Hostname: page-component-745bb68f8f-grxwn Total loading time: 0 Render date: 2025-01-11T04:04:33.275Z Has data issue: false hasContentIssue false
  • English
  • Français

X-cell parasites in the European dab Limanda limanda are related to other X-cell organisms: a discussion on the potential identity of this new group of parasites

Published online by Cambridge University Press:  24 June 2009

M. A. FREEMAN
M. A. FREEMAN*
Affiliation:
Institute of Biological Sciences, University of Malaya, Kuala Lumpur, 50603Malaysia Institute of Aquaculture, University of Stirling, Stirling, Scotland FK9 4LA, UK
*
*Corresponding author: Institute of Biological Sciences, University of Malaya, Kuala Lumpur, 50603Malaysia. Tel: +603 7967 4424. Fax: +603 7967 4178. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Unusual tumour-like pathologies caused by mysterious cells termed ‘X-cells’ have been reported from numerous fish groups worldwide. After nearly 100 years of research, the tumour-like growths have recently been shown to be caused by a protozoan parasite. In the present study, histopathology and small subunit ribosomal DNA (SSU rDNA) sequences are used to assess whether the X-cell parasite infecting Atlantic dab Limanda limanda L. is distinct from the X-cell parasite infecting Japanese flounder and goby, and to determine their systematic position within the protists. SSU rDNA from Scottish dab was 89·3% and 86·7% similar to Japanese X-cell sequences from flounder and goby respectively, indicating that the parasite infecting dab in the Atlantic is distinct from the Pacific species. Histological studies revealed significant gill pathology and demonstrated the precise location of the parasites within the gill tissues using specific in situ hybridization probes. Phylogenetic analyses showed that the X-cell parasites from Scotland and Japan form a monophyletic group within the Myzozoa, and are basal alveolates. However, ultrastructure of X-cells from dab fails to confirm this systematic placement.

Keywords

X-cellprotozoanparasiteSSU rDNAAlveolateMyzozoaancestral
Type
Research Article
Information
Parasitology , Volume 136 , Issue 9 , August 2009 , pp. 967 - 980
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alpers, C. E., McCain, B. B., Myers, M., Wellings, S. R., Poore, M., Bagshaw, J. and Dawe, C. J. (1977). Pathologic anatomy of pseudobranch tumours in Pacific cod, Gadus macrocephalus. Journal of the National Cancer Institute 59, 277–298.Google Scholar
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Azevedo, C. and Corral, L. (1985). Cytochemical analysis of the haplosporosomes and vesicle-like droplets of Haplosporidium lusitanicum (Haplosporidia, Haplosporidiidae), parasite of Helicon pellucidus (Prosobranchia). Journal of Invertebrate Pathology 46, 281–288.Google Scholar
Berthe, F. C. J., Le Roux, F., Peyretaillade, E., Peyret, P., Rodriguez, D, Gouy, M. and Vivarès, C. P. (2000). Phylogenetic analysis of the small subunit ribosomal RNA of Marteilia refringens validates the existence of phylum Paramyxea (Desportes and Perkins, 1990). Journal of Eukaryotic Microbiology 47, 288–193.Google Scholar
Brooks, R. E., McArn, G. E. and Wellings, S. R. (1969). Ultrastructural observations on an unidentified cell type found in epidermal tumors of flounders. Journal of the National Cancer Institute 43, 97–109.Google Scholar
Bucke, D. and Everson, I. (1992). “X-cell” lesions in Notothenia (Lepidonotothen) squamifrons Günther. Bulletin of the European Association of Fish Pathology 12, 83–86.Google Scholar
Cavalier-Smith, T. (2002). The phagotrophic origin of enkaryotes and phylogenetic classification of Protozoa. International Journal of Systematic and Evolutionary Microbiology 53, 297–354.Google Scholar
Cavalier-Smith, T. and Chao, E. E. (2003). “Phylogeny and Classification of Phylum Cercozoa (Protozoa)”. Protist 154, 341–358.CrossRefGoogle Scholar
