Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-22T20:05:51.484Z Has data issue: false hasContentIssue false

Sporogony of Tetracapsuloides bryosalmonae in the brown trout Salmo trutta and the role of the tertiary cell during the vertebrate phase of myxozoan life cycles

Published online by Cambridge University Press:  13 June 2008

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
*
*Corresponding author. Tel: +44 1786 466582. Fax: +44 1786 473122. E-mail: [email protected]

Summary

Tetracapsuloides bryosalmonae is the myxozoan that causes the commercially and ecologically important proliferative kidney disease of salmonid fish species. Immunohistochemistry and electron microscopy were used to examine the development of this parasite within the kidney of the brown trout Salmo trutta. The main replicative phase of T. bryosalmonae is a cell doublet composed of a primary cell and a single secondary cell. Engulfment of one secondary cell by another to form a secondary-tertiary doublet (S-T doublet) heralded the onset of sporogony whereupon the parasite migrated to the kidney tubule lumen. Within the tubule, the parasite transformed into a pseudoplasmodium and anchored to the tubule epithelial cells via pseudopodial extensions. Within each pseudoplasmodium developed a single spore, composed of 4 valve cells, 2 polar capsules and 1 sporoplasm. The pseudoplasmodia formed clusters suggesting that large numbers of spores develop within the fish. This examination of T. bryosalmonae suggests that the main replicative phase of freshwater myxozoans within vertebrates is via direct replication of cell doublets rather than through the rupturing of extrasporogonic stages, while tertiary cell formation relates only to sporogony. Taken in conjunction with existing phylogenetic data, 5 distinct sporogonial sequences are identified for the Myxozoa.

Type
Original Articles
Copyright
Copyright © 2008 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 119, 555561.CrossRefGoogle ScholarPubMed
Baska, F. and Molnár, K. (1988). Blood stages of Sphaerospora spp. (Myxosporea) in cyprinid fishes. Diseases of Aquatic Organisms 5, 2328.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, 583588.CrossRefGoogle Scholar
Canning, E. U., Curry, A., Feist, S. W., Longshaw, M. and Okamura, B. (2000). A new class and order of myxozoans to accommodate parasites of bryozoans with ultrastructural observations on Tetracapsula bryosalmonae (PKX organism). Journal of Eukaryotic Microbiology 47, 456468.CrossRefGoogle ScholarPubMed
Canning, E. U. and Okamura, B. (2004). Biodiversity and evolution of the Myxozoa. Advances in Parasitology 56, 43131.CrossRefGoogle ScholarPubMed
Canning, E. U., Okamura, B. and Curry, A. (1996). Development of a myxozoan parasite Tetracapsula bryozoides gen. n. et sp. n. in Cristatella mucedo (Bryozoa: Phylactolaemata). Folia Parasitologica 43, 249261.Google Scholar
Castagnaro, M., Marin, M., Ghittino, C. and Hedrick, R. P. (1991). Lectin histochemistry and ultrastructure of rainbow trout Oncorhynchus mykiss kidneys affected by proliferative kidney disease. Diseases of Aquatic Organisms 10, 173183.CrossRefGoogle Scholar
Clifton-Hadley, R. S., Bucke, D. and Richards, R. H. (1987). A study of the sequential clinical and pathological changes during proliferative kidney disease in rainbow trout, Salmo gairdneri Richardson. Journal of Fish Diseases 10, 335352.CrossRefGoogle Scholar
