New discoveries of the genus Thuricola Kent, 1881 (Ciliophora, Peritrichia, Vaginicolidae), with descriptions of three poorly known species from China

Borong Lu,

Daode JI,

Yalan Sheng,

Weibo Song,

Xiaozhong Hu,

Xiangrui Chen,

Khaled A. S. Al-Rasheid

Members of the genus Thuricola are a highly specialized group of peritrichous ciliates possessing a protective barrel-shaped lorica. The genus presents many difficulties in terms of species separation and definition, and in this context the present study investigates three species by protargol staining and analyses of SSU rDNA sequences. Based on their morphologic characteristics and biotope, they were identified as three poorly known forms in Thuricola, namely T. obconica Kahl, 1933, T. kellicottiana (Stokes, 1887) Kahl 1935 and T. folliculata Kent, 1881, respectively. T. obconica is characterized by possessing curved lorica and a single valve in vivo. T. kellicottiana is distinguished by two valves with a spine on the main valve, and a generally long internal stalk upon which the zooids sit. T. folliculata also has two valves but lacks a spine. The ciliature of the three species are basically similar. The main features are characterized as follows: infundibular polykineties 1–3 (P1–3) are relatively long and composed of three rows each; P1 bends twice and comprises three equally long rows; P2 ends near the second bend of P1 with all rows exhibiting a staggered arrangement; P3 converges with P1 at adstomal end, its row 1 
 at least twice as long as the other two rows; epistomial membranes 1 and 2 are present. Silverline system in Vorticella-pattern. Phylogenetic analyses indicate that the three ciliates in this study cluster together within one of the two major sub-clades within the Vaginicolidae. 
Słowa kluczowe: Ciliate, Loricate sessilids, Molecular phylogeny, Morphology, Silverline

Bernerth, I. (1982) Ökologische untersuchungen im kühlwassersystem eines konventionellen Großkraftwerks am untermain unter besonderer berücksichtigung der ciliaten (Protozoa). Cour. Forsch.-Inst. Senckenberg. 57: 1–246

Bick H. (1972) Ciliated protozoa: an illustrated guide to the species used as biological indicators in freshwater biology. World Health Organization

Biernacka I. (1963) Die Protozoenfauna in Dantziger Bucht. II. Die Charakteristik der Protozoen in Untersuchten Biotopen der Seekuste. Pol. Arch. Hydrobiol. 11: 53–75

Bock K. J. (1952) Über die marinen Arten der Gattung Thuricola (Ciliata, Peritricha). Kieler Meeresforsch. 8: 227–228

Bock K. J. (1963) Über das Auftreten einer Thuricola (Ciliata, Peritricha) in Belebtschlamm. Zool. Anz. 171: 91–96

Chen X., Pan H. B., Huang J. B., Warren A., Al-Farraj S.A., Gao S. (2016) New considerations on the phylogeny of cyrtophorian ciliates (Protozoa, Ciliophora): expanded sampling to understand their evolutionary relationships.Zool. Scr. 45: 334–348

Daday E. von. (1910) Untersuchungen über die Süsswasser-Mikrofauna Deutsch-Ost-Afrikas. Zoologica 22: 1–314

Dons C. (1922) Notes sur quelques Protozoaires marins. Vidensk. Meddel. Meddel. Dansk. Naturh. Foren. 73:49–84

Dons C. (1948) On some marine sedentary protozoans from Tristan da Cunha. Res. Norwegian Sci. Exped. Tristan da Cunha 1937–1938, 16: 1–16

Entz G. (1904) Einiges uber das variieren der infusorien. Mat. Naturwiss. Ber. Ungarn. 19:125–144.

Eperson S. (1980) Sur la stomatogenèse et les relations phylogenétiques du cilié pèritricha Thuricola folliculata (O. F. Müller, 1786). Protistologica16: 549–564

Foissner W. (1988) A taxonomic and nomenclatural revision of Sladecek’s list of ciliates (Protozoa: Ciliophora) as indicators of water quality. Hydrobiologia166: 1–64

Foissner W., Berger H., Kohmann F. (1992) Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems – Band II: Peritrichida, Heterotrichida, Odontostomtida. Informationsberichte des Bayer. Landesamtes Wasserwirtsch. 5/92: 1–502

