Skip to main content
SpringerLink
Log in

The Morphology and Phylogeny of Three Diophrys Ciliates Collected from the Subtropical Waters of China, Including a New Species (Ciliophora; Euplotia)

  • Published:
Journal of Ocean University of China Aims and scope Submit manuscript

Abstract

Three Diophrys species, D. quadrinucleata n. sp., D. oligothrix Borror, 1965 and D. scutum (Dujardin, 1841) Kahl, 1932, were identified from the subtropical brackish waters in China, their morphology was investigated using live observation and protargol impregnation. D. quadrinucleata n. sp. can be distinguished from the congeners by four ellipsoidal macronuclear nodules. Phylogenetic analyses show that the three species with single marginal cirrus are closely related, namely D. quadrinucleata n. sp., D. apoligothrix Song et al., 2009 and D. japonica Hu, 2008. Our population of D. oligothrix corresponds very well with previous populations in both living morphology and ciliature. However, the SSU rDNA sequences of three well-described populations differ from each other by 11 to 18 nucleotides, indicating that there might be cryptic species in D. oligothrix. Moreover, we provided a detailed description of the symbiotic bacteria/archaeobacteria (?) concentrated on the back surface of D. scutum based on the present population, which was either overlooked or misinterpreted as cortical granules previously.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Agamaliev, F. G., 1971. Complements to the fauna of psammophilic ciliates of the Western coast of the Caspian Sea. Acta Protozoologica, 8: 379–404 (in Russian with English summary).

    Google Scholar 

  • Borror, A. C., 1965a. Morphological comparison of Diophrys scutum (Dujardin, 1841) and Diophrys peloetes n. sp. (Hypotrichida, Ciliophora). Journal of Protozoology, 12: 60–66.

    Google Scholar 

  • Borror, A. C., 1965b. New and little-known tidal marsh ciliates. Transactions of the American Microscopical Society, 84: 550–565.

    Google Scholar 

  • Carey, P. G., 1992. Marine Interstitial Ciliates. An Illustrated Key. Chapman & Hall, London, 351pp.

    Google Scholar 

  • Chen, Z. G., and Song, W. B., 2002. Characterization and identification of the Diophrys species (Protozoa, Ciliophora, Hypotrichida) based on RAPD fingerprinting and ARDRA riboprinting. European Journal of Protistology, 38: 383–391.

    Google Scholar 

  • Curds, C. R., and Wu, I. C. H., 1983. A review of the Euplotidae (Hypotrichida, Ciliophora). Bulletin of the British Museum (NaturalHistory), 44: 191–247.

    Google Scholar 

  • Dujardin, F., 1841. Histoire naturelle des zoophytes. Infusoires, comprénant la physiologie et la classification de ces animaux, et la manière de les étudier al’aide du microscope. Libraire Encyclopédique de Roret, Paris.

    Google Scholar 

  • Edgar, R. C., 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32: 1792–1797.

    Google Scholar 

  • Fan, Y. B., Warren, A., Al-Rasheid, K. A. S., Chen, X., and Shao, C., 2013. Morphology and SSU rRNA gene-based phylogeny of two Diophrys-like ciliates from northern China, with notes on morphogenesis of Pseudodiophrys nigricans (Protozoa, Ciliophora). Journal of Morphology, 274: 395–403.

    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.

    Google Scholar 

  • Hill, B. F., and Borror, A. C., 1992. Redefinition of the genera Diophrys and Paradiophrys and establishment of the genus Diophryopsis n. g. (Ciliophora, Hypotrichida): Implication for the species problem. Journal of Protozoology, 39: 144–153.

    Google Scholar 

  • Hu, X. Z., 2008. Cortical structure in non-dividing and dividing Diophrys japonica spec. nov. (Ciliophora, Euplotida) with notes on morphological variation. European Journal of Protistology, 44: 115–129.

    Google Scholar 

  • Hu, X. Z., Huang, J., and Warren, A., 2012. The morphology and phylogeny of two euplotid ciliates, Diophrys blakeneyensis spec. nov. and Diophrys oligothrix Borror, 1965 (Protozoa, Ciliophora, Euplotida). International Journal of Systematic and Evolutionary Microbiology, 62: 2757–2773.

