1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 69, Issue 4

Techniques and tools for species identification in ciliates: a review Free

Abstract

Ciliates are highly divergent unicellular eukaryotic organisms with nuclear dualism and a highly specialized ciliary pattern. They inhabit all biotopes and play crucial roles in regulating microbial food webs as they prey on bacteria, protists and even on microscopic animals. Nevertheless, subtle morphological differences and tiny sizes hinder proper species identification for many ciliates. In the present review, an attempt has been made to elaborate the various approaches used by modern day ciliate taxonomists for species identification. The different approaches involved in taxonomic characterization of ciliates such as classical (using live-cell observations, staining techniques, etc.), molecular (involving various marker genes) and statistical (delimitation of cryptic species) methods have been reviewed. Ecological and behavioural aspects in species identification have also been discussed. In present-day taxonomy, it is important to use a ‘total evidence’ approach in identifying ciliates, relying on both classical and molecular information whenever possible. This integrative approach will help in the mergence of classical methods with modern-day tools for comprehensive species description in future.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): ciliates , classical approach , DNA based identification , marker genes , molecular approach and taxonomy
Funding
This study was supported by the:
  • Council of Scientific and Industrial Research
  • University Grants Commission
  • Council of Scientific and Industrial Research
© 2019 IUMS
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.003176
2019-01-16
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/69/4/877.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.003176&mimeType=html&fmt=ahah

References

  1. Chen X, Lu X, Luo X, Jiang J, Shao C et al. The diverse morphogenetic patterns in spirotrichs and philasterids: researches based on five-year-projects supported by IRCN-BC and NSFC. Eur J Protistol 2017; 61:439–452 [View Article][PubMed]
     [Google Scholar]
  2. Gao F, Huang J, Zhao Y, Li L, Liu W et al. Systematic studies on ciliates (Alveolata, Ciliophora) in China: progress and achievements based on molecular information. Eur J Protistol 2017; 61:409–423 [View Article][PubMed]
     [Google Scholar]
  3. Clamp JC, Lynn DH. Investigating the biodiversity of ciliates in the 'Age of Integration'. Eur J Protistol 2017; 61:314–322 [View Article][PubMed]
     [Google Scholar]
  4. Lynn DH. The Ciliated Protozoa: characterization, Classification and Guide to the Literature, 3rd ed. Netherlands: Springer-Verlag; 2008
     [Google Scholar]
  5. Hausmann K, Bradbury P. Ciliates: Cells as Organisms Germany, Stuttgart: Gustav Fischer Verlag; 1996
     [Google Scholar]
  6. Somasundaram S, Abraham JS, Maurya S, Makhija S, Gupta R et al. Cellular and molecular basis of heavy metal-induced stress in ciliates. Curr Sci 2018; 114:1858–1865
     [Google Scholar]
  7. Kim BM, Rhee JS, Choi IY, Lee YM. Transcriptional profiling of antioxidant defense system and heat shock protein (Hsp) families in the cadmium- and copper-exposed marine ciliate Euplotes crassu. Genes Genomics 2018; 40:85–98 [View Article][PubMed]
     [Google Scholar]
  8. Abraham JS, Sripoorna S, Choudhary A, Toteja R, Gupta R et al. Assessment of heavy metal toxicity in four species of freshwater ciliates (Spirotrichea:Ciliophora) from Delhi, India. Curr Sci 2017; 113:2141–2150 [View Article]
     [Google Scholar]
  9. Amaro F, Turkewitz AP, Martín-González A, Gutiérrez JC. Whole-cell biosensors for detection of heavy metal ions in environmental samples based on metallothionein promoters from Tetrahymena thermophila . Microb Biotechnol 2011; 4:513–522 [View Article][PubMed]
     [Google Scholar]
  10. Makhija S, Gupta R, Toteja R. Lithium-induced developmental anomalies in the spirotrich ciliate Stylonychia lemnae (Ciliophora, Hypotrichida). Eur J Protistol 2015; 51:290–298 [View Article][PubMed]
     [Google Scholar]
  11. Makhija S, Gupta R, Toteja R, Abraham JS, Sripoorna S. Cadmium induced ultrastructural changes in the ciliate, Stylonychia mytilus (Ciliophora, Hypotrichida). J Cell Tissue Res 2015b; 15:1–7
     [Google Scholar]
  12. Machwe S, Arora S, Gupta R, Sapra GR. Cisplatin induces modifications in the development of cell surface patterns of ciliates. Cell Biol Int 2001; 25:1131–1138 [View Article][PubMed]
     [Google Scholar]
  13. Toteja R, Makhija S, Sripoorna S, Abraham JS, Gupta R. Influence of copper and cadmium toxicity on antioxidant enzyme activity in freshwater ciliates. Indian J Exp Biol 2017; 55:694–701