Clifton-Hadley, R. S. and Feist, S. W. (1989). Proliferative kidney disease in brown trout Salmo trutta – further evidence of a myxosporean etiology. Diseases of Aquatic Organisms 6, 99103.CrossRefGoogle Scholar
Csaba, G., Kovács-Gayer, E., Békési, L., Bucsek, M. and Molnár, K. (1984). Studies into the possible protozoan aetiology of swimbladder inflammation in carp fry. Journal of Fish Diseases 7, 3956.CrossRefGoogle Scholar
Current, W. L. and Janovy, J. (1977). Sporogenesis in Henneguya exilis infecting the channel catfish: an ultrastructural study. Protistologica 13, 157167.Google Scholar
Diamant, A., Whipps, C. M. and Kent, M. L. (2004). A new species of Sphaeromyxa (Myxosporea: Sphaeromyina: Sphaeromyxidae) in Devil Firefish, Pterois miles (Scorpaenidae), from the Northern Red Sea: Morphology, ultrastructure, and phylogeny. Journal of Parasitology 90, 14341442.CrossRefGoogle ScholarPubMed
Dyková, I. and Lom, J. (1988). Chloromyxum reticulatum (Myxozoa, Myxosporea) in the liver of Burbot (Lota lota L.) and its migration to the final site of infection. European Journal of Protistology 23, 258261.CrossRefGoogle Scholar
El-Matbouli, M., Hoffmann, R. W. and Madnok, C. (1995). Light and electron microscopic observations on the route of the triactinomyxon-sporoplasm of Myxobolus cerebralis from epidermis into rainbow trout cartilage. Journal of Fish Biology 46, 919935.Google Scholar
El-Matbouli, M. and Hoffmann, R. W. (1996). Light and electron microscopic descriptions of Sphaerospora coregoni El-Matbouli, Hoffmann and Kern, 1995 (Myxosporea: Sphaerosporidae) from the kidney of whitefish (Coregonus lavaretus). European Journal of Protistology 32, 389398.CrossRefGoogle Scholar
Eszterbauer, E. and Székely, C. (2004). Molecular phylogeny of the kidney-parasitic Sphaerospora renicola from common carp (Cyprinus carpio) and Sphaerospora sp. from goldfish (Carassius auratus auratus). Acta Veterinaria Hungarica 52, 469478.CrossRefGoogle ScholarPubMed
Feist, S. W. and Bucke, D. (1987). Ultrastructural aspects of PKX, the causative agent of proliferative kidney disease in rainbow trout, Salmo gairdneri Richardson. Journal of Fish Diseases 10, 323327.CrossRefGoogle Scholar
Feist, S. W. and Bucke, D. (1993). Proliferative kidney disease in wild salmonids. Fisheries Research 17, 5158.CrossRefGoogle Scholar
Feist, S. W. and Longshaw, M. (2006). Phylum Myxozoa. In Fish Diseases and Disorders Vol. 1. Protozoan and Metazoan Infections, 2nd Edn (ed. Woo, P. T. K.), pp. 362383. CAB International, Wallingford, UK.Google Scholar
Feist, S. W., Longshaw, M., Canning, E. U. and Okamura, B. (2001). Induction of proliferative kidney disease (PKD) in rainbow trout Oncorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae. Diseases of Aquatic Organisms 45, 6168.CrossRefGoogle ScholarPubMed
Ferguson, H. W. and Needham, E. A. (1978). Proliferative kidney disease in rainbow trout Salmo gairdneri Richardson. Journal of Fish Diseases 1, 91108.CrossRefGoogle Scholar
Fiala, I. (2006). The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology 36, 15211534.CrossRefGoogle ScholarPubMed
Foott, J. S., Stone, R. and Nichols, K. (2007). Proliferative kidney disease (Tetracapsuloides bryosalmonae) in Merced River Hatchery juvenile Chinook salmon: Mortality and performance impairment in 2005 smolts. California Fish and Game 93, 5776.Google Scholar
Grabner, D. S. and El-Matbouli, M. (2008). Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) to Fredericella sultana (Bryozoa: Phylactolaemata) by various fish species. Diseases of Aquatic Organisms 79, 133139.CrossRefGoogle ScholarPubMed
