Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2020-02-13
Page range: 435–452
Abstract views: 137
PDF downloaded: 4

Morphological Redescriptions and Molecular Phylogeny of Three Stentor Species (Ciliophora: Heterotrichea: Stentoridae) from Korea

Department of Biological Science, University of Ulsan, Ulsan, 44610, South Korea
Department of Biological Science, University of Ulsan, Ulsan, 44610, South Korea
Department of Biological Science, University of Ulsan, Ulsan, 44610, South Korea
Department of Biological Science, University of Ulsan, Ulsan, 44610, South Korea
Department of Biological Science, University of Ulsan, Ulsan, 44610, South Korea
Protist Stentorids Heterotrichea SSU rRNA Freshwater Korea

Abstract

The morphologies of the three freshwater stentorid ciliates in Korea, Stentor coeruleus (Pallas, 1766); Stentor muelleri Ehrenberg, 1831, and Stentor tartari Murthy & Bai, 1974, were investigated based on live observations and protargol impregnation. The Korean population of S. tartari exhibits the following characteristics: body size 200–355 × 85–135 µm in vivo, 62–106 somatic kineties, 8–13 peristomial kineties, 110–180 adoral membranelles, mostly two macronuclear nodules and 5–18 micronuclei, reddish and colorless cortical granules and the presence of symbiotic algae. We identified S. tartari based on unique characteristics compared to close congeners. Korean populations of S. coeruleus and S. muelleri are congruent with previously described populations in most aspects of their morphologies. Here, for the first time, we report molecular gene sequence information for S. tartari. Small subunit (SSU) rRNA gene sequence-based phylogeny indicates that S. tartari, which has multiple macronuclei, forms a monophyletic group with other Stentor species having a single macronucleus. Our findings based on morphology and SSU rRNA gene sequence information corroborate the hypothesis that the elongated macronucleus evolved from the compact single or multi macronucleus state.

 

References

  1. Balbiani, E.G. (1889) Recherches experimentales sur la merotomie des infusoires cilies. Contribution a I’etude du role du noyau cellulaire. Recueil Zoologique Suisse, 5, 1–72.

    Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540–552.

    https://doi.org/10.1093/oxfordjournals.molbev.a026334

    Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.

    https://doi.org/10.1038/nmeth.2109

    Dragesco, J. (1970) Ciliés libres du Cameroun. Annales de la faculteì des sciences de Yaoundeì, Numéro Hors Série, 1–141.

    Ehrenberg, C.G. (1831) Uber die Entwickelung und Lebensdauer der Infusionsthiere; nebst ferneren Beiträgen zu einer Vergleichung ihrer organischen Systeme. Physikalische Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin, 1831, l–154.

    Ehrenberg, C.G. (1838) Die Infusionsthierchen als vollkommene Organismen. Ein Blick in das tiefere organische Leben der Nalur. Verlag von Leopold Voss, Leipzig, 548 pp.

    https://doi.org/10.5962/bhl.title.58475

    Fernandes, N.M., da Silva Neto, I.D. & Schrago, C.G. (2014) Morphology and phylogenetic position of an unusual Stentor polymorphus (Ciliophora: Heterotrichea) without symbiotic algae. Journal of Eukaryotic Microbiology, 61, 305–312.

    https://doi.org/10.1111/jeu.12108

    Fernandes, N.M., da Silva Paiva, T., da Silva-Neto, I.D., Schlegel, M. & Schrago, C.G. (2016) Expanded phylogenetic analyses of the class Heterotrichea (Ciliophora, Postciliodesmatophora) using five molecular markers and morphological data. Molecular Phylogenetics and Evolution, 95, 229–246.

    https://doi.org/10.1016/j.ympev.2015.10.030

    Foissner, W. (1980) Taxonomische Studien über die Ciliaten des Großglocknergebietes (Hohe Tauern, Osterreich). IX. Ordnungen Heterotrichida und Hypotrichida. Berichte der Naturwissenschaftlich-Medizinischen Vereinigung, Salzburg, 111 pp. [pp. 7–117]

    Foissner, W. & Wölfl, S. (1994) Revision of the genus Stentor Oken (Protozoa, Ciliophora) and description of S. araucanus nov. spec, from South American lakes. Journal of Plankton Research, 16, 255–289.

    https://doi.org/10.1093/plankt/16.3.255

    Foissner, W., Berger, H. & Kohmann, F. (1992) Taxonomische und ökologische Revision der Ciliaten des Saprobiesystems. Band II. Peritrichia, Heterotrichida, Odontostomatida. Informationsberichte des Bayer. Landesamtes für Wasserwirtschaft, München, 502 pp.

