Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-24T16:04:44.608Z Has data issue: false hasContentIssue false

Fine structure of Metchnikovella incurvata Caullery and Mesnil 1914 (microsporidia), a hyperparasite of gregarines Polyrhabdina sp. from the polychaete Pygospio elegans

Published online by Cambridge University Press:  28 February 2013

Y. Y. SOKOLOVA*
Affiliation:
Institute of Cytology, Russian Academy of Sciences, St. Petersburg, Russia Department of Comparative Biomedical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA, USA
G. G. PASKEROVA
Affiliation:
Department of Invertebrate Zoology, St. Petersburg State University, St. Petersburg, Russia
Y. M. ROTARI
Affiliation:
Institute of Ecology of the Volga River Basin RAS, Togliatti, Russia
E. S. NASSONOVA
Affiliation:
Institute of Cytology, Russian Academy of Sciences, St. Petersburg, Russia Department of Invertebrate Zoology, St. Petersburg State University, St. Petersburg, Russia
A. V. SMIRNOV
Affiliation:
Department of Invertebrate Zoology, St. Petersburg State University, St. Petersburg, Russia
*
*Corresponding author. Microscopy Center, Department of Comparative Biomedical Sciences, School of Veterinary Medicine, Louisiana State University, 1909 Skip Bertman Drive, Baton Rouge, LA 70803, USA. Fax: 225 578 9899. E-mail: [email protected]

Summary

Class Rudimicrosporea Sprague 1977, with its single family Metchnikovellidae, comprises hyperparasites of gregarines from the guts of marine invertebrates. Metchnikovellids remain poorly studied in spite of their significance to the evolutionary history of microsporidia; their ultrastructure and life cycles require further investigation. Here we present results of the light- and electron-microscopy study of Metchnikovella incurvata Caulleri and Mesnil 1914, isolated from lecudinid gregarines, parasitizing polychaetes Pygospio elegans in the White Sea littoral zone, and yet described only on the light-microscopic level. The life cycle of this microsporidium includes 2 sporogonies: free (FS) and sac-bound (SBS). In FS, sporonts develop into multinuclear cells (sporogonial plasmodia), which generate sporoblasts and free spores residing in direct contact with the host cytoplasm. Electron microscopy revealed their metchnikovellidean structure: a horseshoe-shaped nucleus, short manubrium perpendicular to the long axis of the spore, and a polar cap in a separate membrane container. Merogony was not observed. The earliest stages of SBS were chains of binucleate cells. They underwent a series of nuclear and cell divisions, produced extracellular envelopes, and split into boomerang-shaped spore sacs, containing up to 16 spores each. Ultrastructure and sizes of sac-bounded spores were similar to those of free-living ones. An amended diagnosis of M. incurvata is provided.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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

