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Cytological and molecular description of Hamiltosporidium tvaerminnensis gen. et sp. nov., a microsporidian parasite of Daphnia magna, and establishment of Hamiltosporidium magnivora comb. nov.


We describe the new microsporidium Hamiltosporidium tvaerminnensis gen. et sp. nov. with an emphasis on its ultrastructural characteristics and phylogenetic position as inferred from the sequence data of SSU rDNA, alpha- and beta-tubulin. This parasite was previously identified as Octosporea bayeri Jírovec, 1936 and has become a model system to study the ecology, epidemiology, evolution and genomics of microsporidia - host interactions. Here, we present evidence that shows its differences from O. bayeri. Hamiltosporidium tvaerminnensis exclusively infects the adipose tissue, the ovaries and the hypodermis of Daphnia magna and is found only in host populations located in coastal rock pool populations in Finland and Sweden. Merogonial stages of H. tvaerminnensis have isolated nuclei; merozoites are formed by binary fission or by the cleaving of a plasmodium with a small number of nuclei. A sporogonial plasmodium with isolated nuclei yields 8 sporoblasts. Elongated spores are generated by the most finger-like plasmodia. The mature spores are polymorphic in shape and size. Most spores are pyriform (4·9–5·6×2·2–2·3 μm) and have their polar filament arranged in 12–13 coils. A second, elongated spore type (6·8–12·0×1·6–2·1 μm) is rod-shaped with blunt ends and measures 6·8–12·0×1·6–2·1 μm. The envelope of the sporophorous vesicle is thin and fragile, formed at the beginning of the sporogony. Cytological and molecular comparisons with Flabelliforma magnivora, a parasite infecting the same tissues in the same host species, reveal that these two species are very closely related, yet distinct. Moreover, both cytological and molecular data indicate that these species are quite distant from F. montana, the type species of the genus Flabelliforma. We therefore propose that F. magnivora also be placed in Hamiltosporidium gen. nov.

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*Corresponding author: University of Basel, Zoological Institute, Vesalgasse 1, 4051 Basel, Switzerland. Tel: +41 (0) 61 267 03 61. Fax: +41 (0) 61 267 03 62. E-mail:
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Altermatt, F., Hottinger, J. W. and Ebert, D. (2007). Parasites promote host gene flow in a metapopulation. Evolutionary Ecology 21, 561575.
Bieger, A. and Ebert, D. (2009). Expression of parasite virulence at different host population densities under natural conditions. Oecologia (Berlin) 160, 247255.
Canning, E. U., Curry, A., Cheney, S. A., Lafranchi-Tristem, N. J., Ebert, D., Refardt, D., Killick-Kendrick, M. and Killick-Kendrick, R. (2001). Flabelliforma montana (Phylum Microsporidia) from Phlebotomus ariasi (Diptera, Psychodidae): ultrastructural observations and phylogenetic relationships. European Journal of Protistology 37, 207221.
Canning, E. U., Killick-Kendrick, R. and Killick-Kendrick, M. (1991). A new microsporidian parasite Flabelliforma montana n.g., n.sp. infecting Phlebotomus ariasi (Diptera, Psychodidae) in France. Journal of Invertebrate Pathology 57, 7181.
Clotilde-Ba, F. L. and Toguebaye, B. S. (1994). Ultrastructure and development of Agmasoma penaei (Microspora, Thelohaniidae) found in Penaeus notialis (Crustacea, Decapoda,Penaeidae) from Senegal. European Journal of Protistology 30, 347353.
Corradi, N., Haag, K. L., Pombert, J. F., Ebert, D. and Keeling, P. J. (2009). Draft genome sequence of the Daphnia pathogen Octosporea bayeri: insights into the gene content of a large microsporidian genome and a model for host-parasite interactions. Genome Biology 10, R106.
Decaestecker, E., Declerck, S., De Meester, L. and Ebert, D. (2005). Ecological implications of parasites in natural Daphnia populations. Oecologia (Berlin) 144, 382390.
Ebert, D. (2005). Ecology, Epidemiology and Evolution of Parasitism in Daphnia,, Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information.
Ebert, D. (2008). Host-parasite coevolution: insights from the Daphnia-parasite model system. Current Opinion in Microbiology 11, 290301.
Ebert, D., Hottinger, J. W. and Pajunen, V. I. (2001). Temporal and spatial dynamics of parasites in a Daphnia metapopulation: which factors explain parasite richness? Ecology 82, 34173434.
Ebert, D., Lipsitch, M. and Mangin, K. L. (2000). The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. American Naturalist 156, 459477.
Green, J. (1957). Parasites and epibionts of Cladocera in rock pools of Tvärminne archipelago. Archivum Societatis Zoologicae Botanicae Fennicae ‘Vanamo’ 12, 512.
Green, J. (1974). Parasites and epibionts of Cladocera. Transactions of the Zoological Society of London 32, 417515.
Hazard, E. I. and Oldacre, S. W. (1975). Revision of Microsporida (Protozoa) close to Thelohania, with descriptions of one new family, eight new genera, and thirteen new species. U.S. Department of Agriculture Technical Bulletin 1530, 1104.
Hostounský, Z. and Žižka, Z. (1979). A modification of the “agar cushion method” for observation and photographic recording microsporidian spores. Journal of Protozoology 26, 41A42A.
