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

  • D. S. GRABNER (a1) and M. EL-MATBOULI (a1)

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.

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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.
Balon, E. K. (1995). Origin and domestication of the wild carp, Cyprinus carpio: from Roman gourmets to the swimming flowers. Aquaculture 129, 347.
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.
Bütschli, O. (1881). Myxosporidien. Zoologisches Jahrbuch 1, 162164.
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.
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.
Canning, E. U. and Okamura, B. (2004). Biodiversity and evolution of the Myxozoa. Advances in Parasitology 56, 43–131.
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.
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.
Eiras, J. C. (2005). An overview on the myxosporean parasites in amphibians and reptiles. Acta Parasitologica 50, 267275.
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.
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.
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.
Hedrick, R. P., MacConnell, E. and de Kinkelin, P. (1993). Proliferative kidney disease of salmonid fish. Annual Review of Fish Diseases 1993, 277290.
Hill, S. L. and Okamura, B. (2007). Endoparasitism in colonial hosts: patterns and processes. Parasitology 134, 841852.
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.
Jiménez-Guri, E., Philippe, H., Okamura, B. and Holland, P. W. H. (2007 a). Buddenbrockia is a cnidarian worm. Science 317, 116118.
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.
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.
Kent, M. L. and Hedrick, R. P. (1986). Development of the PKX myxosporean in rainbow trout Salmo gairdneri. Diseases of Aquatic Organisms 1, 169182.
Lom, J. and Dykova, I. (2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica (Praha) 53, 136.
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.
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.
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.
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.
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.
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.
Schröder, O. (1910). Buddenbrockia plumatellae, eine neue Mesozoenart aus Plumatella repens L. und Pl. fungosa Pall. Zeitschrift für Wissenschaftliche Zoologie 96, 525537.
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.
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.
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.
Tops, S., Curry, A. and Okamura, B. (2005). Diversity and systematics of the Malacosporea (Myxozoa). Invertebrate Biology 124, 285295.
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.
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.
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.
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