Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-18T03:47:45.177Z Has data issue: false hasContentIssue false
  • English
  • Français

Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea), the causative organism of salmonid proliferative kidney disease, to the freshwater bryozoan Fredericella sultana

Published online by Cambridge University Press:  04 September 2006

D. J. MORRIS  and
A. ADAMS
D. J. MORRIS
Affiliation:
Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, UK
A. ADAMS
Affiliation:
Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

Proliferative kidney disease (PKD), caused by the malacosporean parasite Tetracapsuloides bryosalmonae, causes significant losses among salmonids in Western Europe and North America. The role of salmonid fish in the life-cycle of this parasite has been conjectured upon for over a quarter of a century. To examine whether fish can transmit the infection to bryozoans, the known invertebrate host, water containing parasitized brown trout Salmo trutta was pumped into tanks containing colonies of Fredericella sultana collected from the wild. The specific parasite-free status of these colonies being first assessed, by PCR and prolonged laboratory culture. After 6 weeks exposure to the brown trout aquarium effluent, portions of these colonies displayed overt infections with T. bryosalmonae. This was in contrast to control bryozoans, derived from the experimental colonies prior to exposure, which remained T. bryosalmonae negative. In addition, spores obtained from the experimentally infected colonies were exposed to naïve rainbow trout, resulting in clinical PKD, thus completing a cycle of transmission. During the experiments, the infection was noted to inhibit statoblast formation within bryozoans and appeared to be pathogenic, finally killing the bryozoan host. These findings indicate that fish can transmit the parasite to bryozoans and are an integral part of this parasite's life-cycle.

Keywords

PKDPKXTetracapsuloidesMalacosporeaMyxozoalife-cycle
Type
Research Article
Information
Parasitology , Volume 133 , Issue 6 , December 2006 , pp. 701 - 709
Copyright
2006 Cambridge University Press

