Skip to main content

Advertisement

Log in

Candidatus Hafkinia simulans” gen. nov., sp. nov., a Novel Holospora-Like Bacterium from the Macronucleus of the Rare Brackish Water Ciliate Frontonia salmastra (Oligohymenophorea, Ciliophora): Multidisciplinary Characterization of the New Endosymbiont and Its Host

  • Host Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

We characterized a novel Holospora-like bacterium (HLB) (Alphaproteobacteria, Holosporales) living in the macronucleus of the brackish water ciliate Frontonia salmastra. This bacterium was morphologically and ultrastructurally investigated, and its life cycle and infection capabilities were described. We also obtained its 16S rRNA gene sequence and performed in situ hybridization experiments with a specifically-designed probe. A new taxon, “Candidatus Hafkinia simulans”, was established for this HLB. The phylogeny of the family Holosporaceae based on 16S rRNA gene sequences was inferred, adding to the already available data both the sequence of the novel bacterium and those of other Holospora and HLB species recently characterized. Our phylogenetic analysis provided molecular support for the monophyly of HLBs and placed the new endosymbiont as the sister genus of Holospora. Additionally, the host ciliate F. salmastra, recorded in Europe for the first time, was concurrently described through a multidisciplinary study. Frontonia salmastra’s phylogenetic position in the subclass Peniculia and the genus Frontonia was assessed according to 18S rRNA gene sequencing. Comments on the biodiversity of this genus were added according to past and recent literature.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

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

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Görtz HD (1988) Endocytobiosis. In: Görtz HD (ed) Paramecium. Springer Verlag, Berlin, pp 393–405

    Chapter  Google Scholar 

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

    Article  PubMed  Google Scholar 

  4. Fokin SI (2012) Frequency and biodiversity of symbionts in representatives of the main classes of Ciliophora. Eur. J. Protistol. 48:138–148

    Article  PubMed  Google Scholar 

  5. Fujishima M (2009) Endosymbionts in Paramecium. In: Fujishima M (ed) Münster: microbiology monograph, vol 12. Springer-Verlag, Berlin, p 252

    Google Scholar 

  6. Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8:218–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Modeo L, Petroni G, Lobban CS, Verni F, Vannini C (2013) Morphological, ultrastructural, and molecular characterization of Euplotidium rosati n. sp. (Ciliophora, Euplotida) from Guam. J. Eukaryot. Microbiol. 60:25–36

    Article  CAS  PubMed  Google Scholar 

  8. Castelli M, Sassera D, Petroni G (2016) Biodiversity of “non-model” Rickettsiales and their association with aquatic organisms. In: Thomas S (ed) Rickettsiales. Springer, Cham, pp 59–91

    Chapter  Google Scholar 

  9. Castelli M, Serra V, Senra MVX, Basuri CK, Soares CAG, Fokin SI, Modeo L, Petroni G (2018) The hidden world of Rickettsiales symbionts: “Candidatus Spectririckettsia obscura,” a novel bacterium found in Brazilian and Indian Paramecium caudatum. Microb. Ecol. https://doi.org/10.1007/s00248-018-1243-8

  10. Nitla V, Serra V, Fokin SI, Modeo L, Verni F, Sandeep BV, Kalavati C, Petroni G (2018) Critical revision of the family Plagiopylidae (Ciliophora: Plagiopylea), including the description of two novel species, Plagiopyla ramani and Plagiopyla narasimhamurthii, and redescription of Plagiopyla nasuta Stein, 1860 from India. Zool J Linnean Soc XX, p 1–45. https://doi.org/10.1093/zoolinnean/zly041

  11. Görtz HD (1996) Symbiosis in ciliates. In: Hausmann K, Bradbury PS (eds) Ciliates. Cells as organisms. Fischer, Stuttgart, pp 441–462

    Google Scholar 

  12. Görtz HD, Schmidt HJ (2005) Genus Holospora. In: Garrity et al (eds) Bergey’s manual of systematic bacteriology, vol 2, part C2nd edn. Springer, New York, pp 149–151

    Chapter  Google Scholar 

  13. Görtz HD, Fokin SI (2009) Diversity of endosymbiotic bacteria in Paramecium. In: Fujishima M (ed) Endosymbionts in Paramecium. microbiology monographs Vol. 12, chapter 6. Springer-Verlag, Heidelberg, pp 132–160

    Google Scholar 

  14. Fokin SI, Görtz HD (2009) Diversity of Holospora bacteria in Paramecium and their characterization. In: Fujishima M (ed) Endosymbionts in Paramecium. Microbiology monograph Vol. 12, chapter 7. Springer-Verlag, Heidelberg, pp 161–199

