Morphology and Phylogeny of Four Marine Scuticociliates (Protista, Ciliophora), with Descriptions of Two New Species: Pleuronema elegans spec. nov. and Uronema orientalis spec. nov.

Xuming Pan,

Feng Gao,

Miao Miao,

Khaled A. S. Al-Rasheid,

Honggang Ma,

Xinpeng Fan,

Jie Huang


The morphology and infraciliature of four marine scuticociliates, Pleuronema elegans spec. nov., P. setigerum Calkins, 1902, P. grolierei Wang et al., 2008 and Uronema orientalis spec. nov., collected from China seas, were investigated through live observation and protargol staining methods. Pleuronema elegans spec. nov. can be recognized by the combination of the following characters: size in vivo 90–115 × 45–60 µm, slender oval in outline with a distinctly pointed posterior end; about 10 prolonged caudal cilia; consistently two preoral kineties and 18 or 19 somatic kineties; membranelle 2a double-rowed with its posterior end straight; membranelle 3 three-rowed; one macronucleus; marine habitat. Uronema orientalis spec. nov. is distinguished by the following features: in vivo about 40–55 × 20–30 μm with a truncated apical plate; consistently twenty somatic kineties; membranelle 1 single-rowed and divided into two parts which comprise four and three basal bodies respectively; contractile vacuole pore positioned at the end of the second somatic kinety; marine habitat. We also provide improved diagnoses for P. grolierei Wang et al., 2008 and P. setigerum Calkins, 1902 based on current and previous reports. The small subunit rRNA gene of U. orientalis, P. elegans, P. grolierei and P. puytoraci were sequenced. Phylogenetic analyses indicate that Uronema and Pleuronema are not monophyletic.

Słowa kluczowe: Scuticociliates, Pleuronema elegans spec. nov., Uronema orientalis spec. nov., phylogeny

Agatha S., Spindler M., Wilbert N. (1993) Ciliated protozoa (Ciliophora) from Arctic Sea Ice. Acta Protozool. 32: 261–268

Borror A. C. (1963) Morphology and ecology of some uncommon ciliates from Alligator Harbour, Florida. Trans. Am. Microsc. Soc. 82: 125–131

Budiño B., Lamas J., Pata M., Arranz J., Sanmartín M., Leiro J. (2011) Intraspecific variability in several isolates of Philasterides dicentrarchi (syn. Miamiensis avidus), a scuticociliate parasite of farmed turbot. Veterinary Parasitology 175: 260–272

Czapik A. (1964) La stomatogénčse du Cilié Uronema marinum Dujardin (Hymenostomatida, Tetrahymenina). Acta Protozool2: 207–211

Czapik A., Jordan A. (1977) Two new psammobiotic ciliates Hippocomos loricatus gen. n. sp. and Pleuronema tardum n. sp. (Hymenostomata, Pleuronematina). Acta Protozool16: 157–164

Dragesco J., Dragesco-Kernéis A. (1986) Ciliés libres de l’Afrique intertropicale. Introduction à la connaissance et à l’étude des Ciliés. Faune. Trop. Orstom24: 1559

Fan X., Hu X., Al-Farraj S. A., Clamp J. C., Song W. (2011a) Morphological description of three marine ciliates (Ciliophora, Scuticociliatia), with establishment of a new genus and two new species. Eur. J. Protistol47: 186–196

Fan X., Lin X., Al-Rasheid K. A. S., Warren A., Song W. (2011b) The diversity of scuticociliates (Protozoa, Ciliophora): a report on eight marine forms found in coastal waters of China, with a description of one new species. Acta Protozool50: 219–234

Fernandez-Leborans G., Novillo A. (1994) Morphology and taxonomic position of two marine pleuronematine species: Pleuronema lynni and Schizocalyptra marina (Protozoa, Ciliophora). J. Zool. Lond233: 259–275

Foissner W. (1971) Das silberliniensystem von Uronema parduczi sp. n. (Ciliata, Hymenostomatida, Uronematidae). Arch. Protistenkd 113: 34–50

Foissner W., Berger H., Kohmann F. (1994) Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems. Band III: Hymenostomata, Prostomatida, Nassulida. Inform.-ber. Bayer. Land. Wasserwirt. 1/94, 1–548

Foissner W., Jung J., Filker S., Rudolph J., Stoeck T. (2013) Morphology, ontogenesis and molecular phylogeny of Platynematum salinarum nov. spec., a new scuticociliate (Ciliophora, Scuticociliatia) from a solar saltern. Eur. J. Protistol. (in press).

