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Molecular studies on the seasonal occurrence and development of five myxozoans in farmed Salmo trutta L.

Published online by Cambridge University Press:  11 October 2005

A. S. HOLZER ,
C. SOMMERVILLE  and
R. WOOTTEN
A. S. HOLZER
Affiliation:
Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, UK
C. SOMMERVILLE
Affiliation:
Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, UK
R. WOOTTEN
Affiliation:
Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, UK
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Abstract

Five myxozoan species, Tetracapsuloides bryosalmonae, Sphaerospora truttae, Chloromyxum schurovi, Chloromyxum truttae and a Myxobolus species were detected in farmed brown trout, Salmo trutta L. from Central Scotland. Using PCR and in situ hybridization, this study investigated the seasonal occurrence and tissue location of these species in young of the year brown trout. C. schurovi, C. truttae and Myxobolus sp. were first detected in brown trout in April, 2 months before T. bryosalmonae and S. truttae. T. bryosalmonae and S. truttae showed proliferation in the blood with intravascular stages of T. bryosalmonae accumulating in the heart. In contrast, only small amounts of PCR products of C. schurovi and C. truttae were obtained from the blood, suggesting that these species use the vascular system for transport but proliferate only in their target tissues from which large amounts of PCR product were obtained and where parasites were visible in histological sections. Large amounts of PCR product were obtained for T. bryosalmonae, S. truttae and both Chloromyxum species from the gills of brown trout, suggesting the gills as entry locus for these species. The neurotropic Myxobolus species formed plasmodia predominantly in the peripheral nerves, possibly indicating an entry route through the skin. Presporogonic stages of all other species had disappeared by September and mature spores were present from August onwards.

Keywords

MyxozoaSalmo truttaseasonal occurrencemoleculartissue localization
Type
Research Article
Information
Parasitology , Volume 132 , Issue 2 , February 2006 , pp. 193 - 205
Copyright
2005 Cambridge University Press