     [Google Scholar]
  14. Gutiérrez JC, Amaro F, Díaz S, de Francisco P, Cubas LL et al. Ciliate metallothioneins: unique microbial eukaryotic heavy-metal-binder molecules. J Biol Inorg Chem 2011; 16:1025–1034 [View Article][PubMed]
     [Google Scholar]
  15. La Terza A, Miceli C, Luporini P. The gene for the heat-shock protein 70 of Euplotes focardii, an Antarctic psychrophilic ciliate. Antarct Sci 1999; 16:23–28 [View Article]
     [Google Scholar]
  16. Gupta R, Abraham JS, Sripoorna S, Toteja R, Makhija S et al. Taxonomic and morphogenetic description of the freshwater ciliate Aponotohymena isoaustralis n. sp. (Ciliophora; Oxytrichidae) isolated from Sanjay Lake, Delhi, India. Acta Protozool 2017; 56:93–107
     [Google Scholar]
  17. Foissner W. Terrestrial and semiterrestrial ciliates (Protozoa, Ciliophora) from Venezuela and Galápagos. Denisia 2016; 35:1–912
     [Google Scholar]
  18. Gupta R, Kamra K, Sapra GR. Morphology and cell division of the oxytrichids Architricha indica nov. gen., nov. sp., and Histriculus histrio (Müller, 1773), Corliss, 1960 (Ciliophora, Hypotrichida). Eur J Protistol 2006; 42:29–48 [View Article][PubMed]
     [Google Scholar]
  19. Corliss JO. The Ciliated Protozoa: Characterization, Classification and Guide to the Literature, 2nd ed. USA, New York: Pergamon press; 1979
     [Google Scholar]
  20. Wang P, Gao F, Huang J, Strüder-Kypke M, Yi Z. A case study to estimate the applicability of secondary structures of SSU-rRNA gene in taxonomy and phylogenetic analyses of ciliates. Zool Scr 2015; 44:574–585 [View Article]
     [Google Scholar]
  21. Gentekaki E, Kolisko M, Boscaro V, Bright KJ, Dini F et al. Large-scale phylogenomic analysis reveals the phylogenetic position of the problematic taxon Protocruzia and unravels the deep phylogenetic affinities of the ciliate lineages. Mol Phylogenet Evol 2014; 78:36–42 [View Article][PubMed]
     [Google Scholar]
  22. Zhang Q, Yi Z, Fan X, Warren A, Gong J et al. Further insights into the phylogeny of two ciliate classes Nassophorea and Prostomatea (Protista, Ciliophora). Mol Phylogenet Evol 2014; 70:162–170 [View Article][PubMed]
     [Google Scholar]
  23. Gao F, Warren A, Zhang Q, Gong J, Miao M et al. The all-data-based evolutionary hypothesis of ciliated protists with a revised classification of the phylum Ciliophora (Eukaryota, Alveolata). Sci Rep 2016; 6:1–14 [View Article]
     [Google Scholar]
  24. Adl SM, Bass D, Lane CE, Lukes J, Schoch CL et al. Classification of eukaryotes: revisions to the classification, nomenclature and diversity of eukaryotes. J Eukaryot Microbiol 2018 https://doi.org/
     [Google Scholar]
  25. Maurer-Alcalá XX, Yan Y, Pilling OA, Knight R, Katz LA. Twisted tales: insights into genome diversity of ciliates using single-cell 'omics. Genome Biol Evol 2018; 10:1927–1938 [View Article][PubMed]
     [Google Scholar]
  26. Lynn DH, Kolisko M, Bourland W. Phylogenomic analysis of Nassula variabilis n. sp., Furgasonia blochmanni, and Pseudomicrothorax dubius Confirms a Nassophorean Clade. Protist 2018; 169:180–189 [View Article][PubMed]
     [Google Scholar]
  27. Chen X, Wang Y, Sheng Y, Warren A, Gao S. GPSit: An automated method for evolutionary analysis of nonculturable ciliated microeukaryotes. Mol Ecol Resour 2018; 18:700–713 [View Article][PubMed]
     [Google Scholar]
  28. Foissner W. An update of 'basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa'. Int J Syst Evol Microbiol 2014; 64:271–292 [View Article][PubMed]
     [Google Scholar]
  29. Skovorodkin I. A device for immobilizing biological objects in the light microscope studies. Tsitilogia 1990; 32:301–302 (in Russian with English summary)
    [Google Scholar]
  30. Fernandez-Galiano D. Siver impregnation of ciliated protozoa: procedure yielding good results with the pyridinated siver carbonate method. Trans Am Microsc Soc 1976; 95:557–560 [View Article][PubMed]
     [Google Scholar]
  31. Chatton E, Lwoff A. Imprégnation, par diffusion argentique, de l'infraciliature des ciliés marins et d'eau douce, après fixation cytologique et sans desiccation. CR Seances Soc Biol 1930; 104:834–836
     [Google Scholar]
  32. Wilbert N. Eine verbesserte Technik der Protargolimpänation für Ciliaten. Mikrokosmos 1975; 64:171–179
     [Google Scholar]
  33. Montagnes DJS, Lynn DH. A quantitative protargol stain (QPS) for ciliates: method description and test of its quantitative nature. Mar Microb Food Webs 1987; 2:83–93
     [Google Scholar]
  34. Wicklow BJ, Hill BF. A short procedure for protargol staining. In Lee JJ, Soldo AT. (editors) Protocols in Protozoology Kansas, USA: Allen Press; 1992 pp. C-5.1–5.5
     [Google Scholar]
  35. Foissner W. Protargol methods. In Lee JJ, Soldo AT. (editors) Protocols in Protozoology Kansas, USA: Allen Press; 1992 pp. C-6.1–6.0