    Chapter  Google Scholar 

  15. 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

    Article  CAS  PubMed  Google Scholar 

  16. Lanzoni O, Fokin S, Lebedeva N, Migunova A, Petroni G, Potekhin A (2016) Rare freshwater ciliate Paramecium chlorelligerum Kahl, 1935 and its macronuclear symbiont “Candidatus Holospora parva”. PLoS ONE 11(12):e0167928. https://doi.org/10.1371/journal.pone.0167928

  17. Hafkine MW (1890) Maladies infectieuses des paramécies. Ann Inst Pasteur 4:363–379

    Google Scholar 

  18. Potekhin A, Schweikert M, Nekrasova I, Vitali V, Schwarzer S, Anikina A, Kaltz O, Petroni G, Schrallhammer M (2018) Complex life cycle, broad host range and adaptation strategy of the intranuclear Paramecium symbiont Preeria caryophila comb. nov. FEMS Microbiol. Ecol. 94(7):fiy076

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  20. Serra V, Fokin SI, Castelli M, Basuri CK, Nitla VM, Verni F, Sandeep BV, Kalavathi C, Petroni G (2016) “Candidatus Gortzia shahrazadis”, a novel endosymbiont of Paramecium multimicronucleatum and revision of the biogeographical distribution of Holospora-like bacteria. Front. Microbiol. 7:1704. https://doi.org/10.3389/fmicb.2016.01704

    Article  PubMed  PubMed Central  Google Scholar 

  21. Preer LB (1969) Alpha, an infectious macronuclear symbiont of Paramecium aurelia. J Protozool 16:570–578

    Article  CAS  PubMed  Google Scholar 

  22. 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 

  23. 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

    Article  Google Scholar 

  24. Fokin SI, Brigge 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(Supp l1):19–24

    Article  Google Scholar 

  25. Fokin SI (2000) Host specificity of Holospora and its relationships with Paramecium phylogeny. Japan J Protozool 33:94

    Google Scholar 

  26. 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. https://doi.org/10.1099/ijs.0.046631-0

    Article  PubMed  Google Scholar 

  27. Dohra H, Tanaka K, Suzuki T, Fujishima M, Suzuki H (2014) Draft genome sequences of three Holospora species (Holospora obtusa, Holospora undulata, and Holospora elegans), endonuclear symbiotic bacteria of the ciliate Paramecium caudatum. FEMS Microbiol. Lett. 359:16–18. https://doi.org/10.1111/1574-6968.12577

    Article  CAS  PubMed  Google Scholar 

  28. Jankowski AW (1964) Morphology and evolution of ciliophora. III. Diagnoses and phylogenesis of 53 sapropelebionts, mainly of the order Heterotrichida. Arch. Protistenkd. 107:185–294

    Google Scholar 

  29. Esteban G, Fenchel T, Finlay B (1995) Diversity of free-living morphospecies in the ciliates genus Metopus. Arch. Protistenkd. 146:137–164

    Article  Google Scholar 

  30. von Stein F (1867) Der Organismus der Infusionsthiere. II . Abth 2 Naturgeschichte der heterotrichen Infusorien. Wilhelm Engelmann, Leipzig

    Google Scholar 

  31. Görtz HD, Wiemann M (1987) Colonization of the ciliate Stentor multiformis by three different endocytobionts. Endocyt Cell Res 4:177–184

    Google Scholar 

  32. Balbiani EG (1892) Nouvelles recherches expérimentales sur la mérotomie des infusoires ciliés. Ann Microgr 5:1–25

    Google Scholar 

  33. Görtz HD, Maier G (1991) A bacterial infection in a ciliate from sewage sludge. Endocyt Cell Res 8:45–52

    Google Scholar 

  34. Kirby H (1941) A parasite of the macronucleus of Vorticella. J Parasit 27:311–314

    Google Scholar 

  35. Platt-Rohloff L (1996) Untersuchungen an bakteriellen Endosymbiosen in neu isolierten Ciliaten aus marinen und aus Brackwasser-Biotopen. Inauguraldissertion zur Erlangung des Doktorgrades der Fachbereichs Biologie der Freien Universitat Berlin

  36. Laval M (1970) Presence de bacteries intranucleaires chez Zoothamnium pelagicum (Cilie Peritriche) leur role dans la formation des pigments intracytoplasmiques des zoides. Septième Congrès International la Microscopie Électronique, Grenoble, 403–404

