, Volume 806, Issue 1, pp 313–331 | Cite as

Reconsideration of the systematics of Peniculida (Protista, Ciliophora) based on SSU rRNA gene sequences and new morphological features of Marituja and Disematostoma

  • Yuan Xu
  • Feng Gao
  • Xinpeng FanEmail author
Primary Research Paper


Ciliated protists are unicellular eukaryotes that play important roles in aquatic ecosystems. One of the major tasks of ciliate taxonomy is to re-evaluate the systematic confusing taxa using modern methods. In the present study, two peniculid ciliates, Marituja cf. caudata and Disematostoma minor collected from east China, were studied using a multi-method approach. New morphological observations supplied additional information for species identification and systematic revision of the order Peniculida. The small subunit ribosomal RNA gene sequences of M. cf. caudata, D. minor, and Frontonia terricola were characterized for the first time and provided new insights into the phylogeny of Peniculida. The family Stokesiidae Roque, 1961, was expanded to include the genera Disematostoma and Marituja in addition to its type genus Stokesia, since the three genera formed a well-supported clade in the phylogenetic analyses. The diagnosis of Stokesiidae was improved to include the newly recognized synapomorphies, i.e., barren kinetosomes on the dorsal side, a ciliated dorsal suture, and the somatic ciliature that can be recognized as transversely oriented circles. Additionally, the systematic relationships of the genera and families of Peniculida were hypothesized. We argue that more diversified morphological features should be considered when assessing diagnostic traits for ciliate taxa during systematic revisions.


Ciliate Frontoniidae Maritujidae Phylogeny Stokesiidae Taxonomy 



This work was supported by the National Natural Science Foundation of China [Nos. 31572223, 31601843], and the Fundamental Research Funds for the Central Universities (201762017). We thank Dr. Rui Ma and Dr. Bing Ni for their help with scanning electron microcopy.

Supplementary material

10750_2017_3371_MOESM1_ESM.docx (2.8 mb)
Supplementary material 1 (DOCX 2901 kb)


