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Morphological Studies on Four Brackish Water Ciliates of the Class Spirotrichea (Protista, Ciliophora)

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Abstract

We reinvestigate the morphology of two oligotrich and two hypotrich ciliates collected from the coasts of north and south China, viz., Parallelostrombidium obesum Liu et al., 2015, Spirostrombidium apourceolare Liu et al., 2013, Protogastrostyla pulchra (Pereyaslawzewa, 1886) Gong et al., 2007, and Uncinata bradburyae (Gong et al., 2001) Luo et al., 2015. All the populations match well with the original samples identified in previous studies. Supplemental taxonomic data were supplied for these four species of the new populations. The species Parallelostrombidium obesum is characterised by its dorsal-ventrally flattened body shape with anterior and posterior ends transversely truncating, as well as two thigmotactic membranelles and girdle kinety that spirals around the cell one and a half times. Spirostrombidium apourceolare is characterised by its elongate ellipsoidal and dorsal-ventrally flattened body shape, two thigmotactic membranelles, about 11–27 ovoid macronuclear nodules, and girdle kinety that spirals around the cell twice with two undulations. Protogastrostyla pulchra is characterised by its elongate body shape and unique, caudally located food vacuole. Based on the new populations, we described the smaller cortical granules, clustered around dorsal bristles for the first time. The new population of Uncinata bradburyae shares the diagnostic features with the type population, which include prominent beak-like projection in anterior region, the conspicuous gap of adoral zone, proximalmost adoral membranelles distinctly elongated, and infraciliature.

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References

  • Agatha, S., 2004. Evolution of ciliary patterns in the Oligotri-chida (Ciliophora, Spirotricha) and its taxonomic implications. Zoology, 107: 153–168.

    Article  Google Scholar 

  • Agatha, S., 2011. Updated hypothesis on the evolution of oligo-trichid ciliates (Ciliophora, Spirotricha, Oligotrichida) based on somatic ciliary patterns and ontogenetic data@@@. European Journal of Protistology, 47: 51–56.

    Article  Google Scholar 

  • Agatha, S., and Riedel-Lorjé, J. C., 2006. Redescription of Tin-tinnopsis cylindrica Dada., 1887 (Ciliophora: Spirotricha) and unification of tintinnid terminology. Acta Protozoologica, 45: 137–151.

    Google Scholar 

  • Berger, H., 1999. Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Monographiae Biologicae, 78: 1–1080.

    Article  Google Scholar 

  • Berger, H., 2006. Monograph of the Urostyloidea (Ciliophora, Hypotricha). Monographiae Biologicae, 85: 1–1304.

    Article  Google Scholar 

  • Berger, H., 2008. Monograph of the Amphisiellidae and Trachelostylidae (Ciliophora, Hypotrichida). Monographiae Biologicae, 88: 1–737.

    Google Scholar 

  • Berger, H., 2011. Monograph of the Gonostomatidae and Kahliellidae (Ciliophora, Hypotrichida). Monographiae Biologicae, 90: 1–741.

    Article  Google Scholar 

  • Borror, A. C., 1963. Morphology and ecology of the benthic ciliated protozoa of Alligator Harbor, Florida. Archiv für Protistenkunde, 106: 465–534.

    Google Scholar 

  • Burkovsky, I. V., 1970. The ciliates of the mesopsammon of the Kandolaksha Gulf (White Sea) II. Acta Protozoologica, 8: 47–64.

    Google Scholar 

  • Caron, D. A., Countway, P. D., Jones, A. C., Kim, D. Y., and Schnetzer, A., 2012. Marine protistan diversity. Annual Review of Marine Science, 4: 467–493.

    Article  Google Scholar 

  • Chen, L. Y., Liu, W. W., Liu, A., Al-Rasheid, K. A. S., and Shao, C., 2013. Morphology and molecular phylogeny of a new marine hypotrichous ciliate, Hypotrichidium paraconicum n. sp. (Ciliophora, Hypotrichia). Journal of Eukaryotic Microbiology, 60: 588–600.