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, 8188.Google ScholarPubMed
Hedrick, R. P., MacConnell, E. and de Kinkelin, P. (1993). Proliferative kidney disease of salmonid fish. Annual Review of Fish Diseases 1, 277290.CrossRefGoogle Scholar
Hedrick, R. P., McDowell, T. and Groff, J. M. (1990). Sphaerospora ictulari n.sp. (Myxosporea: Sphaerosphoridae) observed in the kidney of channel catfish, Ictalurus punctatus Rafinesque. Journal of Protozoology 37, 107112.CrossRefGoogle ScholarPubMed
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, 17291736.CrossRefGoogle ScholarPubMed
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 hybridisation technique. Journal of Fish Diseases 26, 647655.CrossRefGoogle Scholar
Jirků, M., Fiala, I. and Modry, D. (2007). Tracing the genus Sphaerospora: rediscovery, redescription and phylogeny of the Sphaerospora ranae (Morelle, 1929) n.comb. (Myxosporea, Sphaerosporidae), with emendation of the genus Sphaerospora. Parasitology 134, 17271739.CrossRefGoogle ScholarPubMed
Kaup, F. J., Kuhn, E. M. and Körting, W. (1995). Light microscopic and electron microscopic studies on the sporogenesis of Sphaerospora molnari in the gill lamellas of the common carp (Cyprinus carpio). Berliner und Münchener Tierarztliche Wochenschrift 6, 206214.Google Scholar
Kent, M. L., Andree, K. B., Bartholomew, J. L., El-Matbouli, M., Desser, S. S., Devlin, R. H., Feist, S. W., Hedrick, R. P., Hoffmann, R. W., Khattra, J., Hallett, S. L., Lester, R. J. G., Longshaw, M., Palenzuela, O., Siddall, M. E. and Xiao, C. (2001). Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology 48, 395413.CrossRefGoogle ScholarPubMed
Kent, M. L. and Hedrick, R. P. (1985). PKX, the causative agent of proliferative kidney disease (PKD) in Pacific salmonid fishes and its affinities with the Myxozoa. Journal of Protozoology 32, 254260.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, 159182.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, 455461.CrossRefGoogle ScholarPubMed
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, 103111.Google ScholarPubMed
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, 1213.2.0.CO;2>CrossRefGoogle Scholar
Kpatcha, T. K., Diebakate, C., Faye, N. and Toguebaye, B. S. (1999). Light and electron microscopic observations on Kudoa boopsi sp.n. (Myxosporea: Kudoidae), a gill parasite of Boops boops (Pisces: Teleostei: Sparidae) from coasts of Senegal (West Africa). Acta Protozoologica 38, 317321.Google Scholar
Leino, R. L. (1996). Reaction of rodlet cells to a myxosporean infection in the kidney of the bluegill, Lepornis macrohirus. Canadian Journal of Zoology 74, 217225.CrossRefGoogle Scholar
Lom, J. and Dyková, I. (1986). Comments on myxosporean life cycles. Symposia Biologica Hungarica 32, 309318.Google Scholar
Lom, J. and Dyková, I. (1988). Sporogenesis and spore structure in Kudoa lunata (Myxosporea, Multivalvulida). Parasitology Research 74, 521530.CrossRefGoogle ScholarPubMed
Lom, J. and Dyková, I. (1992). Protozoan Parasites of Fishes. Elsevier, Amsterdam.Google Scholar
Lom, J. and Dyková, I. (2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 58, 136.CrossRefGoogle Scholar
Lom, J., Dyková, I. and Lhotáková, Š. (1982). Fine structure of Sphaerospora renicola Dyková and Lom, 1982 a myxosporean from carp kidney and comments on the origins of pansporoblasts. Protistologica 13, 489502.Google Scholar
Lom, J., Dyková, I. and Pavlásková, M. (1983 a). ‘Unidentified’ mobile protozoans from the blood of carp and some unsolved problems of myxosporean life cycles. Journal of Protozoology 30, 497508.CrossRefGoogle Scholar