     [Google Scholar]
  36. Lynn DH, Staining P. Protargol staining. In Lee JJ, Soldo AT. (editors) Protocols in Protozoology Kansas, USA: Allen Press; 1992 pp. C-4.1–C-4.8
     [Google Scholar]
  37. Chatton E. Sur une méthode rapide d’impregnation a l’argent réduit par l’hydroquinone. C R Seanc Soc Biol 1940; 134:229–232
     [Google Scholar]
  38. Frankel J, Heckmann K. A simplified chatton-lwoff silver impregnation procedure for use in experimental studies with ciliates. Trans Am Microsc Soc 1968; 87:317–321 [View Article]
     [Google Scholar]
  39. Roberts DM, Causton H. Silver nitrate impregnation of ciliated protozoa. Archiv für Protistenkunde 1988; 135:299–318 [View Article]
     [Google Scholar]
  40. Pan X, Bourland WA, Song W. Protargol synthesis: an in-house protocol. J Eukaryot Microbiol 2013; 60:609–614 [View Article][PubMed]
     [Google Scholar]
  41. Ji D, Wang Y. An optimized protocol of protargol staining for ciliated protozoa. J Eukaryot Microbiol 2018; 65:705–708 [View Article][PubMed]
     [Google Scholar]
  42. Kurilov AV. Improvement of silver impregnation technique using in situ synthesized Protargol. Acta Protozool 2017; 56:109–118
     [Google Scholar]
  43. Foissner W. Basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa. Eur J Protistol 1991; 27:313–330 [View Article][PubMed]
     [Google Scholar]
  44. Kim JH, Jung J-H. Cytological staining of protozoa: a case study on the impregnation of hypotrichs (Ciliophora: spirotrichea) using laboratory-synthesized protargol. Animal Cells Syst 2017; 21:412–418 [View Article]
     [Google Scholar]
  45. Berger H, Foissner W. Cladistic relationships and generic characterization of oxytrichid hypotrichs (protozoa, ciliophora). Archiv für Protistenkunde 1997; 148:125–155 [View Article]
     [Google Scholar]
  46. Shao C, Lu X, Ma H. A general overview of the typical 18 frontal-ventral-transverse cirri oxytrichidae s. l. genera (Ciliophora, Hypotrichia). J Ocean Univ China 2015; 14:522–532 [View Article]
     [Google Scholar]
  47. Arregui L, Muñoz-Fontela C, Guinea A, Serrano S. FLUTAX facilitates visualization of the ciliature of oxytrichid hypotrichs. Eur J Protistol 2003; 39:169–172 [View Article]
     [Google Scholar]
  48. Arregui L, Muñoz-Fontela C, Serrano S, Barasoain I, Guinea A. Direct visualization of the microtubular cytoskeleton of ciliated protozoa with a fluorescent taxoid. J Eukaryot Microbiol 2002; 49:312–318 [View Article][PubMed]
     [Google Scholar]
  49. Schliwa M, van Blerkom J. Structural interaction of cytoskeletal components. J Cell Biol 1981; 90:222–235 [View Article][PubMed]
     [Google Scholar]
  50. Petroni G, Rosati G, Vannini C, Modeo L, Dini F et al. In situ identification by fluorescently labeled oligonucleotide probes of morphologically similar, closely related ciliate species. Microb Ecol 2003; 45:156–162 [View Article][PubMed]
     [Google Scholar]
  51. Amann R, Ludwig W. Typing in situ with probes. In Priest FG, Ramos-Cormenzana A, Tindall BJ. (editors) Bacterial Diversity and Systematics Boston, MA: Springer; 1994 pp. 115–135
     [Google Scholar]
  52. Fried J, Ludwig W, Psenner R, Schleifer KH. Improvement of ciliate identification and quantification: a new protocol for fluorescence in situ hybridization (FISH) in combination with silver stain techniques. Syst Appl Microbiol 2002; 25:555–571 [View Article][PubMed]
     [Google Scholar]
  53. Zhan Z, Stoeck T, Dunthorn M, Xu K. Identification of the pathogenic ciliate Pseudocohnilembus persalinus (Oligohymenophorea: Scuticociliatia) by fluorescence in situ hybridization. Eur J Protistol 2014; 50:16–24 [View Article][PubMed]
     [Google Scholar]
  54. Gunderson JH, Goss SH. Fluorescently-labeled oligonucleotide probes can be used to identify protistan food vacuole contents. J Eukaryot Microbiol 1997; 44:300–304 [View Article][PubMed]
     [Google Scholar]
  55. Fried J, Foissner W. Differentiation of two very similar glaucomid ciliate morphospecies (Ciliophora, Tetrahymenida) by fluorescence in situ hybridization with 18S rRNA targeted oligonucleotide probes. J Eukaryot Microbiol 2007; 54:381–387 [View Article][PubMed]
     [Google Scholar]
  56. Skibbe O. An improved quantitative protargol stain for ciliates and other planktonic protists. Arch Hydrobiol 1994; 130:339–347
     [Google Scholar]
  57. Chieco P, Derenzini M. The Feulgen reaction 75 years on. Histochem Cell Biol 1999; 111:345–358 [View Article][PubMed]
     [Google Scholar]
  58. Gupta R, Makhija S, Toteja R. Cell Biology Practical Manual Delhi, India: Prestige Publishers; 2018
     [Google Scholar]
  59. Throndsen J. Preservation and storage. In Sournia A. (editor) Phytoplankton Manual Paris: UNESCO; 1978 pp. 69–74
     [Google Scholar]