    Article  Google Scholar 

  • Chen, L. Y., Zhao, X. L., Shao, C., Miao, M., and Clamp, J., 2017a. Morphology and phylogeny of two new ciliates, Sterkiella sinica sp. nov. and Rubrioxytricha tsinlingensis sp. nov. (Protozoa, Ciliophora, Hypotrichia) from north-west China. Systematics and Biodiversity, 15: 131–142.

    Article  Google Scholar 

  • Chen, X. M., Dong, J., Lin, X. F., and Al-Rasheid, K. A. S., 2011. Morphology and phylogeny of a new urostylid ciliate, Monocoronella carnea n. gen., n. sp. (Ciliophora, Hypotricha) from Daya Bay, southern China. Journal of Eukaryotic Microbiology, 58: 497–503.

    Article  Google Scholar 

  • Chen, X. M., Gao, F., Al-Farraj, S. A., Al-Rasheid, K. A. S., Xu, K. D., and Song, W. B., 2015. Morphology and morphogenesis of a novel mangrove ciliate, Sterkiella subtropica sp. nov. (Protozoa, Ciliophora, Hypotrichia), with phylogenetic analyses based on small-subunit rDNA sequence data. International Journal of Systematic and Evolutionary Microbiology, 65: 2292–2303.

    Article  Google Scholar 

  • Chen, X. M., Lu, X. T., Luo, X. T., Jiang, J. M., Shao, C., Al-Rasheid, K. A. S., Warren, A., and Song, W. B., 2017b. The diverse morphogenetic patterns in spirotrichs and philasterids: Researches based on five-year-projects supported by IRCN-BC and NSFC. European Journal of Protistology, 61: 439–452.

    Article  Google Scholar 

  • Dong, J. Y., Lu, X. T., Shao, C., Huang, J. A., and Al-Rasheid, K. A. S., 2016. Morphology, morphogenesis and molecular phylogeny of a novel saline soil ciliate, Lamtostyla salina n. sp. (Ciliophora, Stichotrichida). European Journal of Protistology, 56: 219–231.

    Article  Google Scholar 

  • Foissner, W., 2016. Terrestrial and semiterrestrial ciliates (Protozoa, Ciliophora) from Venezuela and Galápagos. Denisia, 35: 1–912.

    Google Scholar 

  • Gao, F., Huang, J., 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., and Song, W. B., 2017. Systematic studies on ciliates (Alveolata, Ciliophora) in China: Progress and achievements based on molecular information. European Journal of Protistology, 61: 409–423.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gong, J., Kim, S. J., Kim, S. Y., Min, G. S., Roberts, D. M., Warren, A., and Choi, J. K., 2007. Taxonomic redescriptions of two ciliates, Protogastrostyla pulchra n. g., n. comb. and Hemigastrostyla enigmatica (Ciliophora: Spirotrichea, Sti-chotrichia), with phylogenetic analyses based on 18S and 28S rRNA gene sequences. Journal of Eukaryotic Microbiology, 54: 468–478.

    Google Scholar 

  • Gong, J., Song, W. B., Hu, X. Z., Ma, H. G., and Zhu, M. Z., 2001. Morphology and infraciliature of Holosticha bradbur-yae n. sp. (Ciliophora, Hypotrichida) from the Yellow Sea, China. Hydrobiologia, 464: 63–69.

    Article  Google Scholar 

  • Hu, X. Z., and Song, W. B., 2000. Morphology and morphogenesis of a marine ciliate, Gastrostyla pulchra (Perejaslawzew., 1885) Kah., 1932 (Ciliophora, Hypotrichida). European Journal of Protistology, 36: 201–210.

    Article  Google Scholar 

  • Huang, J. B., Zhang, T. T., Zhang, Q. Q., Li, Y., Warren, A., Pan, H. B., and Yan, Y., 2018. Further insights into the highly derived haptorids (Ciliophora, Litostomatea): Phylogeny based on multigene data. Zoologica Scripta, 47: 231–242.

    Article  Google Scholar 

  • Kahl, A., 1932. Urtiere oder Protozoa I: Wimpertiere oder Cili-ata (Infusoria). Tierwelt Deutschlands, 25: 399–650.