Lom, J., Körting, W. and Dyková, I. (1983 b). Light and electron microscope redescription of Sphaerospora tincae, Plehn, 1925 and S. galinae Evlanov, 1981 (Myxosporea) from the Tench Tinca tinca L. Protistologica 21, 487493.Google Scholar
Lom, J., Dyková, I., Pavlásková, M. and Grupcheva, G. (1983 c). Sphaerospora molnari sp.nov. (Myxozoa: Myxosporea), an agent of gill, skin and blood sphaerosporosis of common carp in Europe. Parasitology 86, 520535.CrossRefGoogle Scholar
Lom, J., Pavlásková, M. and Dyková, I. (1985). Notes on kidney infecting species of the genus Spherospora Theolan (Myxosporea), including a new species of Sphaerospora gobionis sp. nov. and on myxosporean life-cycle stages in the blood of some freshwater fish. Journal of Fish Diseases 8, 221232.CrossRefGoogle Scholar
Longshaw, M., le Deuff, R. M., Harris, A. F. and Feist, S. W. (2002). Development of proliferative kidney disease in rainbow trout, Oncorhynchus mykiss (Walbaum) following short term exposure to Tetracapsula bryosalmonae infected bryozoans. Journal of Fish Diseases 25, 307310.CrossRefGoogle Scholar
MacConnell, E., Smith, C. E., Hedrick, R. P. and Speer, C. A. (1989). Cellular inflammatory response of rainbow trout to the protozoan parasite that causes proliferative kidney disease. Journal of Aquatic Animal Health 1, 108118.2.3.CO;2>CrossRefGoogle Scholar
McGeorge, J., Sommerville, C. and Wootten, R. (1994). Light and electron microscope observations on extrasporogonic and sporogonic stages of a myxosporean parasite of the genus Sphaerospora Thélohan, 1892 from Atlantic salmon, Salmo salar L. in Scotland. Journal of Fish Diseases 17, 227238.CrossRefGoogle Scholar
Mitchell, L. J. (1978). Myxosporidian infections in some fishes of Iowa. Journal of Protozoology 25, 100105.CrossRefGoogle Scholar
Molnár, K. (1988). Presporogonic development of Sphaerospora renicola Dyková and Lom, 1982, in the swimbladder of the common carp, Cyprinus carpio L. Journal of Fish Diseases 11, 489497.CrossRefGoogle Scholar
Molnár, K. (2007). Site preference of myxozoans in the kidneys of Hungarian fishes. Diseases of Aquatic Organisms 78, 4553.CrossRefGoogle ScholarPubMed
Moran, J. D. W., Margolis, L., Webster, J. M. and Kent, M. L. (1999). Development of Kudoa thyrsites (Myxozoa: Myxosporea) in netpen-reared Atlantic salmon determined by light microscopy and a polymerase chain reaction test. Diseases of Aquatic Organisms 37, 185193.CrossRefGoogle Scholar
Morris, D. C., Morris, D. J. and Adams, A. (2002). Molecular evidence of release of Tetracapusla bryosalmonae the causative organism of proliferative kidney disease from infected salmonids into the environment. Journal of Fish Diseases 25, 501504.CrossRefGoogle Scholar
Morris, D. J. and Adams, A. (2004). Localisation of carbohydrate terminals on Tetracapsuloides bryosalmonae using lectin histochemistry and immunogold electron microscopy. Journal of Fish Diseases 27, 3745.CrossRefGoogle ScholarPubMed
Morris, D. J. and Adams, A. (2006). Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea), the causative organism of salmonid proliferative kidney disease to the freshwater bryozoan, Fredericella sultana. Parasitology 133, 701709.CrossRefGoogle Scholar
Morris, D. J. and Adams, A. (2007). Sacculogenesis and sporogony of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) within the bryozoan host Fredericella sultana (Bryozoa: Phylactolaemata). Parasitology Research 101, 983992.CrossRefGoogle 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, 265273.2.3.CO;2>CrossRefGoogle Scholar