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

Anderson, C. L., Canning, E. U. and Okamura, B. ( 1999). Molecular data implicate bryozoans as hosts for PKX (Phylum Myxozoa) and identify a clade of bryozoan parasites within the Myxozoa. Parasitology 199, 555–561.CrossRefGoogle Scholar
Bucke, D., Feist, S. W. and Clifton-Hadley, R. S. ( 1991). The occurrence of proliferative kidney disease (PKD) in cultured and wild fish: further investigations. Journal of Fish Diseases 14, 583–588.CrossRefGoogle Scholar
Canning, E. U., Curry, A., Feist, S. W., Longshaw, M. and Okamura, B. ( 2000). A new class and order of myxozoans to accomodate parasites of bryozoans with ultrastructural observations on Tetracapsula bryosalmonae (PKX organism). Journal of Eukaryotic Microbiology 47, 456–468. doi:10.1111/j.1550-7408.2000.tb00075.xCrossRefGoogle Scholar
Canning, E. U. and Okamura, B. ( 2004). Biodiversity and evolution of the Myxozoa. Advances in Parasitology 56, 43–131.Google Scholar
Canning, E. U., Okamura, B. and Curry, A. ( 1996). Development of a myxosporean parasite Tetracapsula bryozoides gen. n et sp. n in Cristatella mucedo (Bryozoa: Phylactolaemata). Folia Parasitologica 43, 249–261.Google Scholar
Canning, E. U., Tops, S., Currie, A., Wood, T. S. and Okamura, B. ( 2002). Ecology, development and pathogenicity of Buddenbrockia plumatellae Schröder 1910 (Myxozoa, Malacospora) (syn. Tetracapsula bryozoides) and establishment of Tetracapsuloides n. gen. for Tetracapsula bryosalmonae. Journal of Eukaryotic Microbiology 49, 280–295. doi:10.1111/j.1550-7408.2002.tb00371.xCrossRefGoogle Scholar
Chilmonczyk, S. and Monge, D. ( 1999). Flow cytometry as a tool for assessment of the fish cellular immune response to pathogens. Fish and Shellfish Immunology 9, 319–333.CrossRefGoogle Scholar
Clifton-Hadley, R. S. and Feist, S. W. ( 1989). Proliferative kidney disease in brown trout Salmo trutta: further evidence of a myxosporean aetiology. Diseases of Aquatic Organisms 6, 66–103.Google Scholar
Clifton-Hadley, R. S., Richards, R. H. and Bucke, D. ( 1987). Proliferative kidney disease (PKD) in rainbow trout Salmo gairdneri: further observations on the effects of water temperature. Aquaculture 55, 165–171.Google Scholar
de Kinkelin, P. and Loriot, B. ( 2001). A water temperature regime which prevents the occurrence of proliferative kidney disease (PKD) in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 24, 489–493. doi:10.1046/j.1365-2761.2001.00312.xCrossRefGoogle Scholar
Ellis, A. E., McVicar, A. H. and Munro, A. L. S. ( 1985). Proliferative kidney disease in brown trout Salmo trutta L. and Atlantic salmon, Salmo salar L., parr; histopathological and epidemiological observations. Journal of Fish Diseases 8, 447–459.Google Scholar
Feist, S. W. ( 1988). The stickleback (Gasterosteus aculeatus) and PKD in salmonids-culprit or innocent bystander? Bulletin of the European Association of Fish Pathologists 8, 94–96.Google Scholar
Feist, S. W. and Bucke, D. ( 1993). Proliferative kidney disease in wild salmonids. Fisheries Research 17, 51–58. doi:10.1016/0165-7836(93)90006-SCrossRefGoogle Scholar
Feist, S. W., Longshaw, M., Canning, E. U. and Okamura, B. ( 2001). Induction of proliferative kidney disease (PKD) in rainbow trout Onchorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae. Diseases of Aquatic Organisms 45, 61–68.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. doi:10.1046/j.1365-2761.2002.00361.xCrossRefGoogle Scholar
Ferguson, H. W. ( 1981). The effects of water temperature on the development of proliferative kidney disease in rainbow trout, Salmo gairdneri Richardson. Journal of Fish Diseases 4, 175–177.CrossRefGoogle Scholar
Ferguson, H. W. and Needham, E. A. ( 1978). Proliferative kidney disease in rainbow trout Salmo gairdneri Richardson. Journal of Fish Diseases 1, 91–108.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
Hedrick, R. P., Baxa, D. V., de Kinkelin, P. and Okamura, B. ( 2004). Malacosporean-like spores in urine of rainbow trout react with antibody and DNA probes to Tetracapsuloides bryosalmonae. Parasitology Research 92, 81–88. doi: 10.1007/s00436-003-0986-3CrossRefGoogle Scholar
Hedrick, R. P., Kent, M. L. and Toth, R. J. ( 1986). Myxosporeans detected in non-salmonid fishes from waters enzootic for proliferative kidney disease (PKD). Bulletin of the European Association of Fish Pathologists 6, 32–35.Google Scholar
Hedrick, R. P., MacConnell, E. and de Kinkelin, P. ( 1993). Proliferative kidney disease of salmonid fish. Annual Review of Fish Diseases 3, 277–290. doi:10.1016/0959-8030(93)90039-ECrossRefGoogle Scholar
Henderson, M. and Okamura, B. ( 2004). The phylogeography of salmonid proliferative kidney disease in Europe and North America. Proceedings of the Royal Society of London, B 271, 1729–1736. doi:10.1098/rspb.2004.2677CrossRefGoogle Scholar
Kent, M. L. and Hedrick, R. P. ( 1985). Transmission of the causative agent of proliferative kidney disease (PKD) with the blood and spleen of infected fish; further evidence that the PKX parasite belongs to the phylum Myxozoa. Bulletin of the European Association of Fish Pathologists 5, 39–42.Google Scholar
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.Google Scholar
Kent, M. L. and Hedrick, R. P. ( 1987). Effects of cortisol implants on the PKX myxosporean causing proliferative kidney disease in rainbow trout Salmo gairdneri. Journal of Parasitology 73, 455–461.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. doi:10.1577/1548-8667(1998)010<0012: RDSAOI>2.0.CO;2CrossRefGoogle Scholar
Kent, M. L., Khattra, J., Hedrick, R. P. and Devlin, R. H. ( 2000). Tetracapsula renicola n.sp. (Myxozoa: Saccosporidae); the PKX myxozoan-the cause of proliferative kidney disease of salmonid fishes. Journal of Parasitology 86, 103–111.Google Scholar
