplotes sinicus sp. nov. and Euplotes parabalteatus sp. nov., and a new small subunit rRNA gene sequence of Euplotes rariseta (Ciliophora, Spirotrichea, Euplotida). Int J Syst Evol Microbiol 60:1241–1251. doi: 10.1099/ijs.0.012120-0 CrossRefPubMedGoogle Scholar
  82. 82.
    Miao M, Song W, Chen Z et al (2007) A unique euplotid ciliate, Gastrocirrhus (Protozoa, Ciliophora): Assessment of its phylogenetic position inferred from the small subunit rRNA gene sequence. J Eukaryot Microbiol 54:371–378. doi: 10.1111/j.1550-7408.2007.00271.x CrossRefPubMedGoogle Scholar
  83. 83.
    Kimes NE, Johnson WR, Torralba M et al (2013) The Montastraea faveolata microbiome: ecological and temporal influences on a Caribbean reef-building coral in decline. Environ Microbiol 15:2082–2094. doi: 10.1111/1462-2920.12130 CrossRefPubMedGoogle Scholar
  84. 84.
    Yonezawa F (1985) New hypotrichous ciliate Euplotes encysticus sp. nov. J Sci Hiroshima Univ 32:35–45Google Scholar
  85. 85.
    Murray RG, Schleifer KH (1994) Taxonomic notes: a proposal for recording the properties of putative taxa of procaryotes. Int J Syst Bacteriol 44:174–176. doi: 10.1099/00207713-44-1-174 CrossRefPubMedGoogle Scholar
  86. 86.
    Murray RG, Stackebrandt E (1995) Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int J Syst Bacteriol 45:186–187. doi: 10.1099/00207713-45-1-186 CrossRefPubMedGoogle Scholar
  87. 87.
    Berk SG, Faulkner G, Garduño E et al (2008) Packaging of live Legionella pneumophila into pellets expelled by Tetrahymena spp. does not require bacterial replication and depends on a Dot/Icm-mediated survival mechanism. Appl Environ Microbiol 74:2187–2199. doi: 10.1128/AEM.01214-07 PubMedCentralCrossRefPubMedGoogle Scholar
  88. 88.
    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. doi: 10.1099/00221287-140-6-1253 CrossRefPubMedGoogle Scholar
  89. 89.
    Molmeret M, Santic’ M, Asare R et al (2007) Rapid escape of the dot/icm mutants of Legionella pneumophila into the cytosol of mammalian and protozoan cells. Infect Immun 75:3290–3304. doi: 10.1128/IAI.00292-07 PubMedCentralCrossRefPubMedGoogle Scholar
  90. 90.
    Bazzocchi C, Mariconti M, Sassera D et al (2013) Molecular and serological evidence for the circulation of the tick symbiont Midichloria (Rickettsiales: Midichloriaceae) in different mammalian species. Parasit Vectors 6:350. doi: 10.1186/1756-3305-6-350 PubMedCentralCrossRefPubMedGoogle Scholar

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© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Marcus V. X. Senra
    • 1
    • 3
  • Roberto J. P. Dias
    • 2
    • 3
  • Michele Castelli
    • 4
  • Inácio D. Silva-Neto
    • 2
  • Franco Verni
    • 4
  • Carlos A. G. Soares
    • 1
    Email author
  • Giulio Petroni
    • 4
    Email author
  1. 1.Departamento de GenéticaUniversidade Federal do Rio de Janeiro, UFRJRio de JaneiroBrazil
  2. 2.Departamento de ZoologiaUniversidade Federal do Rio de Janeiro, UFRJRio de JaneiroBrazil
  3. 3.Departamento de ZoologiaUniversidade Federal de Juiz de Fora, UFJFRio de JaneiroBrazil
  4. 4.Department of BiologyUniversity of PisaPisaItaly

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