Foissner W., Blake N., Klaus W. O. L. F., Breiner H. W., Stoeck T. (2010) Morphological and molecular characterization of some peritrichs (Ciliophora: Peritrichida) from tank bromeliads, including two new genera: Orborhabdostyla and Vorticellides. Acta Protozool. 48: 291–319

FromentelE. de. (1874–1876) Études sur les microzoaires ou infusoires proprement dits omprenant de nouvelles recherches sur leur organization, leur classification et la description des espèces nouvelles ou peu connus. G. Masson, Paris

Gao F., Huang J. A., Zhao Y., Li L. F., Liu W. W., Miao M., Zhang Q. Q., Li J. M., Yi Z. Z., El-Serehy H. A., Warren A., Song W. B. (2017) Systematic studies on ciliates (Alveolata, Ciliophora): progress and achievements based on molecular information. Eur. J. Protistol. 61: 409–423

Gao F., Li J. M., Song W., Xu D., Warren A., Yi Z. Z., Gao S. (2016a) Multi-gene-based phylogenetic analysis of oligotrich ciliates with emphasis on two dominant groups: Cyrtostrombidiids and strombidiids (Protozoa, Ciliophora). Mol. Phylogenet. Evol. 105: 241–250

Gao F., Warren A., Zhang Q. Q., Gong J., Miao M., Sun P., Xu D., Huang J. A., Yi Z. Z., Song W. B. (2016b) The all-data-based evolutionary hypothesis of ciliated protists with a revised classification of the phylum Ciliophora (Eukaryota, Alveolata). Sci. Rep. 6: 24874

Gentekaki E., Kolisko M., Gong Y., Lynn D. (2017) Phylogenomics solves a long-standing evolutionary puzzle in the ciliate world: The subclass Peritrichia is monophyletic.Mol. Phylogenet. Evol. 106: 1–5

Gong X. J. (1989a) Descriptions of six new species of peritrich from Xinjiang, China. Acta Hydrobiol. Sin. 14: 396–403 (in Chinese with English summary)

Gong X. J. (1989b) Descriptions of three new species of peritrich from Qinghai province, China, Acta Hydrobiol. Sin. 14: 257–261 (in Chinese with English summary)

Hall T. A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. NucleicAcids Symp. Ser.41: 95–98

Hammann I. (1952) Ökologische und biologische Untersuchungen an Süßwasserperitrichen. Arch. Hydrobiol. 47: 177–228

Huang J. B., Luo X. T., Bourland W. A., Gao F. Gao S. (2016) Multigene-based phylogeny of the ciliate families Amphisiellidae and Trachelostylidae (Protozoa: Ciliophora: Hypotrichia). Mol. Phylogenet. Evol. 101: 101–110

Jerome C. A., Simon E. M., Lynn D. H. (1996) Description of Tetrahymena empidokyrea n. sp., a new species in the Tetrahymena pyriformis sibling species complex (Ciliophora, Oligohymenophorea), and an assessment of its phylogenetic position using small-subunit rRNA sequences. Can. J. Zool. 74: 1898–1906

Ji D., Kim J. H., Shahed S. U. A., Sun P., Li L. F., Shin M. K. (2015) Two new species of Zoothamnium (Ciliophora, Peritrichia) from Korea, with new observations of Z. parahentscheli Sun et al., 2009. J. Eukaryot. Microbiol. 62: 505–518

Jiang X. Z., Shen Y. F., Gong X. J. (1983) Aquatic invertebrates of the Tibetan Plateau. Science Press, Beijing

Kahl A. (1933) Ciliata libera et ectocommensalia. In: Grimpe, G., Wagler, E. (Eds.), Tierwelt Nord Ostsee 23 (Teil II, c3). 29–146

Kahl A. (1935) Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria) 4 Peritricha und Chonotricha. Tierwelt Dtl. 30: 651–886

Kellicott D. S. (1884) Observations on infusoria, with descriptions of new species. Proc. Amer. Soc. Microsc. 6: 110–125

Kent W. S. (1881–1882) A manual of the infusoria: including a description of all known flagellate, ciliate, and tentaculiferous protozoa British and foreign, and an account of the organization and affinities of the sponges. David Bogue, London (Vol. II 1881: 433–720; Vol. III 1882: Plates)

Kudo R. R. (1939) Protozoology, second edition. Charles C Thomas, Springfield, Illinois

Kumar S., Stecher G., Tamura K. (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870–1874