    Google Scholar 

  • Hu, X. Z., Lin, X. F., and Song, W. B., 2019. Ciliate Atlas: Species Found in the South China Sea. Science Press, Beijing, 936pp.

    Google Scholar 

  • Huang, J., Dunthorn, M., and Song, W. B., 2012. Expanding character sampling for the molecular phylogeny of euplotid ciliates (Protozoa, Ciliophora) using three markers, with a focus on the family Uronychiidae. Molecular Phylogenetics and Evolution, 63: 598–605.

    Google Scholar 

  • Jankowski, A. W., 1979. Revision of the order Hypotrichida Stein, 1859. Generic catalogue, phylogeny, taxonomy. Proceedings of the Academy of Sciences of the USSR, 86: 48–85.

    Google Scholar 

  • Jankowski, A. W., 2007. Phylum Ciliophora Doflein, 1901. In: Protista. Part 2. Handbook on Zoology. Alimov, A. F., ed., St. Petersburg, Nauka, 415–993.

    Google Scholar 

  • Jiang, J. M., and Song, W. B., 2010. Two new Diophrys-like genera and their type species, Apodiophrys ovalis n. g., n. sp. and Heterodiophrys zhui n. g., n. sp. (Ciliophora: Euplotida), with notes on their molecular phylogeny. Journal of Eukaryotic Microbiology, 57: 354–361.

    Google Scholar 

  • Jiang, J. M., Warren, A., and Song, W. B., 2011. Morphology and molecular phylogeny of two new marine euplotids, Pseudodiophrys nigricans n. g., n. sp., and Paradiophrys zhangi n. sp. (Ciliophora: Euplotida). Journal of Eukaryotic Microbiology, 58: 437–445.

    Google Scholar 

  • Kahl, A., 1932. Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria). 3. Spirotricha. Die Tierwelt Deutshlands und der Angrenzenden Meeresteile, 25: 399–650.

    Google Scholar 

  • Kattar, M. R., 1970. PtEstudo dos protozoarios ciliados psamofilos do litoral Brasileiro. Boletim de Zoologia e Biologia Marinha (Nova Serie), Sao Paulo, 27: 123–206.

    Google Scholar 

  • 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., Mentjies, P., and Drummond, A., 2012. Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28: 1647–1649.

    Google Scholar 

  • Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K., 2018. Mega X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35: 1547–1549.

    Google Scholar 

  • Lian, C. Y., Zhang, T. T., Al-Rasheid, K. A. S., Yu, Y. H., Jiang, J. M., and Huang, J., 2019. Morphology and SSU rDNA-based phylogeny of two Euplotes species from China: W. wuhanensis sp. n. and E. muscicola Kahl, 1932 (Ciliophora, Euplotida). European Journal of Protistology, 6: 1–14.

    Google Scholar 

  • Luo, X. T., Hu, X. Z., and Suzuki, T., 2014. Microscopic investigation of three species of Diophrys (Ciliophora, Euplotida, Uronychiidae) from Japan, including Diophrys peculiaris nov. spec. European Journal of Protistology, 50: 496–508.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Nylander, J. A. A., 2008. MrModeltest 2.3. Department of Systematic Zoology, Uppsala University, Uppsala, Sweden.

    Google Scholar 

  • Raikov, I. B., and Kovaleva, V. G., 1968. Complements to the fauna of psammobiotic ciliates of the Japan Sea (Posjet Gulf). Acta Protozoologica, 6: 309–333.

    Google Scholar 

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

    Google Scholar 

  • Ruinen, J., 1938. Notizen über Ciliaten aus konzentrierten Salzgewässern. Zoologische Mededelingen, 20: 243–256.

    Google Scholar 

  • Shen, Z., Yi, Z. Z., and Warren, A., 2011. The morphology, ontogeny, and small subunit rRNA gene sequence analysis of Diophrys parappendiculata n. sp, (Protozoa, Ciliophora, Euplotida), a new marine ciliate from coastal waters of southern China. Journal of Eukaryotic Microbiology, 58: 242–248.

