Microbial Ecology

, Volume 78, Issue 1, pp 232–242 | Cite as

Detecting Associations Between Ciliated Protists and Prokaryotes with Culture-Independent Single-Cell Microbiomics: a Proof-of-Concept Study

  • Alessia Rossi
  • Alessio Bellone
  • Sergei I. Fokin
  • Vittorio Boscaro
  • Claudia VanniniEmail author
Host Microbe Interactions


Symbioses between prokaryotes and microbial eukaryotes, particularly ciliated protists, have been studied for a long time. Nevertheless, researchers have focused only on a few host genera and species, mainly due to difficulties in cultivating the hosts, and usually have considered a single symbiont at a time. Here, we present a pilot study using a single-cell microbiomic approach to circumvent these issues. Unicellular ciliate isolation followed by simultaneous amplification of eukaryotic and prokaryotic markers was used. Our preliminary test gave reliable and satisfactory results both on samples collected from different habitats (marine and freshwater) and on ciliates belonging to different taxonomic groups. Results suggest that, as already assessed for many macro-organisms like plants and metazoans, ciliated protists harbor distinct microbiomes. The applied approach detected new potential symbionts as well as new hosts for previously described ones, with relatively low time and cost effort and without culturing. When further developed, single-cell microbiomics for ciliates could be applied to a large number of studies aiming to unravel the evolutionary and ecological meaning of these symbiotic systems.


Microbiota Microbiomics Symbiosis SSU rRNA gene Bacterial symbionts Ciliates 



This work was supported by the University of Pisa (565-60%2016, 565-60%2017, PRA_2018_63) and by the Italian Ministry of University and Research (565-FFABR 2017). The authors wish to thank Simone Gabrielli for the help with graphic artworks and Irene Barbagli for the help in sampling. The authors are grateful to the Migliarino San Rossore Massaciuccoli Regional Park for giving permission for sampling.

Supplementary material

248_2018_1279_MOESM1_ESM.doc (30 kb)
Online Resource 1 Table of biodiversity indexes. Average values of evenness and richness indexes (DOC 29.5 kb)
248_2018_1279_MOESM2_ESM.doc (32 kb)
Online Resource 2 Tables with results of Permanova tests between different groups performed with different metrics. (DOC 32 kb)
248_2018_1279_MOESM3_ESM.eps (525 kb)
Online Resource 3 Relative abundances of the ten most frequent bacterial phyla in the obtained libraries are shown in the bar plot. Proteobacteria is always the dominant phylum. The total number of phyla is higher in control communities then in ciliate microbiomes. CM: ciliate microbiomes. CC: control communities (EPS 525 kb)