Küsters E. (1974) Ökologische und systematische Untersuchungen der Aufwuchsciliaten im Königshafen bei List/Sylt. Arch. Hydrobiol. (suppl.) 45: 121–211

Landan G., Graur D. (2008) Local reliability measures from sets of co-optimal multiple sequence alignments. Pac Symp. Biocomput. 13: 15–24

Li J. M., Liu W. W, Gao S., Warren A., Song W. B. (2013) 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 12: 430–437

Liebmann H. (1962) Handbuch der Frischwasser- und Abwasser-biologie. Biologie des Trinkwassers, Badewassers, Fischwassers, Vorfluters und Abwassers. Band I (2nd ed.), 588

Liu W. W., Jiang J. M., Xu Y., Pan X. M., Qu Z. S., Luo X. T., Warren A., Ma H. G., Pan H. B. (2017) Great diversity in marine ciliates: fauna studies in China seas during the years 2011-2016. Eur. J. Protistol. 61:424–438

Lu X., Huang J. A., Shao C., Al-Farraj S. A., Gao S. (2017) Morphology and morphogenesis of a novel saline soil hypotrichous ciliate, Gonostomum sinicum nov. spec. (Ciliophora, Hypotrichia, Gonostomatidae), including a report on the small subunit rDNA sequence. J. Eukaryot. Microbiol. 64: 632–646

Lynn D. H. (2008) The ciliated protozoa: characterization, classification, and guide to the literature, third edition. Springer, Dordrecht

Medlin L., Elwood H. J., Stickel S., Sogin M. L. (1988) The characterization of enzymatically amplified eukaryotes 16S-like ribosomal RNA coding regions. Gene71: 491–500

Müller, O. F. (1786) Animalcula infusoria fluviatilia et marina. Havniae et Lipsize

Nusch E. A. (1970) Ökologische und systematische Untersuchungen der Peritricha (Protozoa, Ciliata) im Aufwuchs von Talsperren und Flusstauen mit verschiedenem Saprobitatsgrad (mit Modellversuchen). Arch. Hydrobiol. (suppl.) 37: 243–386

Nylander J. A. A. (2004) MrModeltest version 2. Evolutionary Biology Centre, Uppsala University, Uppsala

Pan H. B., Jiang J. M., Fan X., Al-Farraj S. A., Gao S. (2017) Phylogeny and taxonomy of five poorly known species of cyrtophorian ciliates (Protozoa: Ciliophora: Phyllopharyngea) from China Seas. Zool.J.Linn.Soc. 180: 475–492

Pan X. M., Bonrland W., Song W. B. (2013) Protargol synthesis: an in-house protocol. J. Eukaryot. Microbiol. 60: 609–614

Penard E. (1914) Les cothurnidés muscicoles. Mém. Soc. Phys. Hist. Nat. Genève 38: 19–68

Penard E. (1922) Études sur les Infusoires d’eau douce. Georg & Cie, Genève 1–331

Peng X., Shi X., Warren A. (2007) Establishment of a new peritrich ciliate genus, Pseudepistylis n. gen. (Ciliophora: Peritrichia: Epistylididae), with a description of a new freshwater species, Pseudepistylis songi n. sp. from Wenzhou, China. Zootaxa 1524: 35–45

Qu Z. S., Pan H. B., Al-Rasheid K. A. S., Hu X., Gao S. (2015) Morphological and phylogenetic studies on three members of the genus Pseudochilodonopsis (Ciliophora, Cyrtophoria) isolated from brackish waters in China, including a novel species, Pseudochilodonopsis quadrivacuolata sp. nov. Int.J.Syst.Evol.Microbiol. 65: 4323–4334

Ronquist F., Teslenko M., Van Der Mark P., Ayres D. L., Darling A., Höhna S., Larger B., Liu L., Suchard M. A., Hurlsenbeck J. P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539–542

Sela I., Ashkenazy H., Katoh K., Pupko T. (2015) GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res.43: W7–W14

Shen Y. F., Gu M. R. (2016) Fauna Sinica: Invertebrata vol. 45 Ciliophora Oligohymenophorea Peritrichida. Science Press, Beijing

Shen Z., Ji D., Yi Z. Z., Al-Rasheid K. A. S., Lin X. (2017) Morphology and phylogenetic placement of three new Zoothamnium species (Ciliophora: Peritrichia) from coastal waters of southern China.J. Eukaryot. Microbiol. 64: 266–277

