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Experimental transmission of malacosporean parasites from bryozoans to common carp (Cyprinus carpio) and minnow (Phoxinus phoxinus)

Published online by Cambridge University Press:  23 October 2009

D. S. GRABNER
Affiliation:
Fish Medicine and Livestock Management, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine, Veterinärplatz 1, 1210Vienna, Austria
M. EL-MATBOULI*
Affiliation:
Fish Medicine and Livestock Management, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine, Veterinärplatz 1, 1210Vienna, Austria
*
*Corresponding author: Tel: +43 1 250774708. Fax: +43 1 250775192. E-mail: [email protected]

Summary

To address whether a fish host is involved in the life cycles of malacosporeans of the genus Buddenbrockia, cohabitation experiments with different bryozoan and fish species were conducted. Samples were analysed by malacosporean-specific PCR, partial sequencing of the 18S rDNA, and light and electron microscopy. Co-habitation challenges with bryozoans resulted in malacosporean infections detected mainly in the kidney of common carp (Cyprinus carpio) and minnow (Phoxinus phoxinus). Sequences of the minnow parasite and of worm-like Buddenbrockia stages in Plumatella repens were identical and showed 99·5% similarity to Buddenbrockia plumatellae and 96·3% similarity to the sequence obtained from carp. One sample, comprising 4–5 zooids of statoblast-raised bryozoans cohabitated with infected carp was PCR-positive, but no overt infection could be observed in the remaining colony. Light and electron-microscopy of kidney samples of infected minnows revealed single cells within kidney tubules, whereas in carp, sporogonic stages were found in kidney tubules. Phylogenetic analysis of the Buddenbrockia spp. known to date placed the carp-infecting species at the base of the B. plumatellae clade, but low posterior probability makes this node questionable. The present study showed that Buddenbrockia spp. were able to infect cyprinid fish, showing stages in kidney-tubules strikingly similar to those of T. bryosalmonae.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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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
Balon, E. K. (1995). Origin and domestication of the wild carp, Cyprinus carpio: from Roman gourmets to the swimming flowers. Aquaculture 129, 347.CrossRefGoogle Scholar
Bartholomew, J. L., Atkinson, S. D., Hallett, S. L., Lowenstine, L. J., Garner, M. M., Gardiner, C. H., Rideout, B. A., Keel, M. K. and Brown, J. D. (2008). Myxozoan parasitism in waterfowl. International Journal for Parasitology 38, 11991207.CrossRefGoogle ScholarPubMed
Bütschli, O. (1881). Myxosporidien. Zoologisches Jahrbuch 1, 162164.Google 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., Curry, A., Hill, S. L. and Okamura, B. (2007). Ultrastructure of Buddenbrockia allmani n. sp. (Myxozoa, Malacosporea), a parasite of Lophopus crystallinus (Bryozoa, Phylactolaemata). Journal of Eukaryotic Microbiology 54, 247262.CrossRefGoogle Scholar
Canning, E. U. and Okamura, B. (2004). Biodiversity and evolution of the Myxozoa. Advances in Parasitology 56, 43–131.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 (Praha) 43, 249261.Google Scholar
Canning, E. U., Tops, S., Curry, A., Wood, T. S. and Okamura, B. (2002). Ecology, development and pathogenicity of Buddenbrockia plumatellae Schröder, 1910 (Myxozoa, Malacosporea) (syn. Tetracapsula bryozoides) and establishment of Tetracapsuloides n. gen. for Tetracapsula bryosalmonae. Journal of Eukaryotic Microbiology 49, 280295.CrossRefGoogle ScholarPubMed
Eiras, J. C. (2005). An overview on the myxosporean parasites in amphibians and reptiles. Acta Parasitologica 50, 267275.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(1), 6168.CrossRefGoogle ScholarPubMed