Cavalier-Smith, T. and Chao, E. E. (2004). Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.). European Journal of Protozoology 40, 185–212.Google Scholar
Davison, W. (1998). X-cell gill disease in Pagothenia borchgreviniki from McMurdo Sound, Antarctica. Polar Biology 19, 17–23.CrossRefGoogle Scholar
Dawe, J. C. (1981). Polyoma tumours in mice and X-cell tumours in fish, viewed through the telescope and microscope. In Phyletic Approaches to Cancer (ed. Dawe, C. J., Harshbanger, J. C., Kondo, S., Sugimura, T. and Takayama, S.), pp. 19–49. Japan Scientific Societies Press, Tokyo, Japan.Google Scholar
Desser, S. S. and Khan, R. A. (1982). Light and electron microscope observations on pathological changes in the gills of the marine fish, Lycodes lavalaei Vladykov and Tremblay, associated with the proliferation of an unidentified cell. Journal of Fish Diseases 5, 351–364.CrossRefGoogle Scholar
Diamant, A. and McVicar, A. H. (1987). The effect of internal and external X-cell lesions on common dab, Limanda limanda L. Aquaculture 67, 127–133.Google Scholar
Diamant, A. and McVicar, A. H. (1989). Distribution of X-cell disease in common dab, Limanda limanda L., in the North Sea, and ultrastructural observations of previously undescribed developmental stages. Journal of Fish Diseases 12, 25–37.Google Scholar
Diamant, A., Fournie, J. W. and Courtney, L. E. (1994). X-cell pseudotumours in a hardhead catfish Arius felis (Ariidae) from Lake Pontchartrain, Louisiana, USA. Diseases of Aquatic Organisms 18, 181–185.CrossRefGoogle Scholar
Dyková, I., Figueras, A. and Novoa, B. (1993). X-cell lesions in the liver of coho salmon Oncorhynchus kisutch. Diseases of Aquatic Organisms 15, 171–174.CrossRefGoogle Scholar
Flores, B. S., Siddall, M. E. and Burreson, E. M. (1996). Phylogeny of the Haplosporidia (Eukaryota: Alveolate) based on small subunit ribosomal RNA gene sequence. Journal of Parasitology 82, 616–623.CrossRefGoogle ScholarPubMed
Franklin, C. E., McKenzie, J. C., Davison, W. and Carey, P. W. (1993). X-cell gill disease obliterates the lamellar blood supply in the Antartic teleost, Pagothenia borchgreviniki (Boulenger 1902). Journal of Fish Diseases 16, 249–254.CrossRefGoogle Scholar
Freeman, M. A., Yokoyama, H. and Ogawa, K. (2008). Description and phylogeny of Ceratomyxa anko sp. n. and Zschokkella lophii sp. n. from the Japanese anglerfish, Lophius litulon (Jordan). Journal of Fish Diseases 31, 921–930. doi:10.1111/j.1365-2761.2008.00965.xCrossRefGoogle Scholar
Ginsburger-Vogel, T. and Desportes, I. (1979). Etude ultrastructurale de la sporulation de Paramarteilia orchestiae gen. n., sp. n., parasite de l'Amphipode Orchestia gammarellus (Pallas). Journal of Protozoology 26, 390–403.Google Scholar
Gorgollón, P., Alfaro, E. and Kuznar, J. (1982). Caracterizacion morfologica de un tumor branquial en la Merluza (Merluccius gayi gayi). Revista Biologica Marina 18, 159–181.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
Harshbarger, J. C. (1984). Pseudoneoplasms in ectothermic animals. National Cancer Institute Monographs 5, 251–273.Google Scholar
Hillis, D. M. and Dixon, M. T. (1991). Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Reviews in Biology 66, 411–453.CrossRefGoogle ScholarPubMed
Hine, P. M. and Wesney, B. (1992). Interelationship of cytoplasmic structures in Bonamia sp. (Haplosporidia) infecting oyster Tiostrea chilensis: an interpretation. Diseases of Aquatic Organisms 14, 59–68.CrossRefGoogle Scholar
Holzer, A. S., Sommerville, C. and Wootten, R. (2003). Tracing the route of Sphaerospora truttae from the entry locus to the target organ of the host, Salmo salar L., using an optimized and specific in situ hybridization technique. Journal of Fish Diseases 26, 647–655.Google Scholar
Ito, Y., Kimura, I. and Miyake, T. (1976). Histopathological and virological investigations of papillomas in soles and gobies in coastal waters of Japan. Progress in Experimental Tumour Research 20, 86–93.CrossRefGoogle ScholarPubMed