  37. Hausmann K, Hausmann E (1981) Structural studies on Trichodina pediculus (Ciliophora, Peritricha). II. The adhesive disc. J Ultrastrust Res 74:144–155

    Article  CAS  Google Scholar 

  38. Dragesco J, Dragesco-Kernéis A (1986) Cilies libres de l’Afrique intertropicale. Introduction a la connaissance et a l’etude des cilies. Faune Tropicale 26:1–559

    Google Scholar 

  39. Skovorodkin IN (1990) A device for immobilization of biological objects in light microscope studies. Cytology (Sankt-Petersburg) 32:301–302

    CAS  Google Scholar 

  40. Corliss JO (1953) Silver impregnation of ciliated protozoa by the Chatton-Lwoff technique. Stain. Technol. 28:97–100

    Article  CAS  PubMed  Google Scholar 

  41. Fokin SI, Gortz HD (1993) Caedibacter macronucleorum sp. nov., a bacterium inhabiting the macronucleus of Paramecium duboscqui. Arch. Protistenkd. 143:319–324

    Article  Google Scholar 

  42. 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

    Article  CAS  PubMed  Google Scholar 

  43. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41:590–596. https://doi.org/10.1093/nar/gks1219

    Article  CAS  Google Scholar 

  46. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696–704

    Article  PubMed  Google Scholar 

  47. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna D, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539–542. https://doi.org/10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  48. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9:772–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Fokin SI, Schweikert M, Brummer F, Gortz HD (2005) Spirostomum spp. (Ciliophora, Protista), a suitable system for endocytobiosis research. Protoplasma 225:93–102

    Article  CAS  PubMed  Google Scholar 

  50. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Manz W, Amann R, 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

    Article  Google Scholar 

  52. 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. 37:141–145. https://doi.org/10.1093/nar/gkn879

    Article  CAS  Google Scholar 

  53. Andreoli I, Mangini L, Ferrantini F, Santangelo G, Verni F, Petroni G (2009) Molecular phylogeny of unculturable Karyorelictea (Alveolata, Ciliophora). Zool Scripta 38:651–662

    Article  Google Scholar 

  54. Modeo L, Fokin SI, Boscaro V, Andreoli I, Ferrantini F, Rosati G, Verni F, Petroni G (2013) Morphology, ultrastructure and molecular phylogeny of the ciliate Sonderia vorax with insights into the systematics of order Plagiopylida. BMC Microbiol. 13:40. https://doi.org/10.1186/1471-2180-13-40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Bullington WE (1939) A study of spiraling in the ciliate Frontonia with a review of the genus and a description of two new species. Arch. Protistenkd. 92:10–66

    Google Scholar 

  56. Berninger UG, Finlay BJ, Canter HM (1986) The spatial distribution and ecology of zoochlorellae-bearing ciliate in a productive pond. J Protozool 33:557–563

    Article  Google Scholar 

  57. Fokin SI, Schweikert M (2003) Bacterial endobionts of Frontonia leucas (Ciliophora, Peniculida). Europ J Protistol 39:311–318

    Article  Google Scholar 

  58. Rossi A, Boscaro V, Carducci D, Serra V, Modeo L, Verni F, Fokin SI, Petroni G (2016) Ciliate communities and hidden biodiversity in freshwater biotopes of the Pistoia province (Tuscany, Italy). Europ J Protistol 53:11–19

    Article  Google Scholar 

  59. Alekperov IH (2005) Atlas of freeliving ciliates (classes Kinetofragminophora, Colpodea, Oligohymenophorea, Polyhymenophora). Borcali NPM, Baku 309 p. (in Russian)

    Google Scholar 

  60. 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. Endocytobiosis Cell Res 12:49–55

    Google Scholar 

  61. Fokin SI (2015) Release of Holospora-like bacteria in different ciliate species. Abstracts of VII ECOP-ISOP joint meeting. Sevilla, Spain, 279

  62. Hess S, Suthaus A, Melkonian M (2016) Characterisation of “Candidatus Finniella” (Rickettsiales, Alphaproteobacteria), novel endosymbionts of Viridiraptorid amoeboflagellates (Cercozoa, Rhizaria). Appl. Environ. Microbiol. 82:659–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Szokoli F, Castelli M, Sabaneyeva E, Schrallhammer M, Krenek S, Doak TG, Berendonk TU, Petroni G (2016) Disentangling the taxonomy of Rickettsiales and description of two novel symbionts (“Candidatus Bealeia paramacronuclearis” and “Candidatus Fokinia cryptica”) sharing the cytoplasm of the ciliate protist Paramecium biaurelia. Appl Environ Microb 82:7236–7247