  60. Wancura MM, Yan Y, Katz LA, Maurer-Alcalá XX. Nuclear features of the heterotrich ciliate Blepharisma americanum: genomic amplification, life cycle, and nuclear inclusion. J Eukaryot Microbiol 2018; 65:4–11 [View Article][PubMed]
     [Google Scholar]
  61. Lessard EJ, Martin MP, Montagnes DJS. A new method for live-staining protists with DAPI and its application as a tracer of ingestion by walleye pollock (Theragra chalcogramma (Pallas)) larvae. J Exp Mar Bio Ecol 1996; 204:43–57 [View Article]
     [Google Scholar]
  62. Strüder-Kypke MC, Montagnes DJS. Development of web-based guides to planktonic protists. Aquatic Microbial Ecology 2002; 27:203–207 [View Article]
     [Google Scholar]
  63. Ruthmann A. Methods in Cell Research UK, London: G. Bell and Sons Ltd; 1970
     [Google Scholar]
  64. Zhao Y, Yi Z, Gentekaki E, Zhan A, Al-Farraj SA et al. Utility of combining morphological characters, nuclear and mitochondrial genes: An attempt to resolve the conflicts of species identification for ciliated protists. Mol Phylogenet Evol 2016; 94:718–729 [View Article][PubMed]
     [Google Scholar]
  65. Patwardhan A, Ray S, Roy A. Molecular markers in phylogenetic studies – a review. J Phylogenet Evol Biol 2014; 2:1–9
     [Google Scholar]
  66. Vďačný P. Integrative taxonomy of ciliates: Assessment of molecular phylogenetic content and morphological homology testing. Eur J Protistol 2017; 61:388–398 [View Article][PubMed]
     [Google Scholar]
  67. Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP. DNA points the way ahead in taxonomy. Nature 2002; 418:479 [View Article][PubMed]
     [Google Scholar]
  68. Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP. A plea for DNA taxonomy. Trends Ecol Evol 2003; 18:70–74 [View Article]
     [Google Scholar]
  69. Hillis DM, Dixon MT. Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 1991; 66:411–453 [View Article][PubMed]
     [Google Scholar]
  70. Sonnenberg R, Nolte AW, Tautz D. An evaluation of LSU rDNA D1-D2 sequences for their use in species identification. Front Zool 2007; 4:6–12 [View Article][PubMed]
     [Google Scholar]
  71. Agatha S, Strüder-Kypke MC. What morphology and molecules tell us about the evolution of Oligotrichea (Alveolata, Ciliophora). Acta Protozool 2014; 53:77–90
     [Google Scholar]
  72. Gao F, Gao S, Wang P, Katz LA, Song W. Phylogenetic analyses of cyclidiids (Protista, Ciliophora, Scuticociliatia) based on multiple genes suggest their close relationship with thigmotrichids. Mol Phylogenet Evol 2014; 75:219–226 [View Article][PubMed]
     [Google Scholar]
  73. Bachy C, Dolan JR, López-García P, Deschamps P, Moreira D. Accuracy of protist diversity assessments: morphology compared with cloning and direct pyrosequencing of 18S rRNA genes and ITS regions using the conspicuous tintinnid ciliates as a case study. ISME J 2013; 7:244–255 [View Article][PubMed]
     [Google Scholar]
  74. Zhao Y, Gentekaki E, Yi Z, Lin X. Genetic differentiation of the mitochondrial cytochrome oxidase C subunit I gene in genus Paramecium (Protista, Ciliophora). PLoS One 2013; 8:e7704410 [View Article][PubMed]
     [Google Scholar]
  75. Strüder-Kypke MC, Lynn DH. Comparative analysis of the mitochondrial cytochrome c oxidase subunit I (COI) gene in ciliates (Alveolata, Ciliophora) and evaluation of its suitability as a biodiversity marker. Syst Biodivers 2010; 8:131–148 [View Article]
     [Google Scholar]
  76. Chantangsi C, Lynn DH, Brandl MT, Cole JC, Hetrick N et al. Barcoding ciliates: a comprehensive study of 75 isolates of the genus Tetrahymena . Int J Syst Evol Microbiol 2007; 57:2412–2425 [View Article][PubMed]
     [Google Scholar]
  77. Li J, Liu W, Gao S, Warren A, Song W. Multigene-based analyses of the phylogenetic evolution of oligotrich ciliates, with consideration of the internal transcribed spacer 2 secondary structure of three systematically ambiguous genera. Eukaryot Cell 2013; 12:430–437 [View Article][PubMed]
     [Google Scholar]
  78. Gao F, Katz LA, Song W. Insights into the phylogenetic and taxonomy of philasterid ciliates (Protozoa, Ciliophora, Scuticociliatia) based on analyses of multiple molecular markers. Mol Phylogenet Evol 2012; 64:308–317 [View Article][PubMed]
     [Google Scholar]
  79. Hoshina R. Secondary structural analyses of ITS1 in Paramecium . Microbes Environ 2010; 25:313–316 [View Article][PubMed]
     [Google Scholar]
  80. Shazib SU, Vďačný P, Kim JH, Jang SW, Shin MK. Molecular phylogeny and species delimitation within the ciliate genus Spirostomum (Ciliophora, Postciliodesmatophora, Heterotrichea), using the internal transcribed spacer region. Mol Phylogenet Evol 2016; 102:128–144 [View Article][PubMed]
     [Google Scholar]