    Google Scholar 

  • Sheng, Y. L., He, M., Zhao, F. Q., Shao, C., and Miao, M., 2018. Phylogenetic relationship analyses of complicated class Spirotrichea based on transcriptomes from three diverse microbial eukaryotes: Uroleptopsis citrina, Euplotes vannus and Protocruzia tuzeti. Molecular Phylogenetics and Evolution, 129: 338–345.

    Google Scholar 

  • Song, W. B., and Packroff, G., 1997. Taxonomische Untersuchungen an marinen Ciliaten aus China mit Beschreibungen von zwei neuen Arten, Strombidium globosaneum nov. spec. und S. platum nov. spec. (Protozoa, Ciliophora). Archiv Für Protistenkunde, 147: 331–360.

    Google Scholar 

  • Song, W. B., and Wilbert, N., 1994. Morphogenesis of the marine ciliate Diophrys oligothrix Borror, 1965 during the cell division (Protozoa, Ciliophora, Hypotrichida). European Journal of Protistology, 30: 38–44.

    Google Scholar 

  • Song, W. B., and Wilbert, N., 2002. Faunistic studies on marine ciliates from the Antarctic benthic area, including descriptions of one epizoic form, 6 new species and 2 new genera (Protozoa: Ciliophora). Acta Protozoologica, 41: 23–61.

    Google Scholar 

  • Song, W. B., Shao, C., Yi, Z. Z., Li, L. Q., Warren, A., Al-Rasheid, K. A. S., and Yang, J. P., 2009a. The morphology, morphogenesis and SSU rRNA gene sequence of a new marine ciliate, Diophrys apoligothrix spec. nov. (Ciliophora; Euplotida). European Journal of Protistology, 45: 38–50.

    Google Scholar 

  • Song, W. B., Warren, A., and Hu, X. Z., 2009b. Free-Living Ciliates in the Bohai and Yellow Seas, China. Science Press, Beijing, 518pp.

    Google Scholar 

  • Song, W. B., Wilbert, N., Al-Rasheid, K. A. S., Warren, A., Shao, C., Long, H. A., Yi, Z. Z., and Li, L. Q., 2007. Redescriptions of two marine hypotrichous ciliates, Diophrys irmgard and D. hystrix (Ciliophora, Euplotida), with a brief revision of the genus Diophrys. Journal of Eukaryotic Microbiology, 54: 283–296.

    Google Scholar 

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

    Google Scholar 

  • Wang, Y. R., Wang, C. D., Jiang, Y. H., Katz, L. A., Gao, F., and Yan, Y., 2019. Further analyses of variation of ribosome DNA copy number and polymorphism in ciliates provide insights relevant to studies of both molecular ecology and phylogeny. Science China Life Sciences, 62: 203–214.

    Google Scholar 

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

    Google Scholar 

  • Zhao, Y., Yi, Z. Z., Gentekaki, E., Zhan, A., Al-Farraj, S. A., and Song, W. B., 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: 718–729.

    Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 31970398), the National Key Research and Development Program of China (No. 2018YFD0900701), the Youth Innovation Promotion Association of the Chinese Academy of Sciences (No. 2019 333), the Technology Innovation Team of Ningbo City (No. 2015C110018), and the K. C. Wong Magna Fund in Ningbo University.

Author information

Author notes

  1. The two authors contributed equally to this work.

Authors and Affiliations

  1. School of Marine Sciences, Ningbo University, Ningbo, 315211, China

    Chaojian Zhang, Tingting Ye & Xiangrui Chen

  2. Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

    Jie Huang

  3. Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, 266003, China

    Borong Lu

  4. College of Fisheries, Ocean University of China, Qingdao, 266003, China

    Borong Lu

Authors
  1. Chaojian Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jie Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tingting Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Borong Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiangrui Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiangrui Chen.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, C., Huang, J., Ye, T. et al. The Morphology and Phylogeny of Three Diophrys Ciliates Collected from the Subtropical Waters of China, Including a New Species (Ciliophora; Euplotia). J. Ocean Univ. China 19, 975–987 (2020). https://doi.org/10.1007/s11802-020-4536-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11802-020-4536-8

Key words

Search

Navigation