    Google Scholar 

  • Krainer, K. H., 1991. Contributions to the morphology, infraciliature and ecology of the planktonic ciliates Strombidium pelagicum n. sp., Pelagostrombidium mirabile (Penar., 1916) n. g., n. comb., and Pelagostrombidium fallax (Zacharia., 1896) n. g., n. comb. (Ciliophora, Oligotrichida). European Journal of Protistology, 27: 60–70.

    Article  Google Scholar 

  • Kumar, S., Bharti, D., Shazib, S. U. A., and Shin, M. K., 2017. Discovery of a new hypotrich ciliate from petroleum contaminated soil. PLoS One, 12: e0178657.

    Article  Google Scholar 

  • Kumar, S., Kamra, K., Bharti, D., Terza, A. L., Sehgal, N., Warren, A., and Sapra, G. R., 2015. Morphology, morphogenesis, and molecular phylogeny of Sterkiella tetracirrata n. sp. (Ciliophora, Oxytrichidae), from the Silent Valley National Park, India. European Journal of Protistology, 51: 86–97.

    Article  Google Scholar 

  • Liu, W., Yi, Z., Li, J., Warren, A., Al-Farraj, S. A., and Lin, X., 2013. Taxonomy, morphology and phylogeny of three new oligotrich ciliates (Protozoa, Ciliophora, Oligotrichia) from southern China. International Journal of Systematic and Evolutionary Microbiology, 63: 4805–4817.

    Article  Google Scholar 

  • Liu, W., Yi, Z., Lin, X., and Al-Rasheid, K. A. S., 2011a. Morphologic and molecular data suggest that Lynnella semiglobulosa n. g., n. sp. represents a new family within the subclass Choreotrichia (Ciliophora, Spirotrichea). Journal of Eu-karyotic Microbiology, 58: 43–49.

    Article  Google Scholar 

  • Liu, W., Yi, Z., Warren, A., Al-Rasheid, K. A. S., Al-Farraj, S. A., Lin, X., and Song, W. B., 2011b. Taxonomy, morphology and molecular systematics of a new oligotrich ciliate, Williophrya maedai gen. nov., sp. nov., with redescriptions of Strombidium basimorphum and Pseudotontonia simplicidens (Protozoa, Ciliophora, Oligotrichia). Systematics and Biodiversity, 9: 247–258.

    Article  Google Scholar 

  • Liu, W. W., Jiang, J. M., Xu, Y., Pan, X. M., Qu, Z. S., Luo, X. T., El-Serehy, H. A., Warren, A., Ma, H. G., and Pan, H. B., 2017. Diversity of free-living marine ciliates (Alveolata, Ciliophora): Faunal studies in coastal waters of China during the years 2011–2016. European Journal of Protistology, 61: 424–438.

    Article  Google Scholar 

  • Liu, W. W., Yi, Z. Z., Lin, X. F., Li, J. Q., Al-Farraj, S. A., Al-Rasheid, K. A. S., and Song, W. B., 2015. Morphology and molecular phylogeny of three new oligotrich ciliates (Protozoa, Ciliophora) from the South China Sea. Zoological Journal of the Linnean Society, 174: 653–665.

    Article  Google Scholar 

  • Lu, X. T., Huang, J. A., Shao, C., Al-Farraj, S. A., and 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. Journal of Eukaryotic Microbiology, 64: 632–646.

    Article  Google Scholar 

  • Luo, X. T., Gao, F., Al-Rasheid, K. A. S., Warren, A., Hu, X. Z., and Song, W. B., 2015. Redefinition of the hypotrichous ciliate Uncinata, with descriptions of the morphology and phylogeny of three urostylids (Protista, Ciliophora). Systematics and Biodiversity, 13: 455–471.

    Article  Google Scholar 

  • Luo, X. T., Gao, F., Yi, Z. Z., Pan, Y., Al-Farraj, S. A., and Warren, A., 2017. Taxonomy and molecular phylogeny of two new brackish hypotrichous ciliates, with the establishment of a new genus (Protozoa, Ciliophora). Zoological Journal of the Linnean Society, 179: 475–491.

