Skip to main content
SpringerLink
Log in

Taxonomic Clarification of A Well-Known Pathogenic Scuticociliate, Miamiensis avidus Thompson & Moewus, 1964 (Ciliophora, Scuticociliatia)

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

Abstract

Miamiensis avidus Thompson & Moewus, 1964, is a cosmopolitan and well-known marine pathogenic ciliated protist. However, the taxonomy of this species up to now has remained controversial, especially with respect to the validity of the morphologically similar species, Philasterides dicentrarchi, which was considered as a junior synonym of M. avidus. In this study, a population of M. avidus was collected from the skin of pharaoh cuttlefish (Sepia pharaonis) cultured near the East China Sea, Ningbo, China and its morphology and phylogeny were investigated in detail based on living characters, infraciliature, small subunit (SSU) rDNA and ITS1-5.8S-ITS2 region sequences. In addition, the morphometrics of a previously reported free-living population, collected from the Bohai Sea, were rechecked and analyzed. We compared the present two isolates with all historic populations of M. avidus and P. dicentrarchi, and found that their morphological characters were either highly similar or exactly identical, indicating that they are the same morphospecies. However, the phylogenetic analyses based on SSU rDNA or ITS1-5.8S-ITS2 region sequences revealed that most M. avidus and P. dicentrarchi populations formed one clade, and the two isolates of M. avidus from Weifang and American Type Culture Collection clustered in another clade, which indicated that there might be cryptic species in Miamiensis avidus.

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

  • Buchmann, K., 2015. Impact and control of protozoan parasites in maricultured fishes. Parasitology, 142: 168–177.

    Article  Google Scholar 

  • Budino, B., Lamas, J., Pata, M. P., Arranz, J. A., Sanmartín, M. L., and 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.

    Article  Google Scholar 

  • Corliss, J. O., 1979. The Ciliated Protozoa: Characterization, Classification, and Guide to the Literature. Pergamon Press, Oxford, 261–262.

    Google Scholar 

  • Dragesco, A., Dragesco, J., Coste, F., Gasc, C., Romestand, B., Raymond, J. C., and Bouix, G. 1995. Philasterides dicentrarchi, n. sp., (Ciliophora, Scuticociliatida), a histophagous opportunistic parasite of Dicentrarchus labrax (Linnaeus, 1758), a reared marine fish. European Journal of Protistology, 31: 327–340.

    Article  Google Scholar 

  • Fan, X. P., Chen, X. R., Song, W. B., Al-Rasheid, K. A. S., and Warren, A., 2010. Two new marine scuticociliates, Sathrophilus planus n. sp. and Pseudoplatynematum dengi n. sp., with improved definition of Pseudoplatynematum (Ciliophora, Oligohymenophora). European Journal of Protistology, 46: 212–220.

    Article  Google Scholar 

  • Fan, X. P., Hu, X. Z., Al-Farraj, S. A., Clamp, J. C., and Song, W. B., 2011a. Morphological description of three marine ciliates (Ciliophora, Scuticociliatia), with establishment of a new genus and two new species. European Journal of Protistology, 47: 186–196.

    Article  Google Scholar 

  • Fan, X. P., Lin, X. F., Al-Rasheid, K. A. S., Al-Farraj, S. A., Warren, A., and Song, W. B., 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 Protozoologica, 50: 219–234.

    Google Scholar 

  • Felipe, A. P., Lamas, J., Sueiro, R. A., Folgueira, I., and Leiro, J. M., 2017. New data on flatfish scuticociliatosis reveal that Miamiensis avidus and Philasterides dicentrarchi are different species. Parasitology, 144: 1394–1411.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gao, F., Gao, S., Wang, P., Katz, L. A., and Song, W. B., 2014. Phylogenetic analyses of cyclidiids (Protista, Ciliophora, Scuticociliatia) based on multiple genes suggest their close relationship with thigmotrichids. Molecular Phylogenetics and Evolution, 75: 219–226.

    Article  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 (Pt B): 409–423, DOI: 10.1016/j.ejop.2017.04.009.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gao, F., Strüder-Kypke, M., Yi, Z. Z., Miao, M., Al-Farraj, S. A., and Song, W., 2012b. Phylogenetic analysis and taxonomic distinction of six genera of pathogenic scuticociliates (Protozoa, Ciliophora) inferred from small-subunit rRNA gene sequences. International Journal of Systematic and Evolutionary Microbiology, 62: 246–256.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gomez-Saladin, E., and Small, E. B., 1993a. Oral morphogenesis of the microstome to macrostome transformation in Miamiensis avidus strain Ma/2. Journal of Eukaryotic Microbiology, 40: 363–370.

    Article  Google Scholar 

  • Gomez-Saladin, E., and Small, E. B., 1993b. Prey-induced transformation of Miamiensis avidus strain Ma/2 by a soluble factor. Journal of Eukaryotic Microbiology, 40: 550–556.