Azevedo, C., Casal, G. and Montes, J. (2008). Ultrastructural developmental cycle of Haplosporidium montforti (Phylum Haplosporidia) in its farmed abalone host, Haliotis tuberculata (Gastropoda). Journal of Parasitology 94, 137142.CrossRefGoogle ScholarPubMed
Becnel, J. J. and Andreadis, T. G. (1999). Microsporidia in insects. In The Microsporidia and Microsporidiosis (ed. Wittner, M. and Weiss, L. M.), pp. 447501. American Society of Microbiology, Washington, DC., USA.Google Scholar
Beard, C. B., Butler, J. F. and Becnel, J. J. (1990). Nolleria pulicis n. gen, n. sp. (Microsporidia, Chytridiopsidae), a microsporidian parasite of the cat flea, Ctenocephalides felis (Siphonaptera, Pulicidae). Journal of Protozoology 37, 9099.CrossRefGoogle Scholar
Beznoussenko, G. V., Dolgikh, V. V., Seliverstova, E. V., Semenov, P. B., Tokarev, Y. S., Trucco, A., Micaroni, M., Di Giandomenico, D., Auinger, P., Senderskly, I. V., Skarlato, S. O., Snigirevskaya, E. S., Komissarchik, Y. Y., Pavelka, M., De Matteis, M. A., Luini, A., Sokolova, Y. Y. and Mironov, A. A. (2007). Analogs of the Golgi complex in microsporidia: structure and avesicular mechanisms of function. Journal of Cell Science 120, 12881298.CrossRefGoogle ScholarPubMed
Caullery, M. and Mesnil, F. (1897). Sur un type nouveau (Metchnikovella n.g.) d'organismes parasites des Grégarines. Comptes Rendus de Seances de la Societe de Biologie, Paris 49, 960962.Google Scholar
Caullery, M. and Mesnil, F. (1914). Sur les Metchnikovellidae et autre Protistes des Grégarines d'Annélides. Comptes Rendus de Seances de la Societe de Biologie, Paris 77, 527532.Google Scholar
Caullery, M. and Mesnil, F. (1919). Metchnikovellidae et autre Protistes des Grégarines d'Annélides. Annales de l'Institut Pasteur 33, 209240.Google Scholar
Dauvin, J.-C., Dewarumez, J.-M. and Gentil, F. (2003). Liste actualisée des espèces d'Annélides Polychètes présentes en Manche. Cahiers de Biologie Marine 44, 6795.Google Scholar
Desportes, I. and Théodoridès, J. (1979). Étude ultrastructurale d'Amphiamblus laubieri n.sp. (Microsporidie, Metchnikovellidae) parasite d'un Grégarine (Lecudina sp.) d'un Echiurien abyssal. Protistologica 15, 435457.Google Scholar
Dubey, J. P. (2007). The history and life cycles of Toxoplasma gondii. In Toxoplasma gondii. The Model Apicomplexan: Perspectives and Methods (ed. Weiss, L. M. and Kim, K.), pp. 119. Academic Press, New York, USA.Google Scholar
Feist, S. W., Hine, P. M., Bateman, K. S., Stentiford, G. D. and Longshaw, M. (2009). Paramarteilia canceri sp. n. (Cercozoa) in the European edible crab (Cancer pagurus) with a proposal for the revision of the order Paramyxida Chatton, 1911. Folia Parasitologica 56, 7385.CrossRefGoogle Scholar
Hildebrand, H. (1974). Observations ultrastructurales sur le stade plasmodial de Metchnikovella wohlfarthi Hildebrand et Vivier 1971, microsporidie hyperparasite de la grégarine Lecudina tuzetae. Protistologica 10, 515.Google Scholar
Hildebrand, H. and Vivier, E. (1971). Observations ultrastructurales sur le sporoblaste de Metchnikovella wohlfarthi, n.sp. (Microsporidies), parasite de la grégarine Lecudina tuzetae. Protistologica 7, 131139.Google Scholar
Larsson, J. I. R. (1993). Description of Chytridiopsis trichopterae n. sp. (Microspora, Chytridiopsidae), a microsporidian parasite of the caddis fly Polycentropus flavomaculatus (Trichoptera, Polycentropodidae), with comments on relationships between families Chytridiopsidae and Metchnikovellidae. Journal of Eukaryotic Microbiology 40, 3748.CrossRefGoogle Scholar
Larsson, J. I. R. (2000). The hyperparasitic microsporidium Amphiacantha longa Caullery et Mesnil, 1914 (Microspora: Metchnikovellidae). Description of the cytology, redescription of the species, emended diagnosis of the genus Amphiacantha and establishment of the new family Amphiacanthidae. Folia Parasitologica 47, 241256.CrossRefGoogle ScholarPubMed
Larsson, R. and Køie, M. (2006). The ultrastructure and reproduction of Amphiamblys capitellides (Microspora, Metchnikovellidae), a parasite of the gregarine Ancora sagittata (Apicomplexa, Lecudinidae), with redescription of the species and comments on the taxonomy. European Journal of Protistology 42, 233248.CrossRefGoogle ScholarPubMed
Leander, B. S. (2007). Marine gregarines: evolutionary prelude to the apicomplexan radiation? Trends in Parasitology 24, 6067.CrossRefGoogle Scholar
Lohr, J. N., Laforsch, C., Koerner, H. and Wolinska, J. (2010). A daphnia parasite (Caullerya mesnili) constitutes a new member of the ichthyosporea, a group of protists near the animal-fungi divergence. Journal of Eukaryotic Microbiology 57, 328336.CrossRefGoogle ScholarPubMed