    Article  CAS  Google Scholar 

  64. Schrallhammer M, Castelli M, Petroni G (2018) Phylogenetic relationships among endosymbiotic R-body producer: bacteria providing their host the killer trait. Syst. Appl. Microbiol. 41:213–220

    Article  PubMed  Google Scholar 

  65. Tashyreva D, Prokopchuk G, Votýpka J, Yabuki A, Horák A, Lukeš J (2018) Life cycle, ultrastructure, and phylogeny of new diplonemids and their endosymbiotic bacteria. mBio 9(2):e02447–e02417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer KH, Whitman WB, Euzéby J, Amann R, Rosselló-Móra R (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645. https://doi.org/10.1038/nrmicro3330

    Article  CAS  PubMed  Google Scholar 

  67. Rosselló-Móra R, Amann R (2015) Past and future species definitions for Bacteria and archaea. Syst. Appl. Microbiol. 38:209–216

    Article  PubMed  Google Scholar 

  68. Fokin SI, Schrallhammer M, Vannini C, Ferrantini F, Petroni G, Görtz HD (2006b) New Holospora endocytobionts in some common ciliates. In: 25th Wiss Tag Deut Gesel Protozool Liebenwalde (Berlin), 28

  69. Ferrantini F, Fokin SI, Vannini C, Verni F, Petroni G (2007) Characterization of a novel Holospora-like symbiont from Frontonia (Ciliophora, Oligohymenophorea). J. Eukaryot. Microbiol. 54:29S

    Article  CAS  Google Scholar 

  70. Long H, Song W, Gong J, Hu X, Ma H, Zhu M, Wang M (2005) Frontonia lynni n. sp., a new marine ciliate (Protozoa, Ciliophora, Hymenostomatida) from Qingdao, China. Zootaxa 1003:57–64

    Article  Google Scholar 

  71. Long H, Song W, Al-Rasheid KAS, Wang Y, Yi Z, Al-Quraishy SA, Lin X, Al-Farraj SA (2008) Taxonomic studies on three marine species of Frontonia from northern China: F. didieri n. sp., F. multinucleata n. sp. and F. tchibisovae Burkovsky 1970 (Ciliophora: Peniculida). Zootaxa 1687:35–50

    Article  Google Scholar 

  72. Gao S, Chen ZG, Shao C, Long HA, Al-Rasheid KA, Song WB (2008) Reconsideration of the phylogenetic position of Frontonia-related Peniculia (Ciliophora, Protozoa) inferred from the small subunit ribosomal RNA gene sequences. Acta Protozool. 47:47–54

    CAS  Google Scholar 

  73. Fan X, Chen X, Song W, Al-Rasheid KA, Warren A (2011) Two novel marine Frontonia species, Frontonia mengi spec. nov. and Frontonia magna spec. nov. (Protozoa; Ciliophora), with notes on their phylogeny based on small-subunit rRNA gene sequence data. Int J Syst Evol Microb 61:1476–1486

    Article  Google Scholar 

  74. Fan X, Lin X, Liu W, Xu Y, Al-Farra SA, Al-Rasheid KA, Warren A (2013) Morphology of three new marine Frontonia species (Ciliophora; Peniculida) with note on the phylogeny of this genus. Europ J Protist 49:312–323

    Article  Google Scholar 

  75. Pan X, Gao F, Liu W, Fan X, Warren A, Song W (2013a) Morphology and SSU rRNA gene sequences of three Frontonia species, including a description of F. subtropica spec. nov. (Ciliophora, Peniculida). Europ J Protistol 49:67–77

    Article  Google Scholar 

  76. Pan X, Liu W, Yi Z, Fan X, Al-Rashid K, Lin X (2013b) Studies on three diverse Frontonia species (Ciliophora, Peniculida), with brif notes on 14 marine or brackish congeners. Acta Protozool. 52:35–49

    Google Scholar 

  77. Fokin SI, Andreoli I, Verni F, Petroni G (2006a) Apofrontonia dohrni sp. n. and the phylogenetic relationships within Peniculia (Protozoa, Ciliophora, Oligohymenophorea). Zool Scripta 35:289–300

    Article  Google Scholar 

  78. Andreoli I, Fokin SI, Verni F, Petroni G (2007) Phylogenetic relationships within Frontoniids. J. Eukaryot. Microbiol. 54:28S