  81. Katz LA, Deberardinis J, Hall MS, Kovner AM, Dunthorn M et al. Heterogeneous rates of molecular evolution among cryptic species of the ciliate morphospecies Chilodonella uncinata . J Mol Evol 2011; 73:266–272 [View Article][PubMed]
     [Google Scholar]
  82. Israel RL, Kosakovsky Pond SL, Muse SV, Katz LA. Evolution of duplicated alpha-tubulin genes in ciliates. Evolution 2002; 56:1110–1122 [View Article][PubMed]
     [Google Scholar]
  83. Roger AJ, Sandblom O, Doolittle WF, Philippe H. An evaluation of elongation factor 1 alpha as a phylogenetic marker for eukaryotes. Mol Biol Evol 1999; 16:218–233 [View Article][PubMed]
     [Google Scholar]
  84. Greczek-Stachura M, Potekhin A, Przyboś E, Rautian M, Skoblo I et al. Identification of Paramecium bursaria syngens through molecular markers-comparative analysis of three loci in the nuclear and mitochondrial DNA. Protist 2012; 163:671–685 [View Article][PubMed]
     [Google Scholar]
  85. Stoeck T, Przybos E, Dunthorn M. The D1-D2 region of the large subunit ribosomal DNA as barcode for ciliates. Mol Ecol Resour 2014; 14:458–468 [View Article][PubMed]
     [Google Scholar]
  86. Dunthorn M, Foissner W, Katz LA. Molecular phylogenetic analysis of class Colpodea (phylum Ciliophora) using broad taxon sampling. Mol Phylogenet Evol 2008; 46:316–327 [View Article][PubMed]
     [Google Scholar]
  87. Hebert PD, Cywinska A, Ball SL, Dewaard JR. Biological identifications through DNA barcodes. Proc Biol Sci 2003; 270:313–321 [View Article][PubMed]
     [Google Scholar]
  88. Stoeck T, Behnke A, Christen R, Amaral-Zettler L, Rodriguez-Mora MJ et al. Massively parallel tag sequencing reveals the complexity of anaerobic marine protistan communities. BMC Biol 2009; 7:72–20 [View Article][PubMed]
     [Google Scholar]
  89. Stoeck T, Bass D, Nebel M, Christen R, Jones MD et al. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol 2010; 19 Suppl 1:21–31 [View Article][PubMed]
     [Google Scholar]
  90. Huber JA, Morrison HG, Huse SM, Neal PR, Sogin ML et al. Effect of PCR amplicon size on assessments of clone library microbial diversity and community structure. Environ Microbiol 2009; 11:1292–1302 [View Article]
     [Google Scholar]
  91. Vďačný P, Orsi W, Bourland WA, Shimano S, Epstein SS et al. Morphological and molecular phylogeny of dileptid and tracheliid ciliates: resolution at the base of the class Litostomatea (Ciliophora, Rhynchostomatia). Eur J Protistol 2011; 47:295–313 [View Article][PubMed]
     [Google Scholar]
  92. Harder CB, Rønn R, Brejnrod A, Bass D, Al-Soud WA et al. Local diversity of heathland Cercozoa explored by in-depth sequencing. ISME J 2016; 10:2488–2497 [View Article][PubMed]
     [Google Scholar]
  93. Behnke A, Engel M, Christen R, Nebel M, Klein RR et al. Depicting more accurate pictures of protistan community complexity using pyrosequencing of hypervariable SSU rRNA gene regions. Environ Microbiol 2011; 13:340–349 [View Article][PubMed]
     [Google Scholar]
  94. Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM. Correction: a method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS One 2009; 4:1–9 [View Article]
     [Google Scholar]
  95. Hebert PD, Penton EH, Burns JM, Janzen DH, Hallwachs W. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator . Proc Natl Acad Sci USA 2004; 101:14812–14817 [View Article][PubMed]
     [Google Scholar]
  96. Mueller RL. Evolutionary rates, divergence dates, and the performance of mitochondrial genes in Bayesian phylogenetic analysis. Syst Biol 2006; 55:289–300 [View Article][PubMed]
     [Google Scholar]
  97. Hebert PD, Ratnasingham S, Dewaard JR. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc Biol Sci 2003; 270:S96–S99 [View Article][PubMed]
     [Google Scholar]
  98. Seifert KA. Barcoding fungi. Progress towards DNA barcoding of fungi. Mol Ecol Resour 2009; 9:83–89
     [Google Scholar]
  99. Evans KM, Wortley AH, Mann DG. An assessment of potential diatom “barcode” genes (cox1, rbcL, 18S and ITS rDNA) and their effectiveness in determining relationships in Sellaphora (Bacillariophyta). Protist 2007; 158:349–364 [View Article]
     [Google Scholar]
  100. Williamson P, Day JG. The problem with protists: is barcoding the answer?. Biologist 2007; 54:86–90
     [Google Scholar]
  101. Brunk CF, Lee LC, Tran AB, Li J. Complete sequence of the mitochondrial genome of Tetrahymena thermophila and comparative methods for identifying highly divergent genes. Nucleic Acids Res 2003; 31:1673–1682 [View Article]
     [Google Scholar]
  102. Burger G, Zhu Y, Littlejohn TG, Greenwood SJ, Schnare MN et al. Complete sequence of the mitochondrial genome of Tetrahymena pyriformis and comparison with Paramecium aurelia mitochondrial DNA. J Mol Biol 2000; 297:365–380 [View Article][PubMed]
     [Google Scholar]