    Google Scholar 

  • Lynn, D. H., 2008. The Ciliated Protozoa: Characterization, Classification, and Guide to the Literature. 3rd edition. Springer, Dordrecht, 605pp.

    Google Scholar 

  • Lynn, D. H., and Gilron, G. L., 1993. Strombidiid ciliates from coastal waters near Kingston Harbor, Jamaica (Ciliophora, Oligotrichia, Strombidiidae). Journal of the Marine Biological Association of the United Kingdom, 73: 47–65.

    Article  Google Scholar 

  • Paiva, T. S., Shao, C., Fernandes, N. M., Borges, B. N., and Silva-Neto, I. D., 2016. Description and phylogeny of Urostyla grandis wiackowskii subsp. nov. (Ciliophora, Hypotricha) from an estuarine mangrove in Brazil. Journal of Eukaryotic Microbiology, 63: 247–261.

    Article  Google Scholar 

  • Pan, X. M., Bourland, W. A., and Song, W. B., 2013. Protargol synthesis: An in-house protocol. Journal of Eukaryotic Microbiology, 60: 609–614.

    Article  Google Scholar 

  • Pan, X. M., Fan, Y. B., Gao, F., Qiu, Z. J., Al-Farraj, S. A., Warren, A., and Shao, C., 2016. Morphology and systematics of two freshwater urostylid ciliates, with description of a new species (Protista, Ciliophora, Hypotrichia). European Journal of Protistology, 52: 73–84.

    Article  Google Scholar 

  • Park, K. M., Jung, J. H., Min, G. S., and Kim, S., 2017. Pseudonotohymena antarctica n. g., n. sp. (Ciliophora, Hypotricha), a new species from Antarctic soil. Journal of Eukaryotic Microbiology, 64: 447–456.

    Article  Google Scholar 

  • Pereyaslawzewa, S., 1886. Protozoaires de la mer Noire. Zap novoross Obshch Estest, 10: 79–114 (in Russian).

    Google Scholar 

  • Petz, W., Song, W. B., and Wilbert, N., 1995. Taxonomy and ecology of the ciliate fauna (Protozoa, Ciliophora) in the endopagial and pelagial of the Weddell Sea, Antarctica. Stap-fia, 40: 1–223.

    Google Scholar 

  • Pierce, R. W., and Turner, J. T., 1992. Ecology of planktonic ciliates in marine food webs. Reviews in Aquatic Sciences, 6: 139–181.

    Google Scholar 

  • Shao, C., Li, L. Q., Zhang, Q. Q., Song, W. B., and Berger, H., 2014. Molecular phylogeny and ontogeny of a new ciliate genus, Paracladotricha salina n. g., n. sp. (Ciliophora, Hypotrichia). Journal of Eukaryotic Microbiology, 61: 371–380.

    Article  Google Scholar 

  • Song, W., Li, J. M., Liu, W. W., Al-Rasheid, K. A. S., Hu, X. Z., and Lin, X. F., 2015a. Taxonomy and molecular phylogeny of four Strombidium species, including description of S. pseudostylifer sp. nov. (Ciliophora, Oligotrichia). Systematics and Biodiversity, 13: 76–92.

    Article  Google Scholar 

  • Song, W., Li, J. M., Hu, X. Z., Liu, W. W., Al-Rasheid, K. A. S., and Miao, M., 2018a. Morphology and phylogeny of three oligotrichous ciliates (s.l.), including description of a new species Parastrombidinopsis zhuhaiensis sp. n. (Ciliophora, Choreotrichia). Acta Protozoologica (in press).

    Google Scholar 

  • Song, W., Wang, L., Li, L., Al-Farraj, S. A., Aleidan, A., Smith, S., and Hu, X., 2018b. Morphological characterizations of four species of Parallelostrombidium (Ciliophora, Oligotrichia), with a note on the phylogeny of the genus. Journal of Eukaryotic Microbiology, 65: 679–693.