  1. Corliss, J. O., 1953. Silver impregnation of ciliated protozoa by the Chatton-Lwoff technic. Biotechnic and Histochemistry 28: 97–100.Google Scholar
  2. Corliss, J. O., 1979. The Ciliated Protozoa. Characterization, Classification and Guide to the Literature. Pergamon Press, New York.Google Scholar
  3. Didier, P., 1994. Sous-classe des Peniculia. In de Puytorac, P. (ed.), Infusoires ciliés. Fasc. 2. Systématique. Traité de Zoologie, Vol. 2. Masson Press, Paris: 603–620.Google Scholar
  4. Dragesco, J. & D. Dragesco-Kernéïs, 1986. Cilies libres de l’ Afrique intertropicale. Collection Faune Tropicale, Vol. 26. ORSTOM, Paris: 1–559.Google Scholar
  5. Fan, X., X. Chen, W. Song, K. A. S. Al-Rasheid & A. Warren, 2010. Two new marine scuticociliates, Sathrophilus planus n. sp. and Pseudoplatynematum dengi n. sp., with improved definition of Pseudoplatynematum (Ciliophora, Oligohymenophorea). European Journal of Protistology 46: 212–220.CrossRefPubMedGoogle Scholar
  6. Fan, X., X. Chen, W. Song, K. A. S. Al-Rasheid & A. Warren, 2011. Two novel marine Frontonia species, F. mengi spec. nov. and F. magna spec. nov. (Protozoa; Ciliophora), with notes on their phylogeny based on SSU rRNA gene sequence data. International Journal of Systematic and Evolutionary Microbiology 61: 1476–1486.CrossRefPubMedGoogle Scholar
  7. Fan, X., X. Lin, W. Liu, Y. Xu, S. A. Al-Farraj & A. Warren, 2013. Morphology and phylogeny of three new marine Frontonia species (Ciliophora; Peniculida) from coastal waters of China. European Journal of Protistology 49: 312–323.CrossRefPubMedGoogle Scholar
  8. Foissner, W., 1987. Neue terrestrische und limnische Ciliaten (Protozoa, Ciliophora) aus Österreich und Deutschland. Sitzungsberichte der Akademie der Wissenschaften 195: 217–268.Google Scholar
  9. Foissner, W., 2013. Description of Glaucomides bromelicola n. gen. n. sp. (Ciliophora, Tetrahymenida), a macrostome forming inhabitant of bromeliads (Bromeliaceae), including redescriptions of Glaucoma scintillans and G. reniformis. Journal of Eukaryotic Microbiology 60: 137–157.CrossRefPubMedGoogle Scholar
  10. Foissner, W. & W. Song, 2002. Apofrontonia lametschwandtneri nov. gen., nov. spec., a new peniculine ciliate (Protozoa, Ciliophora) from Venezuela. European Journal of Protistology 38: 223–234.CrossRefGoogle Scholar
  11. Foissner, W., H. Berger & F. Kohmann, 1994. Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems-Band III: Hymenostomata, Prostomatida, Nassulida. Informationsberichte des Bayerrischen Landesamtes für Wasserwirtschaft 1(94): 1–548.Google Scholar
  12. Foissner, W., H. Berger & J. Schaumburg, 1999. Identification and ecology of limnetic plankton ciliates. Informationsberichte des Bayerrischen Landesamtes für Wasserwirtschaft 3(99): 1–793.Google Scholar
  13. Fokin, S. I., 2008. Rediscovery and characterization of Frontonia fusca (Quennerstedt, 1869) Kahl, 1931 (Ciliophora, Peniculia). Denisia 23: 251–259.Google Scholar
  14. Fokin, S. I., I. Andreoli, F. Verni & G. Petroni, 2006. Apofrontonia dohrni sp. n. and the phylogenetic relationships within Peniculia (Protista, Ciliophora, Oligohymenophorea). Zoologica Scripta 35: 289–300.CrossRefGoogle Scholar
  15. Gao, S., Z. Chen, C. Shao, H. Long, K. A. S. Al-Rasheid & W. Song, 2008. Reconsideration of the phylogenetic position of Frontonia-related Peniculia (Ciliophora, Protozoa) inferred from the small subunit ribosomal RNA gene sequences. Acta Protozoologica 47: 47–54.Google Scholar
  16. Gao, F., A. Warren, Q. Zhang, J. Gong, M. Miao, P. Sun, D. Xu, J. Huang, Z. Yi & W. Song, 2016. The all-data-based evolutionary hypothesis of ciliated protists with a revised classification of the phylum Ciliophora (Eukaryota, Alveolata). Scientific Reports 6: 24874.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gill, R., 1992. Cytoskeletal elements of Frontonia leucas (Ciliophora: Hymenostomatida). Transactions of the American Microscopical Society 111: 327–337.CrossRefGoogle Scholar
  18. Gouy, M., S. Guindon & O. Gascuel, 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27: 221–224.CrossRefPubMedGoogle Scholar
  19. Gu, F. & B. Ni, 1993. The exploration of preparing protozoan specimen for scanning electron microscopy. Journal of Chinese Electron Microscopy Society 12: 525–529.Google Scholar
  20. Guinea, A., A. Sola, J. Longas & D. Fernandez-Galiano, 1990. Morphology and morphogenesis of two species of the genus Lembadion (Ciliophora, Oligohymenophora): Lembadion lucens and Lembadion bullinum. Journal of Eukaryotic Microbiology 37: 553–561.Google Scholar