  103. Park M-H, Jung J-H, Jo E, Park K-M, Baek Y-S et al. Utility of mitochondrial CO1 sequences for species discrimination of Spirotrichea ciliates (Protozoa, Ciliophora). Mitochondrial DNA Part A 2018; 5:1–8 [View Article]
     [Google Scholar]
  104. Coleman AW. ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends Genet 2003; 19:370–375 [View Article][PubMed]
     [Google Scholar]
  105. Alvarez I, Wendel JF. Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 2003; 29:417–434 [View Article][PubMed]
     [Google Scholar]
  106. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003; 31:3406–3415 [View Article][PubMed]
     [Google Scholar]
  107. Miao M, Warren A, Song W, Wang S, Shang H et al. Analysis of the internal transcribed spacer 2 (ITS2) region of scuticociliates and related taxa (Ciliophora, Oligohymenophorea) to infer their evolution and phylogeny. Protist 2008; 159:519–533 [View Article][PubMed]
     [Google Scholar]
  108. de Rijk P, de Wachter R. RnaViz, a program for the visualisation of RNA secondary structure. Nucleic Acids Res 1997; 25:4679–4684 [View Article][PubMed]
     [Google Scholar]
  109. Gentekaki E, Lynn DH. High-level genetic diversity but no population structure inferred from nuclear and mitochondrial markers of the peritrichous ciliate Carchesium polypinum in the Grand River basin (North America). Appl Environ Microbiol 2009; 75:3187–3195 [View Article][PubMed]
     [Google Scholar]
  110. Finlay BJ, Esteban GF, Brown S, Fenchel T, Hoef-Emden K. Multiple cosmopolitan ecotypes within a microbial eukaryote morphospecies. Protist 2006; 157:377–390 [View Article][PubMed]
     [Google Scholar]
  111. Santoferrara LF, McManus GB, Alder VA. Utility of genetic markers and morphology for species discrimination within the order Tintinnida (Ciliophora, Spirotrichea). Protist 2013; 164:24–36 [View Article][PubMed]
     [Google Scholar]
  112. Hamsher SE, Evans KM, Mann DG, Poulíčková A, Saunders GW. Barcoding diatoms: exploring alternatives to COI-5P. Protist 2011; 162:405–422 [View Article][PubMed]
     [Google Scholar]
  113. Beszteri B, Acs E, Medlin LK. Ribosomal DNA sequence variation among sympatric strains of the Cyclotella meneghiniana complex (Bacillariophyceae) reveals cryptic diversity. Protist 2005; 156:317–333 [View Article][PubMed]
     [Google Scholar]
  114. Jones TC, Gates MA. A morphometric analysis of the Euplotes charon morphotype (Ciliophora: Euplotida). J Eukaryot Microbiol 1994; 41:441–450 [View Article]
     [Google Scholar]
  115. Vďačný P, Slovák M, Foissner W. Multivariate morphometric analyses of the predatory ciliate genus Semispathidium (Ciliophora: Litostomatea), with description of S. longiarmatum nov. spec. Eur J Protistol 2014; 50:329–344 [View Article][PubMed]
     [Google Scholar]
  116. Lynn DH, Malcolm JR. A multivariate study of morphometric variation in species of the ciliate genus Colpoda (Ciliophora: Colpodida). Can J Zool 1983; 61:307–316 [View Article]
     [Google Scholar]
  117. Vďačný P, Foissner W. A huge diversity of metopids (Ciliophora, Armophorea) in soil from the Murray River floodplain, Australia. I. Description of five new species and redescription of Metopus setosus Kahl, 1927. Eur J Protistol 2017; 58:35–76 [View Article][PubMed]
     [Google Scholar]
  118. Podani J. SYN-TAX. Version 5.0. Version 5.0. Computer Programs for Multivariate Data Analysis in Ecology and Systematics Budapest: User’s Guide. Scientia Publishing; 2001
     [Google Scholar]
  119. SAS Institute SAS OnlineDoc®, version 8 Cary: SAS Institute; 2000
     [Google Scholar]
  120. Irwin NAT, Sabetrasekh M, Lynn DH. Diversification and phylogenetics of mobilid peritrichs (ciliophora) with description of Urceolaria parakorschelti sp. nov. Protist 2017; 168:481–493 [View Article][PubMed]
     [Google Scholar]
  121. Foissner W, Schubert G. Morphologische und diskriminanzanalytische Trennung von Colpoda aspera Kahl, 1926 und Colpoda elliotti Bradbury et Outka, 1967 (Ciliophora: Colpodidae). Acta Protozool 1983; 22:127–138
     [Google Scholar]
  122. Ginoris YP, Amaral AL, Nicolau A, Coelho MAZ, Ferreira EC. Raw data pre-processing in the protozoa and metazoa identification by image analysis and multivariate statistical techniques. J Chemom 2007; 21:156–164 [View Article]
     [Google Scholar]
  123. Maddison WP. Gene trees in species trees. Syst Biol 1997; 46:523–536 [View Article]
     [Google Scholar]
  124. Nichols R. Gene trees and species trees are not the same. Trends Ecol Evol 2001; 16:358–364 [View Article][PubMed]
     [Google Scholar]
  125. Edwards SV. Is a new and general theory of molecular systematics emerging?. Evolution 2009; 63:1–19 [View Article][PubMed]
     [Google Scholar]
  126. Yang Z, Rannala B. Bayesian species delimitation using multilocus sequence data. Proc Natl Acad Sci USA 2010; 107:9264–9269 [View Article][PubMed]