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References

REFERENCES

Andree, K. B., MacConnell, E. and Hedrick, R. P. ( 1998). A nested polymerase chain reaction for the detection of genomic DNA of Myxobolus cerebralis in rainbow trout Oncorhynchus mykiss. Diseases of Aquatic Organisms 34, 145–154.CrossRefGoogle Scholar
Baldwin, T. J. and Myklebust, K. A. ( 2002). Validation of a single round polymerase chain reaction assay for identification of Myxobolus cerebralis myxospores. Diseases of Aquatic Organisms 49, 185–190.CrossRefGoogle Scholar
Bartholomew, J. L., Rodriguez, R. J. and Arakawa, C. K. ( 1995). Development of a DNA probe for the myxosporean parasite Ceratomyxa shasta, using the polymerase chain reaction with arbitrary primers. Diseases of Aquatic Organisms 21, 215–220.CrossRefGoogle Scholar
Brody, J. R. and Kern, S. E. ( 2004). Sodium boric acid: a Tris-free, cooler conductive medium for DNA electrophoresis. BioTechniques 36, 214–216.Google Scholar
Clifton-Hadley, R. S., Bucke, D. and Richards, R. H. ( 1984). Proliderative kidney disease of salmonid fish: a review. Journal of Fish Diseases 7, 363–377.CrossRefGoogle Scholar
El-Matbouli, M., Hoffman, R. W. and Mandok, C. ( 1995). Light and electronic microscopic observations on the route of the triactinomyxon-sporoplam of Myxobolus cerebralis from epidermis into rainbow trout cartilage. Journal of Fish Biology 46, 919–935.Google Scholar
El-Matbouli, M., Hoffmann, R. W., Schoel, H., McDowell, T. S. and Hedrick, R. P. ( 1999). Whirling disease: Host specificity and interaction between the actinosporean stage of Myxobolus cerebralis and Rainbow trout Oncorhynchus mykiss. Diseases of Aquatic Organisms 35, 1–12.Google Scholar
Eszterbauer, E., Benko, M., Dan, A. and Molnar, K. ( 2001). Identification of fish-parasitic Myxobolus (Myxosporea) species using a combined PCR-RFLP method. Diseases of Aquatic Organisms 44, 35–39.CrossRefGoogle Scholar
Feist, S. W., Peeler, E. J., Gardiner, R., Smith, E. and Longshaw, M. ( 2002). Proliferative kidney disease and renal myxosporidiosis in juvenile salmonids from rivers in England and Wales. Journal of Fish Diseases 25, 451–458.CrossRefGoogle Scholar
Ferguson, H. W. ( 1975). Phagocytosis by the endocardial lining cells of the atrium of plaice (Pleuronectes platessa). Journal of Comparative Pathology 85, 561–569.CrossRefGoogle Scholar
Ferguson, H. W. ( 1981). Effects of temperature on the development of proliferative kidney disease in rainbow trout, Salmo gairdneri Richardson. Journal of Fish Diseases 4, 175–177.CrossRefGoogle Scholar
Foott, J. S. and Hedrick, R. P. ( 1987). Seasonal occurrence of the infectious stage of proliferative kidney disease (PKD) and resistance of rainbow trout, Salmo gairdneri Richardson, to reinfection. Journal of Fish Biology 30, 477–483.CrossRefGoogle Scholar
Gay, M., Okamura, B. and De Kinkelin, P. ( 2001). Evidence that infectious stages of Tetracapsula bryosalmonae for rainbow trout Oncorhynchus mykiss are present throughout the year. Diseases of Aquatic Organisms 46, 31–40.CrossRefGoogle Scholar
Hallett, S. L., Atkinson, S. D. and El-Matbouli, M. ( 2002). Molecular characterisation of two aurantiactinomyxon (Myxozoa) phenotypes reveals one genotype. Journal of Fish Diseases 25, 627–631.CrossRefGoogle Scholar
Hallett, S. L., Atkingson, S. D., Erseus, C. and El-Matbouli, M. ( 2004). Molecular methods to clarify morphometric variability in triactinomyxon spores (Myxozoa) released from different oligochaete hosts. Systematic Parasitology 57, 1–14.Google Scholar
Hendrickson, G. L., Carleton, A. and Manzer, D. ( 1989). Geographic and seasonal distribution of the infective stage of Ceratomyxa shasta (Myxozoa) in northern California. Diseases of Aquatic Organisms 7, 165–169.CrossRefGoogle Scholar
Hillis, D. M. and Dixon, M. T. ( 1991). Ribosomal DNA – Molecular evolution and phylogenetic inference. Quarterly Review of Biology 66, 410–453.CrossRefGoogle Scholar
Hogge, C., Campbell, M. and Johnson, K. ( 2004). Discriminating between a neurotropic Myxobolus sp. and M. cerebralis, the dausative agent of salmonid whirling disease. Journal of Aquatic Animal Health 16, 137–144. DOI: 10.1577/H04–007.1CrossRefGoogle Scholar
Holst, J. C., Nilsen, F., Hodneland, K. and Nylund, A. ( 1993). Observations of the biology and parasites of postsmolt Atlantic salmon, Salmo salar, from the Norwegian Sea. Journal of Fish Biology 42, 962–966.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. DOI:10.1046/j.1365–2761.2003.00501.xCrossRefGoogle Scholar
Holzer, A. S., Sommerville, C. and Wootten, R. ( 2004). Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. International Journal for Parasitology 34, 1099–1111.CrossRefGoogle Scholar