    Article  Google Scholar 

  • Hall, T. A., 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41: 95–98.

    Google Scholar 

  • Huang, J., Luo, X., Bourland, W. A., Gao, F., and Gao, S., 2016. Multigene-based phylogeny of the ciliate families Amphisiellidae and Trachelostylidae (Protozoa: Ciliophora: Hypotrichia). Molecular Phylogenetics and Evolution, 101: 101–110.

    Article  Google Scholar 

  • Iglesias, R., Paramá, A., Alvarez, M. F., Leiro, J., Fernández, J., and Sanmartín, M. L., 2001. Philasterides dicentrarchi (Ciliophora, Scuticociliatida) as the causative agent of scuticociliatosis in farmed turbot Scophthalmus maximus in Galicia (NW Spain). Diseases of Aquatic Organisms, 46: 47–55.

    Article  Google Scholar 

  • Jung S. J., Bae M. J., Oh, M. J., and Lee, J., 2011. Sequence conservation in the internal transcribed spacers and 5.8S ribosomal RNA of parasitic scuticociliates Miamiensis avidus (Ciliophora, Scuticociliatia). Parasitology International, 60: 216–219.

    Article  Google Scholar 

  • Jung, S. J., Im, E. Y., Strüder-Kypke, M. C., Kitamura, S. I., and Woo, P. T. K., 2010. Small subunit ribosomal RNA and mitochondrial cytochrome c oxidase subunit 1 gene sequences of 21 strains of the parasitic scuticociliate Miamiensis avidus (Ciliophora, Scuticociliatia). Parasitology Research, 108: 1153–1161.

    Article  Google Scholar 

  • Jung, S. J., Kitamura, S. I., Song, J. Y., and Oh, M. J., 2007. Miamiensis avidus (Ciliophora: Scuticociliatida) causes systemic infection of olive flounder Paralichthys olivaceus and is a senior synonym of Philasterides dicentrarchi. Diseases of Aquatic Organisms, 73: 227–234.

    Article  Google Scholar 

  • Kim, S. M., Cho, J. B., Kim, S. K., Nam, Y. K., and Kim, K. H., 2004. Occurrence of scuticociliatosis in olive flounder Paralichthys olivaceus by Phiasterides dicentrarchi (Ciliophora: Scuticociliatida). Diseases of Aquatic Organisms, 62: 233–238.

    Article  Google Scholar 

  • Lynn, D. H., 2008. The Ciliated Protozoa: Characterization, Classification and Guide to the Literature. Springer Verlag, Dordrecht, 1–605.

    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.

    Article  Google Scholar 

  • Nylander, J. A. A., 2004. MrModeltest v2. Uppsala University.

    Google Scholar 

  • Pan, X. M., 2016. Seven scuticociliates (Protozoa, Ciliophora) from Alabama, USA, with descriptions of two parasitic species isolated from a freshwater mussel Potamilus purpuratus. European Journal of Taxonomy, 249: 1–19.

    Google Scholar 

  • Pan, X. M., Fan, X. P., Al-Farraj, S. A., Gao, S., and Chen, Y., 2016. Taxonomy and morphology of four ‘ophrys-related’ scuticociliates (Protista, Ciliophora, Scuticociliatia), with the description of a new genus, Paramesanophrys gen. nov. European Journal of Taxonomy, 191: 1–18.

    Google Scholar 

  • Pan, X. M., Liang, C. D., Wang, C. D., Warren, A., Mu, W. J., Chen, H., Yu, L. J., and Chen, Y., 2017. One freshwater species of the genus Cyclidium, Cyclidium sinicum spec. nov. (Protozoa; Ciliophora), with an improved diagnosis of the genus Cyclidium. International Journal of Systematic and Evolutionary Microbiology, 67: 557–564.

    Article  Google Scholar 

  • Pan, X. M., Zhu, M. Z., Ma, H. G., Al-Rasheid, K. A. S., and Hu, X. Z., 2013. Morphology and small-subunit rRNA gene sequences of two novel marine ciliates, Metanophrys orientalis spec. nov. and Uronemella sinensis spec. nov. (Protista, Ciliophora, Scuticociliatia), with an improved diagnosis of the genus Uronemella. International Journal of Systematic and Evolutionary Microbiology, 63: 3515–3523.

    Google Scholar 

  • Posada, D., and Crandall, K. A., 1998. Modeltest: Testing the model of DNA substitution. Bioinformatics, 14: 817–818.

    Article  Google Scholar 

  • Ronquist, F., and Huelsenbeck, J. P., 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19: 1572–1574.

    Article  Google Scholar 

  • Rossteuscher, S., Wenker, C., Jermann, T., Wahli, T., Oldenberg, E., and Schmidt-Posthaus, H., 2008. Severe scuticociliate (Philasterides dicentrarchi) infection in a population of sea dragons (Phycodurus eques and Phyllopteryx taeniolatus). Veterinary Parasitology, 45: 546–550.