  1. 1.
    Gast RJ, Sanders RW, Caron DA (2009) Ecological strategies of protists and their symbiotic relationships with prokaryotic microbes. Trends Microbiol. 17:563–569CrossRefPubMedGoogle Scholar
  2. 2.
    Dziallas C, Allgaier M, Monaghan MT, Grossart HP (2012) Act together – implications of symbioses in aquatic ciliates. Front Microbiol 3:288. CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Nat Acad Sci 110:3229–3236CrossRefPubMedGoogle Scholar
  4. 4.
    Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol. 14:209. CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    de Bary A (1879) Die Erscheinung der Symbiose, ed Trübner KJ (Verlag von Karl,Strassburg)Google Scholar
  6. 6.
    Margulis L, Fester R (1991) Symbiosis as a source of evolutionary innovation: speciation and morphogenesis, Cambridge (Mass), MIT pressGoogle Scholar
  7. 7.
    Shropshire JD, Bordenstein SR (2016) Speciation by symbiosis: the microbiome and behavior. mBio 7:e01785–e01715. CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Desai MS, Strassert JFH, Meuser K, Hertel H, Ikeda-Ohtsubo W, Radek R, Brune A (2010) Strict cospeciation of devescovinid flagellates and Bacteroidales ectosymbionts in the gut of dry-wood termites (Kalotermitidae). Environ Microbiol 12:2120–2132PubMedGoogle Scholar
  9. 9.
    Edgcomb VP (2016) Marine protist associations and environmental impacts across trophic levels in the twilight zone and below. Curr. Opin. Microbiol. 31:169–175CrossRefPubMedGoogle Scholar
  10. 10.
    Görtz HD (2006) Symbiotic associations between ciliates and prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 364–402CrossRefGoogle Scholar
  11. 11.
    Schulz F, Lagkouvardos I, Wascher F, Aistleitner K, Kostanjšek R, Horn M (2014) Life in an unusual intracellular niche: a bacterial symbiont infecting the nucleus of amoebae. ISME J 8:1634–1644CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Yubuki N, Edgcomb VP, Bernhard JM, Leander BS (2009) Ultrastructure and molecular phylogeny of Calkinsia aureus: cellular identity of a novel clade of deep-sea euglenozoans with epibiotic bacteria. BMC Microbiol. 9:16. CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Claparéde E, Lachmann J (1858-1861) Etudes sur les infusoires et les rhizopodes, vol 1-2. Kessmann, GenevaGoogle Scholar
  14. 14.
    Müller J (1856) Einige Beobschtungen an Infusorien. Monatsber Preuss Akad Wissensch, pp 389–393Google Scholar
  15. 15.
    Boscaro V, Felletti M, Vannini C, Ackerman MS, Chain PS, Malfatti S, Vergez LM, Shin M, Doak TG, Lynch M, Petroni G (2013) Polynucleobacter necessarius, a model for genome reduction in both free-living and symbiotic bacteria. Proc Nat Acad Sci 110(46):18590–18595CrossRefPubMedGoogle Scholar
  16. 16.
    Bright M, Espada-Hinojosa S, Lagkouvardos I, Volland JM (2014) The giant ciliate Zoothamnium niveum and its thiotrophic epibiont “Candidatus Thiobios zoothamnicoli”: a model system to study interspecies cooperation. Front Microbiol 5:145. CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Filker S, Kaiser M, Rosselló-Mora R, Dunthorn M, Lax G, Stoeck T (2014) “Candidatus Haloectosymbiotes riaformosensis” (Halobacteriaceae), an archaeal ectosymbiont of the hypersaline ciliate Platynematumsalinarum. Syst Appl Microbiol 37:244–251CrossRefPubMedGoogle Scholar
  18. 18.
    Fokin SI, Görtz HD (2009) Diversity of Holospora-bacteria in Paramecium and their characterization. In: Fujishima M (ed) Endosymbionts in Paramecium, microbiology monographs, 12. Springer-Verlag, Heidelberg, pp 161–199CrossRefGoogle Scholar
  19. 19.
    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 Nat Acad Sci U S A 97:1813–1817CrossRefGoogle Scholar
  20. 20.
    Seah BKB, Schwaha T, Volland JM, Huettel B, Dubilier N, Gruber-Vodicka HR (2017) Specificity in diversity: single origin of a widespread ciliate-bacteria symbiosis. P Roy Soc B-Biol Sci 284:20170764CrossRefGoogle Scholar
  21. 21.
    Zaila KE, Doak TG, Ellerbrock H, Tung CH, Martins ML, Kolbin D, Yao MC, Cassidy-Hanley DM, Clark TG, Chang WJ (2017) Diversity and universality of endosymbiotic rickettsia in the fish parasite Ichthyophthirius multifiliis. Front Microbiol 8:189. CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Boscaro V, Kolisko M, Felletti M, Vannini C, Lynn DH, Keeling PJ (2017) Parallel genome reduction in symbionts descended from closely related free-living bacteria. Nat Ecol Evol 1:1160–1167CrossRefPubMedGoogle Scholar
  23. 23.