Foissner W., Wilbert N. (1981) A comparative study of the infraciliature and silverline system of the freshwater scuticociliates Pseudocohnilembus putrinus (Kahl, 1928) nov. comb., P. pusillus (Quennerstedt, 1869) nov. comb., and the marine forms 
P. marinus Thompson, 1966. J. Protozool.28: 291–297

Gao F., Fan X., Yi Z., Strüder-Kypke M., Song W. (2010) Phylogenetic consideration of two scuticociliate genera, Philasterides and Boveria (Protozoa, Ciliophora) based on 18S rRNA gene sequences. Parasitol. Internat. 59: 549–555

Gao F., Katz L. A. (2014) Phylogenomic analyses support the bifurcation of ciliates into two major clades that differ in properties of nuclear division. Mol. Phylogenet. Evol.70: 240–243

Gao F., Katz L. A., Song W. (2012a) Insights into the phylogenetic and taxonomy of philasterid ciliates (Protozoa, Ciliophora, Scuticociliatia) based on analyses of multiple molecular markers. Mol. Phylogenet. Evol. 64: 308–317

Gao F., Katz L. A., Song W. (2013) Multigene-based analyses on evolutionary phylogeny of two controversial ciliate orders: Pleuronematida and Loxocephalida (Protista, Ciliophora, Oligohymenophorea). Mol. Phylogenet. Evol. 68: 55–63

Gao F., Strüder-Kypke M., Yi Z., Miao M., Al-Farraj S. A., Song W. (2012b) Phylogenetic analysis and taxonomic distinction of six genera of pathogenic scuticociliates (Protozoa, Ciliophora) inferred from small-subunit rRNA gene sequences. Inter. J. Syst. Evol. Microbiol62: 246–256

Grolière C. A. (1974) Étude comparée de la stomatogenèse chez quelques cilies hymenostomes des genres Paralembus Kahl, 1933, Philaster Fabre-Domergue, 1885, Parauronema Thompson, 1967, Tetrahymena Furgasson, 1940. Protistologica 10: 319–331

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

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

Kahl A. (1931) Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria). 2. Holosticha Tierwelt Dtl. 21: 181–398

Lobban C. S., Raymundo L. M., Montagnes D. J. S. (2011) Porpostoma guamensis n. sp., a philasterine scuticociliate associated with brown band disease of corals. J. Eukaryot. Microbiol. 58: 103–113

Long H., Song W., Wang Y., Li J. (2007) Morphological redescription of two endocommensal ciliates, Entorhipidium fukuii Uyemura, 1934 and Madsenia indomita (Madsen, 1931) Kahl, 1934 from digestive tracts of sea urchins of the Yellow Sea, China (Ciliophora; Scuticociliatida). Eur. J. Protistol. 43: 101–114

Lynn D. H. (2008) The Ciliated Protozoa. Characterization, classification and guide to the literature. Springer Verlag, Dordrecht

Lynn D. H., Strüder-Kypke M. (2005) Scuticociliate endosymbionts of echinoids (phylum Echinodermata): phylogenetic relationships among species in the genera Entodiscus, Plagiopyliella, Thyrophylax, and Entorhipidium (phylum Ciliophora). J. Parasitol. 91: 1190–1199

Ma H., Song W. (2003) Stomatogenesis of the marine ciliate Metanophrys sinensis (Protozoa: Ciliophora: Scuticociliatida). J. Mar. Biol. Ass. U. K. 83: 407–410