     [Google Scholar]
  127. Weisse T. Functional diversity of aquatic ciliates. Eur J Protistol 2017; 61:331–358 [View Article][PubMed]
     [Google Scholar]
  128. Weisse T. Ciliates and the rare biosphere-community ecology and population dynamics. J Eukaryot Microbiol 2014; 61:419–433 [View Article][PubMed]
     [Google Scholar]
  129. Dunthorn M, Stoeck T, Clamp J, Warren A, Mahé F. Ciliates and the rare biosphere: a review. J Eukaryot Microbiol 2014; 61:404–409 [View Article][PubMed]
     [Google Scholar]
  130. Pucciarelli S, La Terza A, Ballarini P, Barchetta S, Yu T et al. Molecular cold-adaptation of protein function and gene regulation: The case for comparative genomic analyses in marine ciliated protozoa. Mar Genomics 2009; 2:57–66 [View Article][PubMed]
     [Google Scholar]
  131. Li J, Giesy JP, Yu L, Li G, Liu C. Effects of Tris(1,3-dichloro-2-propyl) Phosphate (TDCPP) in Tetrahymena Thermophila: Targeting the Ribosome. Sci Rep 2015; 5:10562 [View Article][PubMed]
     [Google Scholar]
  132. Warren A, Patterson DJ, Dunthorn M, Clamp JC, Achilles-Day UEM et al. Beyond the "Code": a guide to the description and documentation of biodiversity in ciliated protists (alveolata, ciliophora). J Eukaryot Microbiol 2017; 64:539–554 [View Article][PubMed]
     [Google Scholar]
  133. Ricci N. The behaviour of ciliated protozoa. Anim Behav 1990; 40:1048–1069 [View Article]
     [Google Scholar]
  134. Banchetti R, Erra F. The ethology of protozoa and the “adaptive space” hypothesis: a heuristic approach to the biology of these eukaryotic, unicellular organisms. Protistology 2003; 3:58–68
     [Google Scholar]
  135. Ricci N, Banchetti R. The peculiar case of giants of Oxytricha bifaria (Ciliata, Hypotrichida): a paradigmatic example of cell differentiation and adaptive strategy. Zool Sc 1993; 10:393–410
     [Google Scholar]
  136. Soleymani A, Pennekamp F, Petchey OL, Weibel R. Developing and integrating advanced movement features improves automated classification of ciliate species. PLoS One 2015; 10:e0145345 [View Article][PubMed]
     [Google Scholar]
  137. Leonildi A, Erra F, Banchetti R, Ricci N. The ethograms of Uronychia transfuga and Uronychia setigera (Ciliata, hypotrichida): a comparative approach for new insights into the behaviour of protozoa. Eur J Protistol 1998; 34:426–435 [View Article]
     [Google Scholar]
  138. Bohatová M, Vďačný P. Locomotory behaviour of two phylogenetically distant predatory ciliates: does evolutionary history matter?. Ethol Ecol Evol 2018; 30:195–219 [View Article]
     [Google Scholar]
  139. Ricci N. The ethogram of Oxytricha bifaria (Ciliophora, Hypotrichida). I. The motile behavior. Acta Protozool 1981; 20:393–410
     [Google Scholar]
  140. Ricci N, Giannetti R, Miceli C. The ethogram of Euplotes Crassus (Ciliata, Hypotrichida): I. The wild type. Eur J Protistol 1988; 23:129–140 [View Article][PubMed]
     [Google Scholar]
  141. Ricci N, Verni F. The ethogram of Litonotus lamella, a predator ciliate. Can J Zool 1988; 66:1973–1981
     [Google Scholar]
  142. Banchetti R. Ethology of Ciliates: an appreciation of the work of Nicola Ricci. Eur J Protistol 2003; 39:380–384 [View Article]
     [Google Scholar]
  143. Wake MH. An integrative approach to the biology of biodiversity. Bio Int 1995; 31:1–6
     [Google Scholar]
  144. Dayrat B. Towards integrative taxonomy. Biol J Linn Soc Lond 2005; 85:407–415 [View Article]
     [Google Scholar]
  145. Dawson MN. Renaissance taxonomy: integrative evolutionary analyses in the classification of Scyphozoa. J Mar Biol Ass UK 2005; 85:733–739 [View Article]
     [Google Scholar]
  146. Cedrola F, Rossi M, Dias RJ, Martinele I, D'Agosto M. Methods for taxonomic studies of rumen ciliates (alveolata: ciliophora): a brief review. Zoolog Sci 2015; 32:8–15 [View Article][PubMed]
     [Google Scholar]
  147. McManus GB, Katz LA. Molecular and morphological methods for identifying plankton: what makes a successful marriage?. J Plankton Res 2009; 31:1119–1129 [View Article]
     [Google Scholar]
  148. Buckley R. Parks and tourism. PLoS Biol 2009; 7:e1000143 [View Article][PubMed]
     [Google Scholar]
  149. Modeo L, Petroni G, Rosati G, Montagnes DJ. A multidisciplinary approach to describe protists: redescriptions of Novistrombidium testaceum Anigstein 1914 and Strombidium inclinatum Montagnes, Taylor, and Lynn 1990 (Ciliophora, Oligotrichia). J Eukaryot Microbiol 2003; 50:175–189 [View Article][PubMed]
     [Google Scholar]
  150. Rajter Ľubomír, Vďačný P. Rapid radiation, gradual extinction and parallel evolution challenge generic classification of spathidiid ciliates (Protista, Ciliophora). Zool Scr 2016; 45:200–223
     [Google Scholar]