Kent, M. L. and Hedrick, R. P. (1986). Development of the PKX myxosporean in rainbow trout Salmo gairdneri. Diseases of Aquatic Organisms 1, 169–182.CrossRefGoogle Scholar
Kent, M. L., Myers, M. S., Wellings, S. R. and Elston, R. A. (1988). An internal X-cell pseudotumour in a black croaker (Cheilotrema saturnum). Journal of Wildlife Diseases 24, 142–145.CrossRefGoogle Scholar
Lange, E. and Johannessen, J. V. (1977). Histochemical and ultrastructural studies of chemodectoma-like tumors in the cod (Gadus morhua L.) Laboratory Investigations 37, 96–104.Google Scholar
Leander, B. S., Clopton, R. E. and Keeling, P. J. (2003). Phylogeny of gregarines (Apicomplexa) as inferred from small-subunit rDNA and β-tubulin. International Journal of Systematic and Evolutionary Microbiology 53, 345–354.Google Scholar
Lom, J., Molnár, K. and Dyková, I. (1986). Hoferellus gilsoni (Debaisieux, 1925) comb. n. (Myxozoa, Myxosporea): redescription and mode of attachment to the epithelium of the urinary bladder of its host, the European eel. Protistologica 22, 405–413.Google Scholar
MacLean, S. A. and Despres-Patanjo, L. I. (1993). Gill X-cell lesion in American plaice (Hippoglossoides platessoides) concurrent with lymphocystis infection. Journal of Fish Biology 43, 947–950.Google Scholar
McCain, B. B., Gronlund, W. D., Myers, M. S. and Wellings, S. R. (1979) Tumours and microbial diseases of marine fishes in Alaskan waters. Journal of Fish Diseases 2, 111–130.CrossRefGoogle Scholar
McArn, G. E., Chuinard, R. G., Miller, B. S., Brooks, R. E. and Wellings, S. R. (1968). Pathology of skin tumours found on English sole and starry flounder from Pudget Sound, Washington. Journal of the National Cancer Institute 41, 229–242.Google Scholar
McVicar, A. H., Bucke, D., Watermann, B. and Dethlefsen, V. (1987). Gill X-cell lesions of dab, Limanda limanda L., in the southern North Sea. Diseases of Aquatic Organisms 2, 197–204.CrossRefGoogle Scholar
Miwa, S., Nakayasu, C., Kamaishi, T. and Yoshiura, Y. (2004). X-cells in fish pseudotumours are parasitic protozoans. Diseases of Aquatic Organisms 58, 165–170.Google Scholar
Miwa, S. and Kamaishi, T. (2009). Protistan X-cells in pseudotumors of yellowfin goby Acanthogobius flavimanus are a distinct organism from those in flathead flounder Hippoglossoides dubius. Diseases of Aquatic Organisms (in the Press) doi: 10.3354/dao02058.CrossRefGoogle ScholarPubMed
Montgomery, J. C. and Wells, R. M. G. (1993). Recent advances in the ecophysiology of Antarctic notothenioid fishes: metabolic capacity and sensory performance. In Fish Ecophysiology (ed. Rankin, J. C. and Jensen, F. B.), pp. 341–374. Chapman and Hall, London, UK.CrossRefGoogle Scholar
Morris, D. J., Adams, A. and Richards, R. H. (1999). In situ hybridization of DNA probes to PKX, the causative organism of proliferative kidney disease (PKD). Journal of Fish Diseases 22, 161–163.CrossRefGoogle Scholar
Morris, D. J., Adams, A. and Richards, R. H. (2000). Observations on the electron-dense bodies of the PKX parasite, agent of proliferative kidney disease in salmonids. Diseases of Aquatic Organisms 39, 201–209.Google Scholar
Morrison, C. M., Shum, G., Appy, R. G., Odense, P. and Annand, C. (1982). Histology and prevalence of X-cells lesions in Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Science 39, 1519–1530.CrossRefGoogle Scholar
Myers, M. S. (1981). Pathological anatomy of papilloma-like tumours in the Pacific Ocean perch Sebastesalutus from the Gulf of Alaska. M.S. thesis. University of Washington, Seattle, WA, USA.Google Scholar
Neefs, J. M. and De Wachter, R. (1990). A proposal for the secondary structure of a variable area of eukaryotic small-subunit ribosomal RNA. Nucleic Acids Research 18, 5695–5704.CrossRefGoogle Scholar
Nylander, J. A. A., Ronquist, F., Huelsenbeck, J. P. and Nieves-Aldrey, J. L. (2004). Bayesian phylogenetic analysis of combined data. Systematic Biology 53, 47–67.CrossRefGoogle ScholarPubMed