    Hirakata Y, Oshiki M, Kuroda K, Hatamoto M, Kubota K, Yamaguchi T, Harada H, Araki N (2015) Identification and detection of prokaryotic symbionts in the ciliate Metopus from anaerobic granular sludge. Microbes Environ 30:335–338CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Lanzoni O, Fokin SI, Lebedeva N, Migunova A, Petroni G, Potekhin A (2016) Rare freshwater ciliate Paramecium chlorelligerum Kahl, 1935 and its macronuclear symbiotic bacterium “Candidatus Holospora parva”. PLoS One 11:e0167928. CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Schrallhammer M, Ferrantini F, Vannini C, Galati S, Schweikert M, Görtz HD, Verni F, Petroni G (2013) “Candidatus Megaira polyxenophila” gen. nov. spec. nov.: considerations on evolutionary history, host range and shift of early divergent rickettsiae. PLoS One 8:e72581. CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Lynn DH (2008) The ciliated protozoa: characterization, classification, and guide to the literature. Springer Science and Business Media B.V.Google Scholar
  27. 27.
    Fokin SI (2012) Frequency and biodiversity of symbionts in representatives of the main classes of Ciliophora. Europ J Protistol 48:138–148CrossRefGoogle Scholar
  28. 28.
    Edgcomb VP, Leadbetter ER, Bourland W, Beaudoin D, Bernhard JM (2011) Structured multiple endosymbiosis of bacteria and archaea in a ciliate from marine sulfidic sediments: a survival mechanism in low oxygen, sulfidic sediments? Front Microbiol 2:article 55. CrossRefPubMedGoogle Scholar
  29. 29.
    Gong J, Qing Y, Zou S, Fu R, Su L, Zhang X, Zhang Q (2016) Protist-bacteria associations: Gammaproteobacteria and Alphaproteobacteria are prevalent as digestion-resistant bacteria in ciliated protozoa. Front Microbiol 7:498. CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Bevins CL, Salzman LH (2011) The potter’s wheel: the host’s role in sculpting its microbiota. Cell Mol Life Sci 68(22):3675–3685CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Liu H, Carvalhais LC, Crawford M, Singh E, Dennis PG, Pieterse CMJ, Schenk PM (2017) Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front Microbiol 8:2552. CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59:143–169PubMedPubMedCentralGoogle Scholar
  33. 33.
    Bella C, Koheler L, Grosser K, Berendonk TU, Petroni G, Schrallhammer M (2016) Fitness impact of obligate intranuclear bacterial symbionts depends on host growth phase. Front Microbiol 7:article 2084. CrossRefPubMedGoogle Scholar
  34. 34.
    Duncan AB, Fellous S, Kaltz O (2011) Reverse evolution: selection against costly resistance in disease-free microcosm populations of Paramecium caudatum. Evolution 65:3462–3474CrossRefPubMedGoogle Scholar
  35. 35.
    Dusi E, Krenek S, Schrallhammer M, Sachse R, Rauch G, Kaltz O, Berendonk TU (2014) Vertically transmitted symbiont reduces host fitness along temperature gradient. J Evol Biol 27:796–800CrossRefPubMedGoogle Scholar
  36. 36.
    Fenchel T, Finlay BJ (1991) Endosymbiotic methanogenic bacteria in anaerobic ciliates: significance for the growth efficiency of the host. J Protozool 38:18–22CrossRefGoogle Scholar
  37. 37.
    Görtz HD, Fokin SI (2009) Diversity of endosymbiotic bacteria in Paramecium. In: Fujishima M (ed) Endosymbionts in Paramecium, Microbiology Monographs 12, Chapter 6. Springer-Verlag, Heidelberg, pp 132–160Google Scholar
  38. 38.
    Vannini C, Sigona C, Hahn MWH, Petroni G, Fujishima M (2017) High degree of specificity in the association between symbiotic betaproteobacteria and the host Euplotes. Europ J Protistol 59:124–132CrossRefGoogle Scholar
  39. 39.
    Orsi W, Charvet S, Vd’ačnỳ P, Bernhard JM, Edgcomb VP (2012) Prevalence of partnerships between bacteria and ciliates in oxygen-depleted marine water columns. Front Microbiol 3:341. CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Maurer-Alcalá XX, Knight R, Katz LA (2018) Exploration of the germline genome of the ciliate Chilodonella uncinata through single-cell omics (transcriptomics and genomics). mBio 9:e01836–e01817. CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Kolisko M, Boscaro V, Burki F, Lynn DH, Keeling PJ (2014) Single-cell transcriptomics for microbial eukaryotes. Curr. Biol. 24:R1081–R1082CrossRefPubMedGoogle Scholar
  42. 42.
    Foster RA, Collier JL, Carpenter EJ (2006) Reverse transcription PCR amplification of cyanobacterial symbiont 16S rRNA sequences from single non-photosyntetic eukaryotic marine planktonic host cell. J. Phycol. 42:243–250CrossRefGoogle Scholar