    Article  Google Scholar 

  • Song, W., Zhao, X. L., Liu, W. W., Hu, X. Z., Al-Farraj, S. A., Al-Rasheid, K. A. S., Song, W. B., and Warren, A., 2015b. Biodiversity of oligotrich ciliates in the South China Sea: Description of three new Strombidium species (Protozoa, Ciliophora, Oligotrichia) with phylogenetic analyses. Systematics and Biodiversity, 13: 928–943.

    Google Scholar 

  • Song, W. B., and Bradbury, P. C., 1998. Studies on some new and rare reported marine planktonic ciliates (Ciliophora: Oligotrichida) from coastal waters in North China. Journal of the Marine Biological Association of the United Kingdom, 78: 767–794.

    Article  Google Scholar 

  • Wang, J. Y., Lyu, Z., Warren, A., Wang, F., and Shao, C., 2016. Morphology, ontogeny and molecular phylogeny of a novel saline soil ciliate, Urosomoida paragiliformis n. sp. (Ciliophora, Hypotrichia). European Journal of Protistology, 56: 79–89.

    Article  Google Scholar 

  • Wang, J. Y., Ma, J. Y., Qi, S. Y., and Shao, C., 2017. Morphology, morphogenesis and molecular phylogeny of a new soil ciliate Paragonostomoides xianicum n. sp. (Ciliophora, Hypotrichia, Gonostomatidae). European Journal of Protistology, 61: 233–243.

    Article  Google Scholar 

  • Wang, R., Song, W., Yi, Z. Z., Lin, X. F., AL-Rasheid, K. A. S., and Hu, X. Z., 2018. Morphology and molecular phylogeny of two new species of Spirostrombidium (Ciliophora, Oligotrichia), with a key to species in the genus. Systematics and Biodiversity, 16: 743–756.

    Article  Google Scholar 

  • Wilbert, N., 1975. Eine verbesserte Technik der Protargolimprägnation für Ciliaten. Mikrokosmos, 64: 171–179.

    Google Scholar 

  • Worden, A. Z., Follows, M. J., Giovannoni, S. J., Wilken, S., Zimmerman, A. E., and Keeling, P. J., 2015. Rethinking the marine carbon cycle: Factoring in the multifarious lifestyles of microbes. Science, 347: 1257594.

    Article  Google Scholar 

  • Xu, D. P., Warren, A., and Song, W. B., 2009. Oligotrichs. In: Free-Living Ciliates in the Bohai and Yellow Seas, China. Song, W. B., et al., eds., Science Press, Beijing, 307–351.

    Google Scholar 

  • Xu, D. P., Jiao, N. Z., Ren, R., and Warren, A., 2017. Distribution and diversity of microbial eukaryotes in bathypelagic waters of the South China Sea. Journal of Eukaryotic Microbiology, 64: 370–382.

    Article  Google Scholar 

  • Yan, Y., Rogers, A. J., Gao, F., and Katz, L. A., 2017. Unusual features of non-dividing somatic macronuclei in the ciliate class Karyorelictea. European Journal of Protistology, 61: 399–408.

    Article  Google Scholar 

  • Zhang, Q. Q., Agatha, S., Zhang, W. C., Dong, J., Yu, Y., Jiao, N. Z., and Gong, J., 2017. Three rDNA loci-based phylogenies of tintinnid ciliates (Ciliophora, Spirotrichea, Choreotrichida). Journal of Eukaryotic Microbiology, 64: 226–241.

    Article  Google Scholar 

  • Zhao, X. L., Wang, Y. Y., Wang, Y. R., Liu, Y. F., and Gao, S., 2017. Histone methyltransferase TXR1 is required for both H3 and H3.3 lysine 27 methylation in the well-known ciliated protist Tetrahymena thermophila. Science China Life Sciences, 60: 264–270.

    Article  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (Nos. 31801955, 31702009) and the China Postdoctoral Science Foundation (Nos. 2017M622276, BX20180348)

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Song, Y., Liu, Y., Pan, B. et al. Morphological Studies on Four Brackish Water Ciliates of the Class Spirotrichea (Protista, Ciliophora). J. Ocean Univ. China 18, 663–674 (2019). https://doi.org/10.1007/s11802-019-4096-y

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