Morris, D. J., Adams, A. and Richards, R. H. (2000 a). Observations on the electron dense bodies of the PKX parasite, agent of proliferative kidney disease in salmonids. Diseases of Aquatic Organisms 39, 201209.CrossRefGoogle ScholarPubMed
Morris, D. J., Adams, A. and Richards, R. H. (2000 b). 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, 950956.CrossRefGoogle Scholar
Morris, D. J., Molnar, K., Longshaw, M. and Adams, A. (2006). Immunostaining of spores and plasmodia of disparate myxozoan genera with comments on the properties of the sporular mucus envelope. Parasitology 132, 781790.CrossRefGoogle ScholarPubMed
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, 454459.CrossRefGoogle Scholar
Sitjà-Bobadilla, A. and Alvarez-Pellitero, P. (1993). Ultrastructural and cytochemical observations on the sporogenesis of Sphaerospora testicularis (Protozoa, Myxosporea) from Mediterranean sea bass Dicentrachus labrax (L.). European Journal of Protistology 29, 219229.CrossRefGoogle Scholar
Sitjà-Bobadilla, A., Palenzeula, O. and Alvarez-Pellitero, P. (1995). Ceratomyxa sparusaurati n.sp. (Myxosporea: Bivalvulida), a new parasite from cultured gilthead seabream (Sparus aurata L.) (Teleostei: Sparidae): Light and electron microscopic description. Journal of Eukaryotic Microbiology 42, 529539.CrossRefGoogle Scholar
Smith, C. E., Morrison, J. K., Ramsey, H. W. and Ferguson, H. W. (1984). Proliferative kidney disease – first reported outbreak in North America. Journal of Fish Diseases 7, 207216.CrossRefGoogle Scholar
Stehr, C. (1986). Sporogenesis of the myxosporean Kudoa paniformis Kabata and Whitaker, 1981 infecting the muscle of the Pacific whiting, Merluccius productus (Ayres): an ultrastructural study. Journal of Fish Diseases 9, 505517.CrossRefGoogle Scholar
Sterud, E., Forseth, T., Ugedal, O., Poppe, T. T., Jorgensen, A., Bruheim, T., Fjeldstad, H-P. and Mo, T. A. (2007). Severe mortality in wild Atlantic salmon Salmo salar due to proliferative kidney disease (PKD) caused by Tetracapsuloides bryosalmonae (Myxozoa). Diseases of Aquatic Organisms 77, 191198.CrossRefGoogle ScholarPubMed
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, 109121.CrossRefGoogle ScholarPubMed
Wahli, T., Bernet, D., Segner, H., Pugovkin, D., Burkhardt-Holm, P., Escher, M. and Schmidt-Posthaus, H. (2002). Proliferative kidney disease in Switzerland: current state of knowledge. Journal of Fish Diseases 25, 491500.CrossRefGoogle Scholar
Whipps, C. M., Grossel, G., Adlard, R. D., Yokoyama, H., Bryant, M. S., Munday, B. L. and Kent, M. L. (2004) Phylogeny of the multivalvulidae (Myxozoa, Myxosporea) based on comparative ribosomal DNA sequence analysis. Journal of Parasitology 90, 618622.CrossRefGoogle ScholarPubMed
Xiao, C. X. and Desser, S. S. (2000). Cladistic analysis of myxozoan species with known alternating life-cycles. Systematic Parasitology 46, 8191.CrossRefGoogle ScholarPubMed
Yamamoto, T. and Saunders, J. E. (1979). Light and electron microscopic observations of sporogenesis in the myxosporidian, Ceratomyxa shasta (Noble, 1950). Journal of Fish Diseases 2, 411428.CrossRefGoogle Scholar
Yokoyama, H., Ogawa, K. and Wakabayashi, H. (1990). Light and electron microscopic studies on the development of Hoferellus carassi (Myxosporea), the causative organism of kidney enlargement disease of goldfish. Fish Pathology 25, 149156.CrossRefGoogle Scholar