    Google Scholar 

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

    Article  Google Scholar 

  • Small, E. B., and Lynn, D. H., 1985. Phylum Ciliophora. In: An Illustrated Guide to the Protozoa. Lee, J. J., et al., eds., Society of Protozoologists Special Publication, Lawrence, Kansas, 393–575.

    Google Scholar 

  • Smith, P. J., McVeagh, S. M., Hulston, D., Anderson, S. A., and Gublin, Y., 2009. DNA identification of ciliates associated with disease outbreaks in a New Zealand marine fish hatchery. Diseases of Aquatic Organisms, 86: 163–167.

    Article  Google Scholar 

  • Song, W. B., Warren, A., and Hu, X. Z., 2009. Free-Living Ciliates in the Bohai and Yellow Seas, China. Science Press, Beijing, 178–179.

    Google Scholar 

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

    Google Scholar 

  • Song, W. B., Zhao, Y. J., Xu, K. D., Hu, X. Z., and Gong, J., 2003. Pathogenic Protozoa in Mariculture. Science Press, Beijing, 257–260.

    Google Scholar 

  • Stamatakis, A., Hoover, P., and Rougemont, J., 2008. A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology, 57: 758–771.

    Article  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S., 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28: 2731–2739.

    Article  Google Scholar 

  • Tao, Z., Liu, L., Chen, X. R., Zhou, S. M., and Wang, G. L., 2016. First isolation of Miamiensis avidus (Ciliophora: Scuticociliatida) associated with skin ulcers from reared pharaoh cuttlefish Sepia pharaonis. Diseases of Aquatic Organisms, 122: 67–71.

    Article  Google Scholar 

  • Thompson, J. C., and Moewus, L., 1964. Miamiensis avidus n. g., n. sp., a marine facultative parasite in the ciliate order Hymenostomatida. Journal of Protozoology, 11: 378–381.

    Google Scholar 

  • Wang, C. D., Zhang, T. T., Wang, Y. R., Katz, L. A., Gao, F., and Song, W. B., 2017a. Disentangling sources of variation in SSU rDNA sequences from single cell analyses of ciliates: Impact of copy number variation and experimental error. Proceeding of the Royal Society B, 284: 20170425.

    Article  Google Scholar 

  • Wang, Y., Chen, X., Sheng, Y., Liu, Y., and Gao, S., 2017b. N6-adenine DNA methylation is associated with the linker DNA of H2A.Z-containing well-positioned nucleosomes in Po1 II-transcribed genes in Tetrahymena. Nucleic Acids Research, 45: 11594–11606.

    Article  Google Scholar 

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

    Google Scholar 

  • Xu, Y., Fan, X. P., Al-Farraj, S. A., and Hu, X. Z., 2017. Morphological description of two new ciliates (Ciliophora, Karyorelictea, Cryptopharyngidae): Apocryptopharynx discoidalis spec. nov. and Crytopharynx minutus spec. nov. European Journal of Protistology, 58: 77–86.

    Article  Google Scholar 

  • Yan, Y., Xu, Y., Al-Farraj, S. A., Al-Rasheid, K. A. S., and Song, W., 2016. Morphology and phylogeny of three trachelocercids (Protozoa, Ciliophora, Karyorelictea), with description of two new species and insight to the evolution of the family Trachelocercidae. Zoological Journal of the Linnean Socity, 177: 306–319.

    Article  Google Scholar 

  • Zhao, Y., Fan, X. P., Xu, Y., Hu, X. Z., and Ma, H. G., 2011. Morphological studies on eight marine scuticociliates (Protozoa, Ciliophora) from China. Acta Hydrobiologica Sinica, 35: 929–939.

    Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 31572230), the Open Fund of Zhejiang Provincial Top Key Discipline of Aquaculture in Ningbo University (No. xkzsc1417), the K. C. Wong Magna Fund in Ningbo University, and the Scientific Research Foundation of Graduate School of Ningbo University. We are very grateful to Dr. Jie Huang (Institute of Hydrobiology, Chinese Academy of Sciences) for her help with the phylogenetic analysis.

Author information

Authors and Affiliations

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

    Mingzhen Ma, Borong Lu, Yuhong Shi & Xiangrui Chen

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

    Borong Lu

  3. School of Life Sciences, East China Normal University, Shanghai, 200062, China

    Xinpeng Fan

Authors
  1. Mingzhen Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Borong Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xinpeng Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuhong Shi
    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 authors

Correspondence to Yuhong Shi or Xiangrui Chen.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, M., Lu, B., Fan, X. et al. Taxonomic Clarification of A Well-Known Pathogenic Scuticociliate, Miamiensis avidus Thompson & Moewus, 1964 (Ciliophora, Scuticociliatia). J. Ocean Univ. China 17, 1231–1242 (2018). https://doi.org/10.1007/s11802-018-3702-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11802-018-3702-8

Key words

Search

Navigation