Sommer G. (1951) Die peritrichen ciliaten des Grossen Plöner Sees. Arch. Hydrobiol. 44: 349–440

Sun P, Al-Farraj S. A., Warren A., Ma H. G. (2017) Morphology of four new solitary sessile peritrichs (Ciliophora, Peritrichia) from the Yellow Sea, China, with description on an unidentified species of Paravorticella. Eur. J. Protistol. 57: 73–84

Sun P., Clamp J. C., Xu D., Huang B., Shin M. H. (2016) An integrative approach to phylogeny reveals patterns of environmental distribution and novel evolutionary relationships in a major group of ciliates. Sci. Rep. 6: 21695

Sun P., Clamp J. C., Xu D., Kusuoka Y., Miao W. (2012) Vorticella Linnaeus, 1767 (Ciliophora, Oligohymenophora, Peritrichia) is a grade not a clade: Redefinition of Vorticella and the families Vorticellidae and Astylozoidae using molecular characters derived from the gene coding for small subunit ribosomal RNA. Protist 163: 129–142

Sun P., Ji D., Warren A., Song W. B. (2009) Solitary sessilid peritrichs. In: Free-living ciliates in the Bohai and Yellow Seas, China, (Eds. W.B Song, A. Warren, X. Hu). Science Press, Beijing, 251–254

Stamatakis A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313

Stiller J. (1971) Szájkoszorús csillósok. - Peritricha.Fauna Hung. 105: 1–245 (in Hungarian)

Stokes A. C. (1882) A new Thuricola. Amer. Month. Microsc. J. 3: 182–183

Stokes A. C. (1887) Notices of new fresh-water infusoria. Proc. Am. Phil. Soc. 24: 244–255

Stokes A. C. (1888a) A generic synopsis of the sedentary freshwater Peritricha. An elementary chapter for beginners. Amer. Month Microsc. J. 9: 59–64

Stokes A. C. (1888b) A preliminary contribution toward a history of the fresh-water infusoria of the United States. J. Trenton Nat. Hist. Soc. 1: 71–344

Trueba F. J. (1978) A taxonomic revision of the peritrich ciliate genus Pyxicola. Beaufortia 27: 219–243

Trueba, F. J. (1980) A taxonomic revision of the peritrich ciliate genera Thuricola and Pseudothuricola. Beaufortia 30: 125–138

Wang P., Wang Y. R., Wang C. D., Zhang T. T., Al-Farraj S. A., Gao F. (2017) 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. 112: 96–106

Warren A. (1982) A taxonomic revision of the genus Platycola (Ciliophora: Peritrichida). Bull. Br. Mus. nat. Hist. Zool. 43:95–108

Warren A. (1991) A revision of Cothurnia (Ciliophora: Peritrichida). Bull. Br. Mus. nat. Hist. Zool. 57: 17–59

Wilbert N. (1975) Eine verbesserte Technik der Protargolimprägnation für Ciliaten. Mikrokosmos64: 171–179

Wright T. S. (1858) Description of new protozoa. Edingburgh New Philos. J. 7: 276–281

Xu Z. K. (1990) Notes on two new species of genus Thuricola from Tianjin. Acta Zootaxon. Sin. 15: 6–9 (in Chinese with English summary)

Yan Y., Xu Y., Al-Farraj S. A., Al-Rasheid K. A. S., Song W. B. (2016a) Morphology and phylogeny of three trachelocercids(Protozoa, Ciliophora, Karyorelictea), with description of two new species and insight to the evolution of the family Trachelocercidae.Zool. J. Linn. Soc.177:306–319

Yan Y., Fan Y., Chen X. R., Li L. F., Warren A., Al-Farraj S. A., Song W. B. (2016b) Taxonomy and phylogeny of three heterotrich ciliates (Protozoa, Ciliophora), with description of a new Blepharisma species. Zool. J. Linn. Soc.177:320–334

Zhuang Y., Clamp J. C., Yi Z. Z., Ji D. (2016) A new peritrich ciliate from a hapersaline habitat in northern China. Zootaxa 4169: 179–186

Zhuang Y., Clamp J. C., Yi Z. Z., Ji D. (2018) Phylogeny of the families Zoothamniidae and Epistylididae (Protozoa: Ciliophora: Peritrichia) based on analyses of three rRNA-coding regions. Mol. Phylogenet. Evol. 118: 99–107

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