  43. 43.
    Omar A, Zhang Q, Zou S, Gong J (2017) Morphology and phylogeny of the soil ciliate Metopus yantaiensis n. sp. (Ciliophora, Metopida), with identification of the intracellular bacteria. J. Eukaryot. Microbiol. 64:792–805CrossRefPubMedGoogle Scholar
  44. 44.
    Fenchel T, Esteban GF, Finlay BJ (1997) Local versus global diversity of microorganisms: cryptic diversity of ciliated protozoa. Oikos 80:220–225CrossRefGoogle Scholar
  45. 45.
    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 53:11–19CrossRefGoogle Scholar
  46. 46.
    Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified 16S-like rRNA coding regions. Gene 71:491–499CrossRefPubMedGoogle Scholar
  47. 47.
    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 22:118–130CrossRefPubMedGoogle Scholar
  48. 48.
    Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–147Google Scholar
  49. 49.
    Modeo L, Rosati G, Andreoli I, Gabrielli S, Verni F, Petroni G (2006) Molecular systematics and ultrastructural characterization of a forgotten species: Chattonidium setense (Ciliophora, Heterotrichea). Proc Jpn Acad Ser B Phys Biol Sci 82:359–374CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Andreoli I, Mangini L, Ferrantini F, Santangelo G, Verni F, Petroni G (2009) Molecular phylogeny of unculturable Karyorelictea (Alveolata, Ciliophora). Zool Scripta 38:651–662CrossRefGoogle Scholar
  51. 51.
    Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing based diversity studies. Nucleic Acids Res. 41(1):e1. CrossRefPubMedGoogle Scholar
  52. 52.
    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. 25:3389–3402CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Caporaso JG, Kuczynsky J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Met 7:335–336CrossRefGoogle Scholar
  54. 54.
    Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13(7):581–583CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30:772–780CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Price MN, Dehal PS, Arkin AP (2010) FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618CrossRefPubMedGoogle Scholar
  58. 58.
    Werner JJ, Koren O, Hugenholtz P, DeSantis TZ, Walters WA, Caporaso JG, Angenent LT, Knight R, Ley RE (2012) Impact of training sets on classification of high-throughput bacterial 16S rRNA gene surveys. ISME J 6:94–103CrossRefPubMedGoogle Scholar
  59. 59.
    Stoeck T, Bass D, Nebel M, Christen R, Jones MD, Breiner HW, Richards TA (2010) Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol. Ecol. 19:21–31CrossRefPubMedGoogle Scholar
  60. 60.
    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. 56:119–129CrossRefPubMedGoogle Scholar
  61. 61.
    Vannini C, Boscaro V, Ferrantini F, Benken KA, Mironov TI, Schweikert M, Görtz HD, 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:e87718. CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    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 49:434–442CrossRefPubMedGoogle Scholar
  63. 63.
    Shivaji S, Reddy GS (2014) Phylogenetic analyses of the genus Glaciecola: emended description of the genus Glaciecola, transfer of Glaciecola mesophila, G. agarilytica, G. aquimarina, G. arctica, G. chathamensis, G. polaris and G. psychrophila to the genus Paraglaciecola gen. Nov. as Paraglaciecola mesophila comb. nov., P. agarilytica comb. nov., P. aquimarina comb. nov., P. arctica comb. nov., P. chathamensis comb. nov., P. polaris comb. nov. and P. psychrophila comb. nov., and description of Paraglaciecola oceanifecundans sp. nov., isolated from the Southern Ocean. Int. J. Syst. Evol. Microbiol. 64:3264–3275CrossRefPubMedGoogle Scholar
  64. 64.
    Šimek K, Kojecká P, Nedoma J, Hartman P, Vrba J, Dolan JR (1999) Shifts in bacterial community composition associated with different microzooplankton size fraction in a eutrophic reservoir. Limol Oceanogr 44:1634–1644CrossRefGoogle Scholar
  65. 65.
    Hahn MW, Höfle MG (2001) Grazing of protozoa and its effect on aquatic populations of bacteria. FEMS Microbiol. Ecol. 35:113–121CrossRefPubMedGoogle Scholar
  66. 66.
    Jürgens K, Matz C (2002) Predation as shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie Van Leeuwenhoek 81:413–434CrossRefPubMedGoogle Scholar
  67. 67.
    Matz C, McDougald D, Moreno AM, Yung PY, Yildiz FH, Kjelleberg S (2005) Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio colerae. Proc Natl Acad Sci 102:16819–16824CrossRefPubMedGoogle Scholar