  21. Huang, J., Z. Chen, W. Song & H. Berger, 2014. Three-gene based phylogeny of the Urostyloidea (Protista, Ciliophora, Hypotricha), with notes on classification of some core taxa. Molecular Phylogenetics and Evolution 70: 337–347.CrossRefPubMedPubMedCentralGoogle Scholar
  22. International Commission on Zoological Nomenclature, 1999. International code of zoological nomenclature, adopted by the International Union of Biological Sciences. International Trust for Zoological Nomenclature, London.Google Scholar
  23. Jankowski, A. W., 2007. Phylum Ciliophora Doflein, 1901. In Alimov, A. F. (ed.), Protista. Part 2, Handbook on Zoology. Russian Academy of Sciences, Zoological Institute, Nauka, St. Petersburg: 415–993.Google Scholar
  24. Kahl, A., 1926. Neue und wenig bekannte Formen der holotrichen und heterostrichen Ciliaten. Archiv Für Protistenkunde 55: 197–438.Google Scholar
  25. Kahl, A., 1931. Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria). 2. Holotricha. Tierwelt Dtl 21: 181–398.Google Scholar
  26. Krainer, K. H., 1988. Alpha-Taxonomie und Ökologie neuer sowie mehrerer wenig bekannter pelagischer Ciliaten (Protozoa: Ciliophora aus den Klassen Kinetofragminophora, Oligohymenophora, Polyhymenophora) einiger Grundwasserbaggerteiche des nordlichen Leibnitzer Feldes (Steiermark, Österreich). Dissertation of University of Graz, 209+41.Google Scholar
  27. Krainer, K. H., 1995. Taxonomische Untersuchungen an neuen und wenig bekannten planktischen Ciliaten (Protozoa: Ciliophora) aus Baggerseen in Österreich. Lauterbornia 21: 39–68.Google Scholar
  28. Krenek, S., T. U. Berendonk & S. I. Fokin, 2015. New Paramecium (Ciliophora, Oligohymenophorea) congeners shape our view on its biodiversity. Organisms Diversity & Evolution 15: 215–233.CrossRefGoogle Scholar
  29. Long, H., W. Song, J. Gong, X. Hu, H. Ma, M. Zhu & M. Wang, 2005. Frontonia lynni n. sp., a new marine ciliate (Protozoa, Ciliophora, Hymenostomatida) from Qingdao, China. Zootaxa 1003: 57–64.CrossRefGoogle Scholar
  30. Long, H., W. Song, K. A. S. Al-Rasheid, Y. Wang, Z. Yi, S. A. Al-Quraishy, X. Lin & S. A. Al-Farraj, 2008. Taxonomic studies on three marine species of Frontonia from northern China: F. didieri n. sp., F. multinucleata n. sp. and F. tchibisovae Burkovsky, 1970 (Ciliophora: Peniculida). Zootaxa 1687: 35–50.Google Scholar
  31. Lynn, D. H., 2008. The Ciliated Protozoa. Characterization, Classification, and Guide to the Literature. Springer, Dordrecht.Google Scholar
  32. Ma, H., J. K. Choi & W. Song, 2003. An improved silver carbonate impregnation for marine ciliated protozoa. Acta Protozoologica 42: 161–164.Google Scholar
  33. Martin-Gonzaleaz, A., S. Serrano & D. Fernandez-Gallano, 1990. On the morphology, morphogenesis, and argyrome of Disematostoma buetschlii (Ciliophora, Frontoniidae). Canadian Journal of Zoology 68: 245–253.CrossRefGoogle Scholar
  34. Medlin, L., H. J. Elwood, S. Stickel & M. L. Sogin, 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71: 491–499.CrossRefPubMedGoogle Scholar
  35. Michiels, M. & N. Wilbert, 1973. Etude morphologique du cilié hyménostome péniculien Disematostoma minor Kahl, 1926. Protistologica 4: 455–458.Google Scholar
  36. Miller, M. A., W. Pfeiffer & T. Schwartz, 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop 14: 1–8.Google Scholar
  37. Nylander, J. A., 2004. MrModeltest v2. Uppsala University, Uppsala.Google Scholar
  38. Obolkina, L. A., 1995. Ciliophora. In Timoshkin, O. A. (ed.), Guide and Key to Pelagic Animals of Baikal with Ecological Notes. “Nauka” Siberian Publishing Firm RAS, Novosibirsk: 182–205.Google Scholar
  39. Packroff, G. & N. Wilbert, 1991. Taxonomische studien über die ciliatenfauna (Protozoa, Ciliophora) der Eifelmaare. Archiv Für Protistenkunde 140: 121–139.CrossRefGoogle Scholar
  40. Pan, X., W. Liu, Z. Yi, X. Fan, K. A. S. Al-Rasheid & X. Lin, 2013. Studies on three diverse Frontonia species (Ciliophora, Peniculida), with brief notes on 14 marine or brackish congeners. Acta Protozoologica 52: 35–49.Google Scholar
  41. Patterson, D. J., 1981. On the origin of the postoral microtubules of Paramecium putrinum (Hymenostomatida, Ciliophora). Protistologica 4: 525–531.Google Scholar
  42. Penn, O., E. Privman, H. Ashkenazy, G. Landan, D. Graur & T. Pupko, 2010a. GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Research 38: W23–W28.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Penn, O., E. Privman, G. Landan, D. Graur & T. Pupko, 2010b. An alignment confidence score capturing robustness to guide tree uncertainty. Molecular Biology and Evolution 27: 1759–1767.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Posada, D. & K. A. Crandall, 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818.CrossRefPubMedGoogle Scholar