Kent, M. L., Whitaker, D. J. and Margolis, L. ( 1993). Sphaerospora oncorhynchi n.sp. (Myxosporea: Sphaerosporidae) from the kidney of sockeye salmon (Onchorynchus nerka) in British Columbia and its possible relationship to the myxosporean causing proliferative kidney disease. Canadian Journal of Zoology 71, 2425–2430.Google Scholar
Lom, J. and Dyková, I. ( 2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53, 1–36.CrossRefGoogle Scholar
Longshaw, M., Feist, S. W., Canning, E. U. and Okamura, B. ( 1999). First identification of PKX in bryozoans from the United Kingdom – molecular evidence. Bulletin of the European Association of Fish Pathologists 19, 146–148.Google Scholar
MacConnel, E. and Smith, C. ( 1990). Non-salmonid fish inhabiting a hatchery water supply enzootic for proliferative kidney disease infected with one myxosporean, Myxobilatus spp. Bulletin of the European Association of Fish Pathologists 10, 149–151.Google Scholar
McGurk, C. ( 2005). Culture of malacosporeans (Myxozoa) and development of control strategies for proliferative kidney disease. Ph.D. thesis, Institute of Aquaculture, University of Stirling, UK.
McGurk, C., Morris, D. J., Auchinachie, N. A. and Adams, A. ( 2006). Development of Tetracapsuloides bryosalmonae in bryozoan hosts (as examined by light microscopy) and quantitation of infective dose to rainbow trout (Oncorhynchus mykiss). Veterinary Parasitology 135, 249–257. doi:10.1016/j.vetpar.2005.07.022CrossRefGoogle Scholar
Morris, D. J. and Adams, A. ( 2006 a). Proliferative, presaccular stages of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) within the bryozoan host Fredericella sultana (Bryozoa: Phylactolaemata). Journal of Parasitology (in the Press).Google Scholar
Morris, D. J. and Adams, A. ( 2006 b). Transmission of freshwater myxozoans during the asexual propagation of invertebrate hosts. International Journal for Parasitology 36, 371–377.Google Scholar
Morris, D. J., Adams, A., Feist, S. W., McGeorge, J. and Richards, R. H. ( 2000 a). Immunohistochemical and PCR studies of wild fish for Tetracapsula bryosalmonae (PKX), the causative organism of proliferative kidney disease. Journal of Fish Diseases 23, 129–135. doi:10.1046/j.1365-2761.2000.00227.xCrossRefGoogle Scholar
Morris, D. J., Adams, A. and Richards, R. H. ( 1997). Studies of the PKX parasite in rainbow trout via immunohistochemistry and immunogold electron microscopy. Journal of Aquatic Animal Health 9, 265–273. doi:10.1577/1548-8667. (1997)009<0265:SOTPPI>2.3.CO;2CrossRefGoogle Scholar
Morris, D. J., Adams, A. and Richards, R. H. ( 2000 b). In situ hybridization 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.Google Scholar
Morris, D. J., Ferguson, H. W. and Adams, A. ( 2005). Severe, chronic proliferative kidney disease (PKD) induced in rainbow trout Oncorhynchus mykiss held at a constant 18 °C. Diseases of Aquatic Organisms 66, 221–226.CrossRefGoogle Scholar
Morris, D. C., Morris, D. J. and Adams, A. ( 2002 a). Molecular evidence of release of Tetracapsula bryosalmonae, the causative organism of proliferative kidney disease from infected salmonids into the environment. Journal of Fish Diseases 25, 501–504. doi:10.1046/j.1365-2761.2002.00352.xCrossRefGoogle Scholar
Morris, D. J., Morris, D. C. and Adams, A. ( 2002 b). Development and release of a malacosporean (Myxozoa) from Plumatella repens (Bryozoa: Phylactolaemata). Folia Parasitologica 49, 25–34.Google Scholar
Okamura, B. ( 1996). Occurrence, prevalence and the effects of the myxozoan Tetracapsula bryozoides parasitic in the freshwater bryozoan Cristatella mucedo (Bryozoa: Phylactolaemata). Folia Parasitologica 43, 262–266.Google Scholar
Okamura, B., Anderson, C. L., Longshaw, M., Feist, S. W. and Canning, E. U. ( 2001). Patterns of occurrence and 18ssu rDNA sequence variation of PKX (Tetracapsula bryosalmonae) the causative agent of salmonid Proliferative Kidney Disease. Journal of Parasitology 87, 379–385.CrossRefGoogle Scholar
Okamura, B. and Wood, T. S. ( 2002). Bryozoans as hosts for Tetracapsula bryosalmonae, the PKX organism. Journal of Fish Diseases 25, 469–475. doi:10.1046/j.1365-2761.2002.00376.xCrossRefGoogle Scholar
Seagrave, C. P., Bucke, D. and Alderman, D. J. ( 1980). Ultrastructure of a Haplosporean like organism: the possible causative agent of proliferative kidney disease in rainbow trout. Journal of Fish Biology 16, 453–459.CrossRefGoogle Scholar
Seagrave, C. P., Bucke, D., Hudson, E. B. and McGregor, D. ( 1981). A survey of the prevalence and distribution of proliferative kidney disease in England and Wales. Journal of Fish Diseases 4, 437–439.CrossRefGoogle Scholar
Tops, S., Baxa, D. V., McDowell, T. S., Hedrick, R. P. and Okamura, B. ( 2004). Evaluation of malacosporean life cycles through transmission studies. Diseases of Aquatic Organisms 60, 109–121.CrossRefGoogle Scholar
Tops, S., Curry, A. and Okamura, B. ( 2005). Diversity and systematics of the Malacosporea (Myxozoa). Invertebrate Biology 124, 285–295. doi:10.1111/j.1744-7410.2005.00026.xCrossRefGoogle Scholar
Tops, S. and Okamura, B. ( 2003). Infection of bryozoans by Tetracapsuloides bryosalmonae at sites endemic for salmonid proliferative kidney disease. Diseases of Aquatic Organisms 57, 221–226.CrossRefGoogle Scholar
Tops, S. and Okamura, B. ( 2005). Malacosporean parasites (Myxozoa, Malacosporea) of freshwater bryozoans (Bryozoa, Phylactolaemata): a review. Denisia 28, 287–298.Google Scholar
Voronin, V. N. ( 1993). PKX like organism in common carp during swim-bladder inflammation: further evidence of an association with the myxosporean Sphaerospora renicola. Bulletin of the European Association of Fish Pathologists 13, 127–129.Google Scholar
Wahli, T., Kneusel, R., Bernet, D., Segner, H., Pugovkin, D., Burkhardt-Holm, P., Escher, M. and Scmidt-Posthaus, H. ( 2002). Proliferative kidney disease in Switzerland: current state of knowledge. Journal of Fish Diseases 25, 491–500. doi:10.1046/j.1365-2761.2002.00401.xCrossRefGoogle Scholar