Friedrich, C., Ingolic, E., Freitag, B., Kastberger, G., Hohmann, V., Skofitsch, G., Neumeister, U. and Kepka, O. (2000). A myxozoan-like parasite causing xenomas in the brain of the mole Talpa europea L., 1758. Parasitology 121, 483492.CrossRefGoogle 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., MacConnell, E. and de Kinkelin, P. (1993). Proliferative kidney disease of salmonid fish. Annual Review of Fish Diseases 1993, 277290.CrossRefGoogle Scholar
Hill, S. L. and Okamura, B. (2007). Endoparasitism in colonial hosts: patterns and processes. Parasitology 134, 841852.CrossRefGoogle ScholarPubMed
Jiménez-Guri, E., Okamura, B. and Holland, P. W. H. (2007 b). Origin and evolution of a myxozoan worm. Integrative and Comparative Biology 47(5), 752758.CrossRefGoogle ScholarPubMed
Jiménez-Guri, E., Philippe, H., Okamura, B. and Holland, P. W. H. (2007 a). Buddenbrockia is a cnidarian worm. Science 317, 116118.CrossRefGoogle ScholarPubMed
Kallert, D. M., El-Matbouli, M. and Haas, W. (2005). Polar filament discharge of Myxobolus cerebralis actinospores is triggered by combined non-specific mechanical and chemical cues. Parasitology 131, 609616.CrossRefGoogle ScholarPubMed
Keane, T. M., Creevey, C. J., Pentony, M. M., Naughton, T. J. and McInerney, J. O. (2006). Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evolutionary Biology 6, 29.CrossRefGoogle Scholar
Kent, M. L. and Hedrick, R. P. (1986). Development of the PKX myxosporean in rainbow trout Salmo gairdneri. Diseases of Aquatic Organisms 1, 169182.CrossRefGoogle Scholar
Lom, J. and Dykova, I. (2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica (Praha) 53, 136.CrossRefGoogle ScholarPubMed
McGurk, C., Morris, D. J. and Adams, A. (2006). Sequential development of Buddenbrockia plumatellae (Myxozoa: Malacosporea) within Plumatella repens (Bryozoa: Phylactolaemata). Diseases of Aquatic Organisms 73, 159169.CrossRefGoogle ScholarPubMed
Morris, D. J., Morris, D. C. and Adams, A. (2002). Development and release of a malacosporean (Myxoazoa) from Plumatella repens (Bryozoa: Phylactolaemata). Folia Parasitologica (Praha) 49, 2534.CrossRefGoogle Scholar
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. (2008). 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. Parasitology 135, 10751092.CrossRefGoogle ScholarPubMed
Prunescu, C-C., Prunescu, P., Pucek, Z. and Lom, J. (2007). The first finding of myxosporean development from plasmodia to spores in terrestrial mammals: Soricimyxum fegati gen. et sp. n. (Myxozoa) from Sorex araneus (Soricomorpha). Folia Parasitologica (Praha) 54, 159164.CrossRefGoogle Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.CrossRefGoogle ScholarPubMed
Schröder, O. (1910). Buddenbrockia plumatellae, eine neue Mesozoenart aus Plumatella repens L. und Pl. fungosa Pall. Zeitschrift für Wissenschaftliche Zoologie 96, 525537.Google Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.CrossRefGoogle ScholarPubMed
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 25, 48764882.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
Tops, S., Curry, A. and Okamura, B. (2005). Diversity and systematics of the Malacosporea (Myxozoa). Invertebrate Biology 124, 285295.CrossRefGoogle Scholar
Voronin, V. N. (1993). PKX like organism in common carp during swimbladder inflammation: further evidence of an association with the myxosporean Sphaerospora renicola. Bulletin of the European Association of Fish Pathologists 13(4), 127129.Google Scholar
Voronin, V. N. and Chernysheva, N. B. (1993). An intracellular gill parasite as the possible causative agent of mortality during swim-bladder inflammation in common carp, Cyprinus carpio L. Journal of Fish Diseases 16, 609611.CrossRefGoogle Scholar
Wood, T. S. and Okamura, B. (2005). A New Key to the Freshwater Bryozoans of Britain, Ireland and Continental Europe with Notes on their Ecology. Published by the Freshwater Biology Association, Scientific Publication No. 63, Cumbria.Google Scholar