Perkins, F. O. (1969). Electron microscope studies of sporulation in the oyster pathogen Minchinia costalis (Sporozoa: Haplosoridia). Journal of Parasitology 55, 897–920.CrossRefGoogle Scholar
Peters, N., Peters, G., Stich, H. F., Acton, A. B. and Bresching, G. (1978). On differences in skin tumours of Pacific and Atlantic flatfish. Journal of Fish Diseases 1, 3–25.CrossRefGoogle Scholar
Peters, N., Schmidt, W., Kranz, H. and Stich, H. F. (1983). Nuclear inclusions in the X-cells of skin papillomas on Pacific flatfish. Journal of Fish Diseases 6, 533–536.CrossRefGoogle Scholar
Peters, N., Stich, H. F. and Kranz, H. (1981). The relationship between lymphocystis disease and X-cell papillomatosis in flatfish. Phyletic Approaches to Cancer. Japan Scientific Societies Press, Tokyo, Japan.Google Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Saitou, N. and Nei, M. (1987). The Neighbour-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
Saldarriaga, J. F., McEwan, M. L., Fast, N. M., Taylor, F. J. R. and Keeling, P. J. (2003). Multiple protein phylogenies show that Oxyrrhis marina and Perkinsus marinus are early branches of the dinoflagellate lineage. International Journal of Systematic and Evolutionary Microbiology 53, 355–365.CrossRefGoogle ScholarPubMed
Shinkawa, T. and Yamazaki, F. (1987). Proliferative patterns of X-cells found in the tumorous lesions of Japanese goby. Nippon Suisan Gakkaishi 53, 563–568.CrossRefGoogle Scholar
Siddall, M. E., Stokes, N. A. and Burreson, E. M. (1995). Molecular phylogenetic evidence that the phylum Haplosporidia has an alveolate ancestry. Molecular Biology and Evolution 12, 573–581.Google ScholarPubMed
Sprague, V. (1979). Classification of the Haplosporidia. Marine Fisheries Review 41, 40–44.Google Scholar
Sprague, V. (1982). Microspora; Myxozoa; Ascetospora. In Synopsis and Classification of Living Organisms, Vol. 1 (ed. Parker, S. P.), pp. 589–601. McGraw-Hill, New York, USA.Google Scholar
States, D. J., Gish, W. and Altschul, S. F. (1991). Improved sensitivity of nucleic acid database similarity searches using application specific scoring matrices. METHODS: A Companion to Methods in Enzymology 3, 66–70.Google Scholar
Stich, H. F., Acton, A. B. and Forrester, C. R. (1976). Fish tumors and sub-lethal effects of pollutants. Journal of the Fisheries Research Board of Canada 33, 1993–2001.Google Scholar
Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis using Parsimony (*and other Methods), v. 4.0 beta10. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 4876–4882.CrossRefGoogle Scholar
Watermann, B. (1982). An unidentified cell type associated with an inflammatory condition of the subcutaneous connective tissue in dab, Limanda limanda L. Journal of Fish Diseases 5, 257–261.Google Scholar
Watermann, B. and Dethlefsen, V. (1982). Histology of pseudobranchial tumours in Atlantic cod (Gadus morhua) from the North Sea and the Baltic Sea. Helgoländer Meeresuntersuchungen 35, 231–242.Google Scholar
Wellings, S. R. and Chuinard, R. G. (1964). Epidermal papillomas with virus-like particles in flathead sole, Hippoglossoides elassodon. Science 146, 374–388.CrossRefGoogle ScholarPubMed
Wellings, S. R., Chuinard, R. G., Gourley, R. T. and Cooper, R. A. (1964). Epidermal papillomas in the flathead sole, Hippoglossoides elassodon, with notes on the occurrence of similar neoplasms in other pleuronectids. Journal of the National Cancer Institute 33, 991–1004.Google Scholar
Wellings, S. R., McCain, B. B. and Miller, B. S. (1976). Epidermal papillomas in Pleuronectidae of Puget Sound, Washington. Progress in Experimental Tumor Research 20, 55–74.Google Scholar
Yamazaki, F., Hibino, T., Oishi, K., Harada, T., Stich, H. F. and Acton, A. B. (1978). X-cell morphology in the epidermal papillomas of flatfish collected from coastal waters of Hokkaido, Japan. Bulletin of the Japanese Society of Scientific Fisheries 44, 407–413.CrossRefGoogle Scholar