  45. Ronquist, F. & J. P. Huelsenbeck, 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.CrossRefPubMedGoogle Scholar
  46. Serrano, S., A. Sola, A. Guinea & R. Gil, 1990. Morphology and morphogenesis of Disematostoma colpidioides (Ciliophora, Frontoniidae): its systematic implications. European Journal of Protistology 25: 353–360.CrossRefPubMedGoogle Scholar
  47. Serrano, S., R. Gil, A. Sola, L. Arregui & A. Guinea, 1994. Cytoskeletal organization of Disematostoma colpidioides (Ciliophora, Frontoniidae). Acta Protozoologica 33: 87–92.Google Scholar
  48. Small, E. B. & D. H. Lynn, 1985. Phylum Ciliophora, Doflein, 1901. In Lee, J. J., S. H. Hutner & E. C. Bovee (eds), An Illustrated Guide to the Protozoa. Society of Protozoologists, Lawrence: 393–575.Google Scholar
  49. Stamatakis, A., 2014. RAxML Version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Strüder-Kypke, M. C., A. D. Wright, S. I. Fokin & D. H. Lynn, 2000. Phylogenetic relationships of the subclass Peniculia (Oligohymenophorea, Ciliophora) inferred from small subunit rRNA gene sequences. Journal of Eukaryotic Microbiology 47: 419–429.CrossRefPubMedGoogle Scholar
  51. Suzuki, T. & C. Miyabe, 2007. Ecological balance between ciliate plankton and its prey candidates, pico- and nanoplankton, in the East China Sea. Hydrobiologia 586: 403–410.CrossRefGoogle Scholar
  52. Tarcz, S., 2013. Intraspecific differentiation of Paramecium novaurelia strains (Ciliophora, Protozoa) inferred from phylogenetic analysis of ribosomal and mitochondrial DNA variation. European Journal of Protistology 49: 50–61.CrossRefPubMedGoogle Scholar
  53. Tuffrau, M. & A. Savoie, 1961. Etude Morphologique du Cilié Hymenostome Disematostoma colpidioides von Gelei, 1954. The Journal of Protozoology. 8: 64–68.CrossRefGoogle Scholar
  54. Warren, A., D. J. Patterson, M. Dunthorn, J. C. Clamp, U. E. Achilles-Day, E. Aescht, S. A. Al-Farraj, S. Al-Quraishy, K. Al-Rasheid, M. Carr, J. G. Day, M. Dellinger, H. A. El-Serehy, Y. Fan, Y. Fan, Y. Fan, F. Gao, S. Gao, J. Gong, R. Gupta, X. Hu, K. Kamra, G. Langlois, X. Lin, D. Lipscomb, C. S. Lobban, P. Luporini, D. H. Lynn, D. H. Lynn, D. H. Lynn, H. Ma, M. Macek, J. Mackenzie-Dodds, S. Makhija, R. I. Mansergh, M. Martín-Cereceda, N. McMiller, D. J. S. Montagnes, S. Nikolaeva, G. O. Ong’ondo, B. Pérez-Uz, J. Purushothaman, P. Quintela-Alonso, J. Rotterová, L. Santoferrara, C. Shao, Z. Shen, X. Shi, W. Song, T. Stoeck, A. La Terza, A. Vallesi, M. Wang, T. Weisse, K. Wiackowski, L. Wu, K. Xu, Z. Yi, R. Zufall & S. Agatha, 2017. Beyond the “Code”: a guide to the description and documentation of biodiversity in Ciliated Protists (Alveolata, Ciliophora). Journal of Eukaryotic Microbiology. doi: 10.1111/jeu.12391.PubMedCentralGoogle Scholar
  55. Wichterman, R., 1986. The Biology of Paramecium. Plenum, New York.CrossRefGoogle Scholar
  56. Wiackowski, K. & W. Kocerba-Soroka, 2017. Selective predation by a harpacticoid copepod on ciliates in phytotelmata: a laboratory experiment. Hydrobiologia 790: 13–22.CrossRefGoogle Scholar
  57. Wilbert, N., 1972. Die Infraciliatur von Marituja pelagica Gajewskaja, 1928. The Journal of Protozoology 19: 590–592.CrossRefGoogle Scholar
  58. Wilbert, N., 1975. Eine verbesserte Technik der Protargolimprägnation für Ciliaten. Mikrokosmos 64: 171–179.Google Scholar
  59. Yildiz, I. & N. G. Senler, 2013. Frontonia anatolica n. sp. a new peniculid ciliate (Protista, Ciliophora) from Lake Van, Turkey. Turkish Journal of Zoology 37: 24–30.Google Scholar
  60. Zhao, Y., E. Gentekaki, Z. Yi & X. Lin, 2013. Genetic differentiation of the mitochondrial cytochrome oxidase c subunit I gene in genus Paramecium (Protista, Ciliophora). Plos ONE 8: e77044–e77044.CrossRefPubMedPubMedCentralGoogle Scholar
  61. Zhao, Y., Z. Yi, E. Gentekaki, A. Zhan, S. A. Al-Farraj & W. Song, 2016. Utility of combining morphological characters, nuclear and mitochondrial genes: an attempt to resolve the conflicts of species identification for ciliated protists. Molecular Phylogenetics and Evolution 94(Pt B): 718–729.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.State Key Laboratory of Estuarine and Coastal ResearchEast China Normal UniversityShanghaiChina
  2. 2.Institute of Evolution and Marine BiodiversityOcean University of ChinaQingdaoChina
  3. 3.School of Life SciencesEast China Normal UniversityShanghaiChina

Personalised recommendations