Nassonova, E., Gorbunov, A., Naumov, A., Issi, I. and Smirnov, A. (2011). Molecular phylogeny of Bertramia asperospora, a protozoan rotifer parasite with obscure taxonomic position: shuffling cards in favor of ichthyosporeans. In VI European Congress of Protistology, Berlin, 24–29 July 2011, pp. 92.Google Scholar
Ormières, R., Loubès, C. and Maurand, J. (1981). Amphyamblys bhatiellae n. sp., microsporidie parasite de Bhatiella marphysae Setna, 1931, Eugrégarine d'Annélide Polychète. Protistologica 17, 273280.Google Scholar
Perkins, F. O., Barta, J. R., Clopton, R. E., Peirce, M. A. and Upton, S. J. (2000). Phylum Apicomplexa. In The Illustrated Guide to the Protozoa (ed. Lee, J. J., Leedale, G. F. and Bradbury, P.), Vol. 1, pp. 190369. Society of Protozoologists, Lawrence, KS, USA.Google Scholar
Radek, R. and Herth, W. (1999). Ultrastructural investigation of the spore-forming protist Nephridiophaga blattellae in the Malpighian tubules of the German cockroach Blattella germanica. Parasitology Research 85, 216231.CrossRefGoogle ScholarPubMed
Rotari, Y. M. (1988). Microsporidia – hyperparasites of the White Sea polychaetes. M.S. dissertation. Biological Sciences, Department of Invertebrate Zoology, Leningrad State University, Leningrad USSR.Google Scholar
Rotari, Y. and Paskerova, G. (2007). New data on hyperparasitic microsporidians from polychaetes of the White Sea. In Proceedings of the V European Congress of Protistology and XI European Conference on Ciliate Biology, St. Petersburg. Protistology 5, 6768.Google Scholar
Simdianov, T., Yudina, V. and Aleoshin, V. (2009). First data on molecular phylogeny of microsporidian family Metchnikovellidae. In Proceedings of the XIII International Congress of Protistology, Armacao dos Buzios, Brasil, p. 144.Google Scholar
Sokolova, Y. and Mironov, A. (2008). Structure and function of the Golgi organelle in parasitic protists. In The Golgi Apparatus: State of the Art 110 Years after Camillo Golgi's Discovery (ed. Mironov, A. and Pavelka, M.), pp. 647674. Springer, Wien, Austria and New York, USA.CrossRefGoogle Scholar
Sokolova, Y., Snigirevskaya, E., Morzhina, E., Skarlato, S., Mironov, A. and Komissarchik, Y. (2001). Visualization of early Golgi compartments at proliferate and sporogenic stages of a microsporidian Nosema grylli. Journal of Eukaryotic Microbiology 86S87S.Google ScholarPubMed
Sprague, V. (1977). Classification and phylogeny. In Comparative Pathobiology, Vol. 2. Systematics of the Microsporidia (ed. Bulla, L. A. and Cheng, T. C.), pp. 130. Plenum Press, New York, USA.Google Scholar
Sprague, V., Becnel, J. J. and Hazard, E. I. (1992). Taxonomy of phylum microspora. Critical Reviews in Microbiology 18, 285395.CrossRefGoogle ScholarPubMed
Takvorian, P. M. and Cali, A. (1994). Enzyme histochemical identification of the Golgi apparatus in the microsporidian Glugea stephani. Journal of Eukaryotic Microbiology 41, 63S64S.Google ScholarPubMed
Tuzet, O. and Ormières, R. (1962). Grégarines de Roscoff. Cahiers de Biologie Marine 3, 289306.Google Scholar
Vavra, J. and Larsson, J. I. R. (1999). Structure of the Microsporidia. In The Microsporidia and Microsporidiosis (ed. Wittner, M. and Weiss, L. M.), pp. 784. American Society of Microbiology, Washington, DC., USA.Google Scholar
Vivier, E. (1965). Étude, au microscope électronique, de la spore de Metchnikovella hovassei n. sp.: appartenance des Metchnikovellidae aux Microsporidies. Comptes Rendus de Seances de la Societe de Biologie, Paris 260, 69826984.Google Scholar
Vivier, E. (1975). The microsporidia of the Protozoa. Protistologica 11, 345361.Google Scholar
Vivier, E. and Schrével, J. (1973). Étude en microscopie photonique et électronique de différents stades du cycle de Metchnikovella hovassei et observations sur la position systématique des Metchnikovellidae. Protistologica 9, 95118.Google Scholar
Weidner, E., Byrd, W., Scarborough, A., Pleshinger, J. and Sibley, D. (1984). Microsporidian spore discharge and the transfer of polaroplast organelle membrane into plasma membrane. Journal of Protozoology 31, 195198.CrossRefGoogle Scholar
Weidner, E., Manale, S. B., Halonen, S. K. and Lynn, J. W. (1994). Microsporidian spore invasion tubes as revealed by fluorescent probes. Biological Bulletin 187, 255256.CrossRefGoogle ScholarPubMed
Weiser, J. (1977). Contribution to the classification of Microsporidia. Acta Societatis Zoologicae Bohemoslovenicae 41, 308320.Google Scholar