Medlin L., Elwood H. J., Stickel S., Sogin M. L. (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71: 491–499

Miao M., Wang Y., Li L., Al-Rasheid K. A. S., Song W. (2009) Molecular phylogeny of the scuticociliate Philaster (Protozoa, Ciliophora) based on SSU rRNA gene sequences information, with description of a new species P. apodigitiformis sp. n. Syst. Biodivers. 7: 381–388

Miao M., Warren A., Song W., Wang S., Shang H., Chen Z. (2008) Analysis of the internal transcribed spacer 2 (ITS2) region of scuticociliates and related taxa (Ciliophora, Oligohymenophorea) to infer their evolution and phylogeny. Protist 159: 519–533

Noland L. E. (1937) Observations on marine ciliates of the gulf coast of Florida. Trans. Am. Micros. Soc. 56: 160–171

Nylander J. A. A. (2004) MrModeltest version 2. Distributed by the author. Department of Systematic Zoology, Evolutionary Biology Centre, Uppsala University, Uppsala

Pan H., Huang J., Hu X., Fan X., Al-Rasheid K. A. S., Song W. (2010) Morphology and SSU rRNA gene sequences of three marine ciliates from Yellow Sea, China, including one new species, Uronema heteromarinum nov. spec. (Ciliophora, Scuticociliatida). Acta Protozool49: 45–49

Pan X., Bourland W., Song W. (2013a) Protargol Synthesis: An in-house protocol. J. Eukaryot. Microbiol. 60: 609–614

Pan X., Gao F., Liu W., Fan X., Warren A., Song W. (2013b) Morphology and SSU rRNA gene sequences of three Frontonia species, including a description of F. subtropica spec. nov. (Ciliophora, Peniculida). Eur. J. Protistol49: 67–77

Pan X., Liu W., Yi Z., Fan X., Al-Rasheid K., Lin X. (2013c) Studies on three diverse Frontonia species (Ciliophora, Peniculida), with brief notes on 14 marine or brackish congeners. Acta Protozool52: 35–49

Pan X., Shao C., Ma H., Fan X., Al-Rasheid K. A. S., Al-Farraj S. A., Hu X. (2011) Redescriptions of two marine scuticociliates from China, with notes on stomatogenesis in Parauronema longum (Ciliophora, Scuticociliatida). Acta Protozool50: 301–310

Pan X., Zhu M., Ma H., Al-Rasheid K. A. S., Hu X. (2013d) Morphology and small-subunit rRNA gene sequences of two new marine ciliates, Metanophrys orientalis spec. nov. and Uronemella sinensis spec. nov. (Protista, Ciliophora, Scuticociliatia), with an improved diagnosis of the genus UronemellaInter. 
J. Syst. Evol. Microbiol
63: 3513–3523

Perez-Uz, B., Song W. (1995) Uronema gallicum sp. n. (Protozoa: Ciliophora) a new marine scuticociliate from the coastal area of Calais. Acta Protozool. 34: 143149

Posada D., Crandall K. A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818

Ronquist F., Huelsenbeck J. P. (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574

Salinas I., Maas E. W., Muñoz P. (2011) Characterization of acid phosphatases from marine scuticociliate parasites and their activation by host’s factors. Parasitology 138: 836–847

Seo J., Jeon E., Jung S., Park M., Kim J., Kim K., Woo S., Lee E. (2013) Molecular cloning and expression analysis of peptidase genes in the fish-pathogenic scuticociliate Miamiensis avidus. BMC Veterinary Research 9: 10

Small E. B. (1964) An analysis of morphology and ontogenesis in the genus Pleuronema Dujardin, 1841, a description of two new species and a new genus, and a comparative analysis of stomatogenesis. Ph. D. Dissertation. Univ. California, Los Angeles, 297 pp.

