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Ultrastructure and phylogeny of Philasterides dicentrarchi (Ciliophora, Scuticociliatia) from farmed turbot in NW Spain

Published online by Cambridge University Press:  03 January 2006

A. PARAMÁ ,
J. A. ARRANZ ,
M. F. ÁLVAREZ ,
M. L. SANMARTÍN  and
J. LEIRO
A. PARAMÁ
Affiliation:
Laboratorio de Parasitología, Departamento de Microbiología y Parasitología, Instituto de Investigación y Análisis Alimentarios, Universidad de Santiago de Compostela, C/ Constantino Candeira s/n, 15782, Santiago de Compostela, Spain
J. A. ARRANZ
Affiliation:
Laboratorio de Parasitología, Departamento de Microbiología y Parasitología, Instituto de Investigación y Análisis Alimentarios, Universidad de Santiago de Compostela, C/ Constantino Candeira s/n, 15782, Santiago de Compostela, Spain
M. F. ÁLVAREZ
Affiliation:
Laboratorio de Parasitología, Departamento de Microbiología y Parasitología, Instituto de Investigación y Análisis Alimentarios, Universidad de Santiago de Compostela, C/ Constantino Candeira s/n, 15782, Santiago de Compostela, Spain
M. L. SANMARTÍN
Affiliation:
Laboratorio de Parasitología, Departamento de Microbiología y Parasitología, Instituto de Investigación y Análisis Alimentarios, Universidad de Santiago de Compostela, C/ Constantino Candeira s/n, 15782, Santiago de Compostela, Spain
J. LEIRO
Affiliation:
Laboratorio de Parasitología, Departamento de Microbiología y Parasitología, Instituto de Investigación y Análisis Alimentarios, Universidad de Santiago de Compostela, C/ Constantino Candeira s/n, 15782, Santiago de Compostela, Spain
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Abstract

Several species of opportunistic histophagous scuticociliates have been implicated in systemic infections of farmed fish. In turbot, scuticociliatosis is an emerging disease, and the identification of the parasite species involved is controversial. We have previously isolated Philasterides dicentrarchi from farmed turbot scuticociliatosis outbreaks in northwest Spain. In the present study, we report detailed ultrastructural studies of this parasite, and investigate phylogenetic relations with other members of the order Philasterida on the basis of sequence comparison of the small-subunit rRNA (SSUrRNA) gene. Ultrastructural study indicates the presence of dikinetids in the anterior two-thirds of the body; micronucleus closely associated with the macronucleus, though not physically connected; numerous mitochondria located below the cell cortex, parallel to the surface; numerous spherical and fusiform extrusomes located close to the plasma membrane. We consider that these characteristics are useful for diagnosis of infections by this parasite. A nested 350-bp nucleotide sequence of the SSUrRNA gene of the turbot P. dicentrachi isolate showed high identity with previously reported SSUrRNA gene sequences from 2 scuticociliates isolated from olive flounder Paralichthys olivaceus in Korea, namely P. dicentrarchi (98%) and Miamiensis avidus (99%); conversely, our P. dicentrarchi sequence showed low identity (86%) with that of Uronema marinum, a scuticociliate that has also been implicated in scuticociliatosis outbreaks in turbot in Europe and olive flounder in Asia. Phylogenetic tree construction on the basis of the SSUrRNA gene sequences, using the neighbour-joining method, confirm that the different P. dicentrarchi isolates and M. avidus are closely related and a possible synonymy between both ciliates species should be considered.