  151. Sun P, Clamp J, Xu D, Huang B, Shin MK. An integrative approach to phylogeny reveals patterns of environmental distribution and novel evolutionary relationships in a major group of ciliates. Sci Rep 2016; 6:1–12 [View Article]
     [Google Scholar]
  152. Lynn DH, Gómez-Gutiérrez J, Strüder-Kypke MC, Shaw CT. Ciliate species diversity and host-parasitoid codiversification in Pseudocollinia infecting krill, with description of Pseudocollinia similis sp. nov. Dis Aquat Organ 2014; 112:89–102 [View Article][PubMed]
     [Google Scholar]
  153. Dawson SC, Pace NR. Novel kingdom-level eukaryotic diversity in anoxic environments. Proc Natl Acad Sci USA 2002; 99:8324–8329 [View Article][PubMed]
     [Google Scholar]
  154. Dopheide A, Lear G, Stott R, Lewis G. Molecular characterization of ciliate diversity in stream biofilms. Appl Environ Microbiol 2008; 74:1740–1747 [View Article][PubMed]
     [Google Scholar]
  155. Stoeck T, Hayward B, Taylor GT, Varela R, Epstein SS. A multiple PCR-primer approach to access the microeukaryotic diversity in environmental samples. Protist 2006; 157:31–43 [View Article][PubMed]
     [Google Scholar]
  156. Puitika T, Kasahara Y, Miyoshi N, Sato Y, Shimano S. A taxon-specific oligonucleotide primer set for PCR-based detection of soil ciliate. Microbes Environ 2007; 22:78–81 [View Article]
     [Google Scholar]
  157. Medlin L, Elwood HJ, Stickel S, Sogin ML. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 1988; 71:491–499 [View Article][PubMed]
     [Google Scholar]
  158. Lara E, Berney C, Harms H, Chatzinotas A. Cultivation-independent analysis reveals a shift in ciliate 18S rRNA gene diversity in a polycyclic aromatic hydrocarbon-polluted soil. FEMS Microbiol Ecol 2007; 62:365–373 [View Article][PubMed]
     [Google Scholar]
  159. Wang P, Wang Y, Wang C, Zhang T, Al-Farraj SA et al. Further consideration on the phylogeny of the Ciliophora: Analyses using both mitochondrial and nuclear data with focus on the extremely confused class Phyllopharyngea. Mol Phylogenet Evol 2017; 112:96–106 [View Article][PubMed]
     [Google Scholar]
  160. Hadziavdic K, Lekang K, Lanzen A, Jonassen I, Thompson EM et al. Characterization of the 18S rRNA gene for designing universal eukaryote specific primers. PLoS One 2014; 9:e87624 [View Article][PubMed]
     [Google Scholar]
  161. Hugerth LW, Muller EE, Hu YO, Lebrun LA, Roume H et al. Systematic design of 18S rRNA gene primers for determining eukaryotic diversity in microbial consortia. PLoS One 2014; 9:e95567 [View Article][PubMed]
     [Google Scholar]
  162. Xu Y, Vick-Majors T, Morgan-Kiss R, Priscu JC, Amaral-Zettler L. Ciliate diversity, community structure, and novel taxa in lakes of the McMurdo Dry Valleys, Antarctica. Biol Bull 2014; 227:175–190 [View Article][PubMed]
     [Google Scholar]
  163. Przybos´ E, Tarcz S, Surmacz M, Sawka N, Fokin SI. Paramecium tredecaurelia: a unique non-polymorphic species of the P. aurelia spp. complex (Oligohymenophorea, Ciliophora). Acta Protozool 2013; 52:257–266
     [Google Scholar]
  164. Barth D, Krenek S, Fokin SI, Berendonk TU. Intraspecific genetic variation in Paramecium revealed by mitochondrial cytochrome C oxidase I sequences. J Eukaryot Microbiol 2006; 53:20–25 [View Article][PubMed]
     [Google Scholar]
  165. Moreira D, von der Heyden S, Bass D, López-García P, Chao E et al. Global eukaryote phylogeny: combined small- and large-subunit ribosomal DNA trees support monophyly of Rhizaria, Retaria and Excavata. Mol Phylogenet Evol 2007; 44:255–266 [View Article][PubMed]
     [Google Scholar]
  166. Markmann M, Tautz D. Reverse taxonomy: an approach towards determining the diversity of meiobenthic organisms based on ribosomal RNA signature sequences. Philos Trans R Soc Lond B Biol Sci 2005; 360:1917–1924 [View Article][PubMed]
     [Google Scholar]
  167. Lynn DH, Strüder-Kypke MC. Species of tetrahymena identical by small subunit rRNA gene sequences are discriminated by mitochondrial cytochrome c oxidase I gene sequences. J Eukaryot Microbiol 2006; 53:385–387 [View Article][PubMed]
     [Google Scholar]
  168. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 1994; 3:294–299[PubMed]
     [Google Scholar]
  169. Zahid MT, Shakoori FR, Zulifqar S, Jahan N, Shakoori AR. A new ciliate species, Tetrahymena farahensis, isolated from the industrial wastewater and its phylogenetic relationship with other members of the genus Tetrahymena . Pakistan J Zool 2014; 46:1433–1445
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.003176
Loading
Techniques and tools for species identification in ciliates: a review
Int J Syst Evol Microbiol 69, 877 (2019); https://doi.org/10.1099/ijsem.0.003176
/content/journal/ijsem/10.1099/ijsem.0.003176
/content/journal/ijsem/10.1099/ijsem.0.003176
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error