    Gajewskaja, N. (1933) Zur Oekologie. Morphologie und Systematik der Infusorien des Baikalsees. Zoologica, Stuttgart, 32, 1–29.

    Gong, Y., Yu, Y., Zhu, F. & Feng, W. (2007) Molecular phylogeny of Stentor (Ciliophora: Heterotrichea) based on small subunit ribosomal RNA sequences. Journal of Eukaryotic Microbiology, 54, 45–48.

    https://doi.org/10.1111/j.1550-7408.2006.00147.x

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

    https://doi.org/10.1080/10635150390235520

    Izquierdo-Carrasco, F., Smith, S.A. & Stamatakis, A. (2011) Algorithms, data structures, and numerics for likelihood-based phylogenetic inference of huge trees. BMC Bioinformatics, 12, 470.

    https://doi.org/10.1186/1471-2105-12-470

    Johnson, H.P. (1893) A contribution to the morphology and biology of the Stentors. Journal of Morphology, 8, 468–552.

    https://doi.org/10.1002/jmor.1050080303

    Kahl, A. (1932) Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria) 3. Spirotricha. Tierwelt Deutschlands, 25, 399–650.

    Kamra, K. & Sapra, G.R. (1990) Partial retention of parental ciliature during morphogenesis of the ciliate Coniculostomum monilata (Dragesco and Njiné, 1971) Njiné, 1978 (Oxytrichidae, Hypotrichida). European Journal of Protistology, 25, 264–278.

    https://doi.org/10.1016/S0932-4739(11)80179-3

    Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.

    https://doi.org/10.1093/bioinformatics/bts199

    Kumazawa, H. (1974) Two species of the genus Stentor (Ciliata). Journal of Science of the Hiroshima University, 25, 147–154.

    Kumazawa, H. (2002) Notes on the taxonomy of Stentor Oken (Protozoa, Ciliophora) and a description of a new species. Journal of Plankton Research, 24, 69–75.

    https://doi.org/10.1093/plankt/24.1.69

    Leibmann, H. (1962) Handbuch der Frischwasser- und Abwasser- Biologie. Band I. Biologie des Trinkwassers, Badewassers, Fischwassers, Vorfluters und Abwassers. R. Oldenbourg, München, 588 pp.

    Li, L., Huang, J., Song, W., Shin, M.K., AL-Rasheid, K.A.S. & Berger, H. (2010) Apogastrostyla rigescens (Kahl, 1932) gen. nov., comb. nov. (Ciliophora, Hypotricha): morphology, notes on cell division, SSU rRNA gene sequence data, and neotypification. Acta Protozoologica, 49, 195–212.

    Lynn, D.H. (2008) The ciliated protozoa characterization, classification, and guide to the literature. Springer, Dordrecht, 605 pp.

    https://doi.org/10.1007/978-1-4020-8239-9

    Maskell, W.M. (1886) On the freshwater infusoria of the Wellington district, Transactions and Proceedings of the Royal Society of New Zealand, 19, 49–61.

    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.

    https://doi.org/10.1016/0378-1119(88)90066-2

    Murthy, K.V.N. & Bai, A.R.K. (1974) Stentor tartari sp. n. from India. The Journal of Protozoology, 21, 505–506.

    https://doi.org/10.1111/j.1550-7408.1974.tb03687.x

    Nilsson, J.R. (1986) The African heterotrich ciliate, Stentor andreseni sp. nov., and S. amethystinus Leidy. Biologiske Skrifter, 27, 5–43.

    Pallas, P.S. (1766) Elenchus Zoophytorum. Petrum van Cleef, Hagae-Comitum, 451 pp.