Keywords

turbotScophthalmus maximusPhilasterides dicentrarchiscuticociliatesultrastructuresmall subunit rRNAphylogeny
Type
Research Article
Information
Parasitology , Volume 132 , Issue 4 , April 2006 , pp. 555 - 564
Copyright
2006 Cambridge University Press

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References

REFERENCES

Allen, R. D. ( 1971). Fine structure of membranous and microfibrillar systems in the cortex of Paramecium caudatum. Journal of Cell Biology 49, 1–20.CrossRefGoogle Scholar
Álvarez-Pellitero, P., Palenzuela, O., Padrós, F., Sitjà-Bobadilla, A., Riaza, A., Silva, R. and Arán, J. ( 2004). Histophagous scuticociliatids (Ciliophora) parasiting turbot Scophthalmus maximus: morphology, in vitro culture and virulence. Folia Parasitologica 51, 177–187.CrossRefGoogle Scholar
Chapman, G. B. and Kern, R. C. ( 1983). Ultrastructural aspects of the somatic cortex and contractile vacuole of the ciliate, Ichthyophthirius multifiliis Fouquet. Journal of Protozoology 30, 481–490.CrossRefGoogle Scholar
Cheung, P. J., Nigrelli, R. F. and Ruggieri, D. ( 1980). Studies of the morphology of Uronema marinum Dujardin (Ciliatea: Uronematidae) with a description of the histopathology of the infection in marine fishes. Journal of Fish Diseases 3, 295–303.CrossRefGoogle Scholar
Dyková, I. and Figueras, A. ( 1994). Histopathological changes in turbot Scophthalmus maximus due to a histiophagous ciliate. Diseases of Aquatic Organisms 18, 5–9.CrossRefGoogle Scholar
Dragesco, A., Dragesco, J., Coste, F., Gasc, C., Romestand, B., Raymond, J. 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 Protistology 31, 327–340.Google Scholar
Elliott, A. m. and Bak, I. L. ( 1964). The fate of mitochondria during aging in Tetrahymena pyriformis. Journal of Cell Biology 21, 113–129.CrossRefGoogle Scholar
Fleury, A. ( 1991). Dynamics of the cytoskeleton during morphogenesis in the ciliate Euplotes. II. Cortex and continuous microtubular systems. European Journal of Protistology 27, 220–237.CrossRefGoogle Scholar
Fleury, A. and Laurent, M. ( 1994). Transmission of surface pattern through a dedifferentiated stage in the ciliate Paraurostyla. Evidence from the analysis of microtubule and basal body deployment. Journal of Eukaryotic Microbiology 41, 276–291.Google Scholar
Gorovsky, M. A. ( 1973). Macro- and micronuclei of Tetrahymena pyriformis: a model system for studying the structure and function of eukaryotic nuclei. Journal of Protozoology 20, 19–25.CrossRefGoogle Scholar
Hausmann, K. ( 1978). Extrusive organelles in Protists. International Review of Cytology 52, 197–276.CrossRefGoogle Scholar
Hausmann, K. and Hülsmann, N. ( 1996). Protozoology. Part III. Selected Topics of General Protozoology. Comparative Morphology and Physiology of Protozoa. Georg Thieme Verlag Stuttgart, New York.
Higgins, D., Thompson, J., Gibson, T., Thompson, J. D., Higgins, D. G. and Gibson, T. J. ( 1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.Google Scholar
Iglesias, R., Paramá, A., Álvarez, 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.CrossRefGoogle Scholar
Iglesias, R., Paramá, A., Álvarez, M. F., Leiro, J., Aja, C. and Sanmartín, M. L. ( 2003). In vitro requirements for the fish pathogen Philasterides dicentrarchi (Ciliophora, Scuticociliatida). Veterinary Parasitology 111, 19–30.CrossRefGoogle Scholar