    Article  Google Scholar 

  79. Cai X, Wang C, Pan X, El-Serehy HA, Mu W, Gao F, Qiu Z (2018) Morphology and systematics of two freshwater Frontonia species (Ciliophora, Peniculida) from northeastern China, with comparisons among the freshwater Frontonia spp. Europ J Protistolo 63:105–116

    Article  Google Scholar 

  80. Xu Y, Gao F, Fan X (2018) Reconsideration of the systematics of Peniculida (Protista, Ciliophora) based on SSU rRNA gene sequences and new morphological features of Marituja and Disematostoma. Hydrobiologia 806:313–331

    Article  Google Scholar 

  81. Chen Y, Zhao Y, Pan X, Ding W, Al-Rasheid KA, Qiu Z (2014) Morphology and phylogeny of a new Frontonia ciliate, F. paramagna spec. nov. (Ciliophora, Peniculida) from Harbin, Northeast China. Zootaxa 3827:375–386

    Article  PubMed  Google Scholar 

  82. Zhao Y, Yi Z, Gentekaki E, Zhan A, Al-Farraj SA, Song W (2016) Utility of combining morphological characters, nuclear and mitochondrial genes: an attempt to resolve the conflicts of species identification for ciliated protists. Mol Phylogen Evol 94:718–729

    Article  Google Scholar 

  83. Jurand A, Lipps HJ (1973) Two types of mitochondria in Euplotes minuta. Arch. Protistenkd. 115:133–136

    Google Scholar 

  84. Quennerstedt A (1869) Bidrag till Sveriges Infusorie-fauna III. Acta Univ Lund 6:1–35

    Google Scholar 

  85. Kahl A (1931) Holotricha. In: Dahl F (ed) Die Tierwelt Deutschlands and der angrenzenden Meeresteile. 21 Teil. Urtiere oder Protozoa. G. Fisher, Jena, pp S.181–S.398

    Google Scholar 

  86. Fokin SI (2008) Rediscovery and characterisation of Frontonia fusca (Quennerstedt, 1869) Kahl, 1931 (Ciliphora, Peniculia). Denisia 23:251–259

    Google Scholar 

  87. Petz W, Song W, Wilbert N (1995) Taxonomy and ecology of the ciliate fauna (Protozoa, Ciliphora) in the endopagial and pelagial of the Weddell Sea, Antarctica. Stapfia 40:1–223

    Google Scholar 

  88. Strüder-Kypke MC, Wright ADG, Fokin SI, Lynn DH (2000) Phylogenetic relationships of the subclass Peniculia (Oligohymenophorea, Ciliophora) inferred from small subunit rRNA gene sequences. J Euk Microbiol 47:419–429

    Article  PubMed  Google Scholar 

  89. Finlay BJ, Berninger UG, Stewart LJ, Hindle RM, Davidson W (1987) Some factors controlling the distribution of two pond-dwelling ciliates with algal symbionts (Frontonia vernalis and Euplotes daidaleos). J Protozool 34:349–356

    Article  Google Scholar 

  90. Esteban GF, Fenchel T, Finlay BJ (2010) Mixotrophy in ciliates. Protist 161:621–641. https://doi.org/10.1016/j.protis.2010.08.002

    Article  CAS  PubMed  Google Scholar 

  91. Ehrenberg CG (1838) Die infusionsthierchen als vollkommene organismen. Voss, Leipzig

    Book  Google Scholar 

  92. Fokin SI (2017) The genus Frontonia Ehrenberg, 1833. Unfinished story. Inter Congr Protistol 30th July–4th August 2017. Prague, Czech Republic. Book of abstracts:77

Download references

Acknowledgments

The authors are grateful to Simone Gabrielli for his patient and precious assistance in tree editing.

Funding

This research was supported by a grant from Italian Research Ministry (MIUR – Ministero Italiano dell’ Università e della Ricerca) to S.I. Fokin; and by the PRA_2018_63 project from University of Pisa to G. Petroni.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Sergei I. Fokin or Valentina Serra.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fokin, S.I., Serra, V., Ferrantini, F. et al.Candidatus Hafkinia simulans” gen. nov., sp. nov., a Novel Holospora-Like Bacterium from the Macronucleus of the Rare Brackish Water Ciliate Frontonia salmastra (Oligohymenophorea, Ciliophora): Multidisciplinary Characterization of the New Endosymbiont and Its Host. Microb Ecol 77, 1092–1106 (2019). https://doi.org/10.1007/s00248-018-1311-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-018-1311-0

Keywords

Profiles

  1. Giulio Petroni