    Posada, D. (2008) JModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.

    https://doi.org/10.1093/molbev/msn083

    Posada, D. & Buckley, T.R. (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology, 53, 793–808.

    https://doi.org/10.1080/10635150490522304

    Price, M.N., Dehal, P.S. & Arkin, A.P. (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS One, 5, e9490. https://doi.org/10.1371/journal.pone.0009490

    Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.

    https://doi.org/10.1093/sysbio/sys029

    Roux, J. (1901) Faune infusorienne des eaux stagnantes des environs de Genève. Meìmoire Couronneì du Prix Davy par la Faculteì des Sciences de L’Universiteì de Geneìve, 19, 1–149.

    Schmidt, S.L., Foissner, W., Schlegel, M. & Bernhard, D. (2007) Mo­lecular phylogeny of the Heterotrichea (Ciliophora, Postcil­iodesmatophora) based on small subunit rRNA gene sequences. Journal of Eukaryotic Microbiology, 54, 358–363.

    https://doi.org/10.1111/j.1550-7408.2007.00269.x

    Shazib, S.U.A., Vďačný, P., Kim, J.H., Jang, S.W. & Shin, M.K. (2014) Phylogenetic relationships of the ciliate class Heterotrichea (Protista, Ciliophora, Postciliodesmatophora) inferred from multiple molecular markers and multifaceted analysis strategy. Molecular Phylogenetics and Evolution, 78, 118–135.

    https://doi.org/10.1016/j.ympev.2014.05.012

    Song, W. & Wilbert, N. (1989) Taxonomische Untersuchungen an Aufwuchsciliaten (Protozoa, Ciliophora) im Poppelsdorfer Weiher, Bonn. Lauterbornia, 3, 2–221.

    Stamatakis, A. (2006) Phylogenetic models of rate heterogeneity: a high-performance computing perspective. In: Proceedings 20th IEEE International Parallel & Distributed Processing Symposium, 2006, 1–8.

    https://doi.org/10.1109/IPDPS.2006.1639535

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

    https://doi.org/10.1093/bioinformatics/btu033

    Stein, F. (1867) Der Organismus der Infusionsthiere nach eigenen Forschungen in systematischer Reihenfolge bearbeiteit. II. Abtheilung, 1) Darstellung der neueusten Forschungsergebnisse über Bau, Fortpflanzung und Entwickelung der Infusionsthiere, 2) Naturgeschichte der heterotrichen Infusorien. W. Engelmann, Leipzig, 355 pp.

    Swarczewsky, B. (1929) Zur Kenntnis der Baikalprotistenfauna. Die an den Baikalgammariden lebenden Infusorien. VI. Stentorina. Archiv für Protistenkunde, 65, 38–44.

    Talavera, G. & Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology, 56, 564–577.

    https://doi.org/10.1080/10635150701472164

    Tartar, V. (1958) Stentor introversus. n. sp. The Journal of Protozoolology, 5, 93–95.

    https://doi.org/10.1111/j.1550-7408.1958.tb02533.x

    Tartar, V. (1961) The biology of Stentor. Pergamon Press, Oxford, 413 pp.

    https://doi.org/10.5962/bhl.title.7444

    Thamm, M., Schmidt, S.L. & Bernhard, D. (2010) Insights into the phylogeny of the genus Stentor (Heterotrichea, Ciliophora) with special emphasis on the evolution of the macronucleus based on SSU rDNA data. Acta Protozoologica, 49, 149–157.

    Tuffrau, M. (1968) Les structures fibrillaires somatiques et buccales chez les cilits hCt6rotriches. Protistologica, 3 (1967), 369–394.

    Villeneuve-Brachon, S. (1940) Recherches sur les cilies heterotriches. Cinetome, argyrome, myonemes. Formes nouvelles ou peu connues. Archives de zoologie expérimentale et générale, 82, 180.

    Vuxanovici, A. (1961) Cercetari asupra unor infuzori dulcicoli din lacurile regiunii Bucuresti (Recherches sur les infusoires d’eau douce de la région de Bucarest). Studii Cerc. Biol., Seria “biologie animala”, 13, 431–443. [in Rumanian with Russian and French summary]

    Wilbert, N. (1975) Eine verbesserte Technik der protargolimprägnation für Ciliatenm. Mikrokosmos, 64, 171–179.