Jung, S.-J., Kitamura, S.-I., Song, J.-Y., Joung, I.-Y. and Oh, M.-J. ( 2005). Complete small subunit rRNA gene sequence of the scuticociliate Miamiensis avidus pathogenic to olive flounder Paralichthys olivaceus. Diseases of Aquatic Organisms 64, 159–162.CrossRefGoogle Scholar
Jee, B. Y., Kim, Y. C. and Park, M. S. ( 2001). Morphology and biology of parasite responsible for scuticociliatosis of cultured olive flounder Paralichthys olivaceus. Diseases of Aquatic Organisms 47, 49–55.CrossRefGoogle Scholar
Kaneshiro, E. S. and Holz, G. G. Jr. ( 1976). Observations on the ultrastructure of Uronema spp., marine scuticociliates. Journal of Protozoology 23, 503–517.CrossRefGoogle Scholar
Kim, S.m., Cho, J. B., Kim, S. K., Nam, Y. K. and Kim, K. H. ( 2004 a). Occurrence of scuticociliatosis in olive flounder Paralichthys olivaceus by Philasterides dicentrarchi (Ciliophora: Scuticociliatida). Diseases of Aquatic Organisms 62, 233–238.Google Scholar
Kim, S. M., Cho, J. B., Lee, E. H., Kwon, S. R., Kim, S. K., Nam, Y. K. and Kim, K. H. ( 2004 b). Pseudocohnilembus persalinus (Ciliophora: Scuticociitida) is an additional species causing scuticociliatosis in olive flounder Paralichthys olivaceus. Diseases of Aquatic Organisms 62, 239–244.Google Scholar
Kugrens, P., Lee, R. E. and Corliss, J. O. ( 1994). Ultrastructure, biogenesis and functions of extrusive organelles in selected non-ciliate protists. Protoplasma 181, 164–190.CrossRefGoogle Scholar
Kumar, S., Tamura, K. and Nei, M. ( 2004). MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.CrossRefGoogle Scholar
Kurz, S. and Tiedtke, A. ( 1993) The Golgi apparatus of Tetrahymena thermophila. Journal of Eukaryotic Microbiology 40, 10–13.CrossRefGoogle Scholar
Leiro, J., Siso, M. I. G., Paramá, A., Ubeira, F. m. and Sanmartín, M. L. ( 2000). RFLP analysis of PCR-amplified small subunit ribosomal DNA of three fish microsporidian species. Parasitology 120, 113–119.CrossRefGoogle Scholar
Leiro, J., Iglesias, R., Paramá, A., Aragort, W. and Sanmartín, M. L. ( 2002). PCR detection of Tetramicra brevifilum (Microspora) infection in turbot (Scophthalmus maximus L.) musculature. Parasitology 124, 145–151.CrossRefGoogle Scholar
Munday, B. L., O'Donoghue, P. J., Watts, M., Rough, K. and Hawkesford, T. ( 1997). Fatal encephalitis due to the scuticociliate Uronema nigricans in sea-caged, southern bluefin tuna Thunnus maccoyii. Diseases of Aquatic Organisms 30, 17–25.CrossRefGoogle Scholar
Orias, E. and Rasmussen, L. ( 1976). Dual capacity for nutrient uptake in Tetrahymena. IV. Growth without food vacuoles and its implications. Experimental Cell Research 102, 127–137.CrossRefGoogle Scholar
Paramá, A, Iglesias, R., Álvarez, M. F., Leiro, J., Aja, C. and Sanmartín, M. L. ( 2003). Philasterides dicentrarchi (Cicliophora, Scuticociliatida): experimental infection and possible routes of entry in farmed turbot (Scophthalmus maximus). Aquaculture 217, 73–80.CrossRefGoogle Scholar
Rosati, G. and Modeo, L. ( 2003). Extrusomes in ciliates: diversification, distribution and phylogenetic implications. Journal of Eukaryotic Microbiology 50, 383–402.CrossRefGoogle Scholar
Song, W. 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
Sterud, E., Hansen, M. K. and Mo, T. A. ( 2000). Systemic infection with Uronema-like ciliates in farmed turbot, Scophthalmus maximus (L.). Journal Fish Diseases 23, 33–37.CrossRefGoogle Scholar
Tokuyasu, K. and Scherbaum, O. H. ( 1965). Ultrastructure of mucocysts and pellicle of Tetrahymena pyriformis. Journal of Cell Biology 27, 87–81.CrossRefGoogle Scholar