Kent, M. L., Khattra, J., Hervio, D. M. L. and Devlin, R. H. ( 1998). Ribosomal DNA sequence analysis of isolates of the PKX myxosporean and their relationship to members of the genus Sphaerospora. Journal of Aquatic Animal Health 10, 12–21.2.0.CO;2>CrossRefGoogle Scholar
Lom, J. and Arthur, J. R. ( 1989). A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases 12, 151–156.CrossRefGoogle Scholar
Lom, J., Molnar, K. and Dyková, I. ( 1986). Hoferellus gilsoni (Debaissieux, 1925) comb. n. (Myxozoa, Myxosporea): re-discription and mode of attachment to the epithelium of the urinary bladder of its host, the European eel. Protistologica 22, 405–413.Google Scholar
McGeorge, J. ( 1994). Studies on the biology of Sphaerospora sp. (Myxozoa: Myxosporea) from farmed Atlantic salmon, Salmo salar L., in Scotland. Ph.D. thesis, Institute of Aquaculture, University of Stirling.
McGeorge, J. M., Sommerville, C. and Wootten, R. ( 1994). Light and electron microscope observations on extrasporogonic and sporogonic stages of a myxosporean parasite of the genus Sphaerospora Thelohan, 1892 from Atlantic salmon, Salmo salar L., in Scotland. Journal of Fish Diseases 17, 227–238.CrossRefGoogle Scholar
McGeorge, J. M., Sommerville, C. and Wootten, R. ( 1996). Epizootiology of Sphaerospora truttae (Myxozoa: Myxosporea) infections of Atlantic salmon Salmo salar at freshwater smolt producing hatcheries in Scotland. Diseases of Aquatic Organisms 26, 33–41.CrossRefGoogle Scholar
Melendy, J. and Cone, D. K. ( 2001). Initial infection, distribution, and seasonal occurrence of Hoferellus gilsoni (Myxozoa) within a population of Anguilla rostrata (Anguillidae) in southern Nova Scotia. Journal of Parasitology 87, 957–960.CrossRefGoogle Scholar
Morris, D. J., Adams, A. and Richards, R. H. ( 2000). In situ hybridisation identifies the gill as a portal of entry for PKX (Phylum Myxozoa), the causative agent of proliferative kidney disease in salmonids. Parasitology Research 86, 950–956.CrossRefGoogle Scholar
Morris, D. C., Morris, D. J. and Adams, A. ( 2002). Development of improved PCR to prevent false positives and false negatives in the detection of Tetracapsula bryosalmonae, the causative agent of proliferative kidney disease. Journal of Fish Diseases 25, 483–490.CrossRefGoogle Scholar
Okamura, B., Anderson, C. L., Longshaw, M., Feist, S. W. and Canning, E. U. ( 2001). Patterns of occurrence and 18S rDNA sequence variation of PKX (Tetracapsula bryosalmonae), the causative agent of salmonid proliferative kidney disease. Journal of Parasitology 87, 379–385.CrossRefGoogle Scholar
Palenzuela, O. and Bartholomew, J. L. ( 2002). Molecular tools for the diagnosis of Ceratomyxa shasta (Myxozoa). In Molecular Diagnosis of Salmonid Diseases ( ed. Cunningham, C. O.), pp. 285–298. Kluwer Academic Publishers, Netherlands.CrossRef
Palenzuela, O., Trobridge, G. and Bartholomew, J. L. ( 1999). Development of a polymerase chain reaction diagnostic assay for Ceratomyxa shasta, a myxosporean parasite of salmonid fish. Diseases of Aquatic Organisms 36, 45–51.CrossRefGoogle Scholar
Pearse, A. G. E. ( 1968). Histochemistry, Theoretical and Applied. Churchill Livingstone, London.
Press, C. M. L. and Evensen, O. ( 1999). The morphology of the immune system in teleost fishes. Fish and Shellfish Immunology 9, 309–318.CrossRefGoogle Scholar
Saulnier, D. and De Kinkelin, P. ( 1997). Polymerase chain reaction primers for investigations on the causative agent of proliferative kidney disease of salmonids. Journal of Fish Diseases 20, 467–470.CrossRefGoogle Scholar
Shul'man, B. S. and Ieshko, E. P. ( 2003). Chloromyxum schurovi sp.n. – a new myxosporidian species (Myxosporea: Sphaerosporidae) from salmonid fishes (Salmonidae). Parazitologiia 37, 246–247.Google Scholar
Sedlaczek, J. ( 1991). Chloromyxum sp. (Myxosporidia) in der Niere von Salmo trutta f. fario (Osteichthyes). Angewandte Parasitologie 32, 137–142.Google Scholar
Wootten, R. and McVicar, A. H. ( 1982). Some preliminary observations on proliferative kidney disease in wild brown trout, Salmo trutta L. in a Scottish stream. Bulletin of the European Association of Fish Pathologists 4, 60–62.Google Scholar
Wyatt, E. J. ( 1978). A new host and site of infection for Myxobolus kisutchi and host record for Myxobolus insidiosus. Journal of Parasitology 64, 169–170.CrossRefGoogle Scholar
Xiao, C. and Desser, S. S. ( 2000). Molecular characterization of myxozoan parasites from Lake Sasajewun, Algonquin Park, Ontario, by riboprinting. Journal of Eukaryotic Microbiology 47, 85–89.CrossRefGoogle Scholar
Yasutake, W. T. and Wood, E. M. ( 1957). Some myxosporidia found in Pacific northwest salmonids. Journal of Parasitology 43, 633–642.CrossRefGoogle Scholar