James, T. Y., Kauff, F., Schoch, C. L., Matheny, P. B., Hofstetter, V., Cox, C. J., Celio, G., Gueidan, C., Fraker, E., Miadlikowska, J., Lumbsch, H. T., Rauhut, A., Reeb, V., Arnold, A. E., Amtoft, A., Stajich, J. E., Hosaka, K., Sung, G.-H., Johnson, D., O'Rourke, B., Crockett, M., Binder, M., Curtis, J. M., Slot, J. C., Wang, Z., Wilson, A. W., Schüssler, A., Longcore, J. E., O'Donnell, K., Mozley-Standridge, S., Porter, D., Letcher, P. M., Powell, M. J., Taylor, J. W., White, M. M., Griffith, G. W., Davies, D. R., Humber, R. A., Morton, J. B., Sugiyama, J., Rossman, A. Y., Rogers, J. D., Pfister, D. H., Hewitt, D., Hansen, K., Hambleton, S., Shoemaker, R. A., Kohlmeyer, J., Volkmann-Kohlmeyer, B., Spotts, R. A., Serdani, M., Crous, P. W., Hughes, K. W., Matsuura, K., Langer, E., Langer, G., Untereiner, W. A., Lücking, R., Büdel, B., Geiser, D. M., Aptroot, A., Diederich, P., Schmitt, I., Schultz, M., Yahr, R., Hibbett, D. S., Lutzoni, F., McLaughlin, D. J., Spatafora, J. W. and Vilgalys, R. (2006). Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature, London 443, 818822. doi: 10.1038/nature05110
Jírovec, O. (1936). Über einige in Daphnia magna parasitierende Mikrosporidien. Zoologischer Anzeiger 116, 136142.
Larsson, J. I. R. (1988). Identification of Microsporidia genera (Protozoa, Microspora) – a guide with comments on the taxonomy. Archiv für Protistenkunde 136, 137.
Larsson, J. I. R. (1999). Identification of Microsporidia. Acta Protozoologica 38, 161197.
Larsson, J. I. R., Ebert, D., Mangin, K. L. and Vavra, J. (1998). Ultrastructural study and description of Flabelliforma magnivora sp n (Microspora : Duboscqiidae), a microsporidian parasite of Daphnia magna (Crustacea : Cladocera : Daphniidae). Acta Protozoologica 37, 4152.
Larsson, J. I. R., Ebert, D., Vavra, J. and Voronin, V. N. (1996). Redescription of Pleistophora intestinalis Chatton, 1907, a microsporidian parasite of Daphnia magna and Daphnia pulex, with establishment of the genus Glugoides (Microspora, Glugeidae). European Journal of Protistology 32, 251261.
Lass, S. and Ebert, D. (2006). Apparent seasonality of parasite dynamics: analysis of cyclic prevalence patterns. Proceedings of the Royal Society of London, B 273, 199206.
Lee, S. C., Corradi, N., Byrnes III, E. J., Torres-Martinez, S., Dietrich, F. S., Keeling, P. J. and Heitman, J. (2008). Microsporidia evolved from ancestral sexual fungi. Current Biology 18, 15.
Mangin, K. L., Lipsitch, M. and Ebert, D. (1995). Virulence and transmission modes of two microsporidia in Daphnia magna. Parasitology 111, 133142.
Morris, D. J. and Freeman, M. A. (2010). Hyperparasitism has wide-ranging implications for studies on the invertebrate phase of myxosporean (Myxozoa) life cycles. International Journal for Parasitology 40, 357369.
Ormières, R., Baudoin, J., Brugerolle, G. and Pralavorio, R. (1976). Ultrastructure de quelques stades de la Microsporidie Octosporea muscaedomesticae Flu, parasite de Ceratitis capitata (Wiedemann) (Diptère, Trypetidae). Journal of Eukaryotic Microbiology 23, 320328.
Refardt, D., Canning, E. U., Mathis, A., Cheney, S. A., Lafranchi-Tristem, N. J. and Ebert, D. (2002). Small subunit ribosomal DNA phylogeny of microsporidia that infect Daphnia (Crustacea : Cladocera). Parasitology 124, 381389.
Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. The Journal of Cell Biology 17, 208212.
Romeis, B. (1968). Mikroskopische Technik, R. Oldenbourg, München, Germany and Wien, Austria.
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.
Stirnadel, H. A. and Ebert, D. (1997). Prevalence, host specificity and impact on host fecundity of microparasites and epibionts in three sympatric Daphnia species. Journal of Animal Ecology 66, 212222.
Tautz, D., Arctander, P., Minelli, A., Thomas, R. H. and Vogler, A. P. (2003). A plea for DNA taxonomy. Trends in Ecology and Evolution 18, 7074.
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 48764882.
Vávra, J. and Larsson, J. I. R. (1999). Structure of the microsporidia. In The Microsporidia and Microsporidiosis (ed. Wittner, M. and Weiss, L. M.), pp. 7–84. ASM Press, Washington, D.C., USA.
Vizoso, D. B. and Ebert, D. (2004). Within-host dynamics of a microsporidium with horizontal and vertical transmission: Octosporea bayeri in Daphnia magna. Parasitology 128, 3138.
Vizoso, D. B. and Ebert, D. (2005). Mixed inoculations of a microsporidian parasite with horizontal and vertical infections. Oecologia (Berlin) 143, 157166.
Vizoso, D. B., Lass, S. and Ebert, D. (2005). Different mechanisms of transmission of the microsporidium Octosporea bayeri: a cocktail of solutions for the problem of parasite permanence. Parasitology 130, 501509.
Zbinden, M., Haag, C. R. and Ebert, D. (2008). Experimental evolution of field populations of Daphnia magna in response to parasite treatment. Journal of evolutionary Biology 21, 1088–1078.
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