Small E. B., Lynn D. H. (1985) Phylum Ciliophora Doflein, 1901. In: An illustrated guide to the Protozoa, (Eds. J. J. Lee, S. H. Hunter, E. C. Bovee). Society of Protozoologist, Lawrence, Kansas, 393–575

Song W. (2000) Morphological and taxonomical studies on some marine scuticociliates from China Sea, with description of two new species, Philasterides armatalis sp. n. and Cyclidium varibonneti sp. n. (Protozoa: Ciliophora: Scuticociliatida). Acta Protozool. 39: 295–322

Song W., Shang H., Chen Z., Ma H. (2002) Comparison of some closely-related Metanophrys-taxa with description of a new species Metanophrys similis nov. spec. (Ciliophora, Scuticociliatida). Eur. J. Protistol. 38: 45–53

Song W., Warren A., Hu X. (2007) Free-living ciliates in Bohai and Yellow Sea, China. Science Press, Beijing

Song W., Wilbert N. (2000) Redefinition and redescription of some marine scuticociliates from China, with report of a new species, Metanophrys sinensis nov. spec. (Ciliophora, Scuticociliatida). Zool. Anz. 239: 45–74

Song W., Wilbert N. (2002) Reinvestigations of three “well-known” marine scuticociliates: Uronemella filificum (Kahl, 1931) nov. gen., nov. comb., Pseudocohnilembus hargisi Evans & Thompson, 1964 and Cyclidium citrullus Cohn 1865, with description of the new genus Uronemella (Protozoa, Ciliophora, Scuticociliatida).Zool. Anz. 241: 317–331

Tamura K., Dudley J., Nei M., Kumar S. (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596–1599

Thompson J. C. (1964) A redescription of Uronema marinum, and a proposed new family Uronematidae. Virginia J. Sci. 15: 80–87

Thompson J. C. (1972) Ciliated protozoa of the Antarctic Peninsula. In: Antarctic terrestrial biology, (Ed. G. A. Llano). Antarctic Res. Ser. 20: 261–288

Thompson J. C., Kaneshiro E. S. (1968) Redescriptions of Uronema filificum and Uronema elegans. J. Protozool. 15: 141–144

Wang Y., Hu X., Long H., Al-Rasheid K. A. S., Al-Farraj S., Song W. (2008a) Morphological studies indicate that Pleuronema grolierei nov. spec. and P. coronatum Kent, 1881 represent different sections of the genus Pleuronema (Ciliophora: Scuticociliatida). Eur. J. Protistol. 44: 131–140

Wang Y., Song W., Hu X., Warren A., Chen X., Al-Rasheid K. A. S. 
(2008b) Descriptions of two new marine species of 
Pleuronema, P. czapikae sp. n. and P. wiackowskii sp. n. (Ciliophora: Scuticociliatida), from the Yellow Sea, North China. Acta Protozool. 47: 35–45

Wang Y., Song W., Warren A., Al-Rasheid K. S., Al-Quraishy S., Al-Farraj S. A., Hu X., Pan H. (2009) Descriptions of two new marine scuticociliates, Pleuronema sinica n. sp. and P. wilberti n. sp. (Ciliophora: Scuticociliatida), from the Yellow Sea, China. Eur. J. Protistol. 45: 29–37

Whang I., Kang H. S., Lee J. (2013) Identification of scuticociliates (Pseudocohnilembus persalinusP. longisetusUronema marinum and Miamiensis avidus) based on the cox1 sequence. Parasitol. Int. 62: 7–13

Wilbert N., Song W. (2008) A further study on littoral ciliates (Protozoa, Ciliophora) near King George Island, Antarctica, with description of a new genus and seven new species. J. Nat. Hist. 42: 979–1012

Yi Z., Song W., Gong J., Warren A., Al-Rasheid K.A.S., Al-Arifi S., Al-Khedhairy A.A. (2009) Phylogeny of six oligohymenophoreans (Protozoa, Ciliophora) inferred from small subunit rRNA gene sequences. Zool. Scr. 38: 323–331





Received on 2nd December, 2013; revised on 6th February, 2014; accepted on 26th March, 2014

Czasopismo w darmowym dostępie.

Czasopismo ukazuje się w sposób ciągły on-line.
Pierwotną formą czasopisma jest wersja elektroniczna.