  68. 68.
    Hahn MW, Scheuer T, Jezberova J Koll U, Jezbera J, Šimek K, Vannini C, Petroni G, Wu QL (2012) The passive yet successful way of planktonic life: genomic and experimental analysis of the ecology of a free-living Polynucleobacter population. PLoS One 7:e32772. CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Castelli M, serra V, Senra M, Basuri CK, Soares CAG, Fokin SI, Modeo L, Petroni G (2018) The hidden world of Rickettsiales symbionts: “Candidatus Spectrorickettsia obscura”, a novel bacterium found in Brazilian and Indian Paramecium caudatum. Microb Ecol.
  70. 70.
    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 14:2553–2563CrossRefPubMedGoogle Scholar
  71. 71.
    van Hoek AHAM, van Alen TA, Sprakel VSI, Leunissen JAM, Brigge T, Vogels GD, Hackstein JHP (2000) Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates. Mol. Biol. Evol. 17:251–258CrossRefPubMedGoogle Scholar
  72. 72.
    Eloe-Fadrosh EA, Ivanova NN, Woyke T, Kyrpides NC (2016) Metagenomics uncovers gaps in amplicon-based detection of microbial diversity. Nat Microbiol 1:15032CrossRefPubMedGoogle Scholar
  73. 73.
    Boscaro V, Vannini C, Fokin SI, Verni F, Petroni G (2012) Characterization of “Candidatus Nebulobacter yamunensis” from the cytoplasm of Euplotes aediculatus (Ciliophora, Spirotrichea) and emended description of the family Francisellaceae. System and Appl Microbiol 35:432–440CrossRefGoogle Scholar
  74. 74.
    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. 61:455–464CrossRefPubMedGoogle Scholar
  75. 75.
    Martínez-Pérez ME, Macek M, Castro Galván MT (2004) Do protozoa control the elimination of Vibrio colerae in brackish water? Internat Rev Hydrobiol 89:215–227CrossRefGoogle Scholar
  76. 76.
    Sun S, Noorlan P, McDougald D (2018, 1017) Dual role of mechanisms involved in resistance to predation by protozoa and virulence to humans. Front Microbiol 9.
  77. 77.
    Garrity GM, Brenner DJ, Krieg NR, Staley JT (2005) The family Neisseriaceae. In: BERGEY’S MANUAL OF systematic bacteriology Second Edition, Volume Two The Proteobacteria, Bergey’s Manual Trust, pp 775–863.Google Scholar
  78. 78.
    Giordano C, Falleni M, Capria AL, Caracciolo F, Petrini M, Barnini S (2016) First report of Wautersiella falsenii genomovar 2 isolated from the respiratory tract of an immunosuppressed man. IDCases 4:27–29CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Hosseini Dehkordi SH, Lee S, Aponte J, Stavropoulos C (2017) Corynebacterium striatum as an unusual case of endocarditis in an intravenous drug user: case report and review of the literature. Infect Dis Clin Pract 25:301–304CrossRefGoogle Scholar
  80. 80.
    Eisenman H, Letsiou I, Feuchtinger A, Beisker W, Mannweiler E, Hutzler P, Arnz P (2001) Interception of small particles by flocculent structures, sessile ciliates, and the basic layer of a wastewater biofilm. Appl Environ Microbiol 67:4286–4292CrossRefGoogle Scholar
  81. 81.
    Thurman J, Parry JD, Hill PJ, Laybourn-Parry J (2010) The filter feeders Colpidium striatum and Tetrahymena piriformis display selective feeding behaviours in the presence of mixed, equally-sized, bacterial prey. Protist 161:577–588CrossRefPubMedGoogle Scholar
  82. 82.
    Bautista-Reyes F, Macek M (2012) Ciliate food vacuole content and bacterial community composition in the warm-monomictic crater Lake Alchichica, Mexico. FEMS Microbiol Ecol 79:85–97CrossRefPubMedGoogle Scholar
  83. 83.
    Tuorto SJ, Taghon GL (2014) Rates of benthic bacterivory of marine ciliates as a function of prey concentration. J Exp Mar Bio Ecol 460:129–134CrossRefGoogle Scholar
  84. 84.
    Fenchel T (1980) Suspension feeding in ciliated protozoa: functional response and particle size selection. Microb. Ecol. 6:1–11CrossRefPubMedGoogle Scholar
  85. 85.
    Montagnes DJS, Barbosa AB, Boenigk J, Davidson K, Jürgens K, Macek M, Parry JD, Roberts EC, Šimek K (2008) Selective feeding behaviour of key free-living protists: avenue for continued study. Aquat. Microb. Ecol. 53:83–98CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of BiologyUniversity of PisaPisaItaly
  2. 2.Department of Invertebrate ZoologySt.-Petersburg State UniversitySt. PetersburgRussia
  3. 3.St. Petersburg Branch of the S.I. Vavilov Institute of History of Science and TechnologyRussian Academy of SciencesSt. PetersburgRussia
  4. 4.Department of BotanyUniversity of British ColumbiaVancouverCanada

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