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Cucumispora dikerogammari n. gen. (Fungi: Microsporidia) infecting the invasive amphipod Dikerogammarus villosus: a potential emerging disease in European rivers

Published online by Cambridge University Press:  21 September 2009

M. O. OVCHARENKO ,
K. BACELA ,
T. WILKINSON ,
J. E. IRONSIDE ,
T. RIGAUD  and
R. A. WATTIER
M. O. OVCHARENKO*
Affiliation:
Witold Stefański Institute of Parasitology of the Polish Academy of Sciences, 00-818 Warsaw, Poland Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, 01601 Kiev, Ukraine
K. BACELA
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS 5561 Biogéosciences, Université de Bourgogne, 21000 Dijon, France Department of Invertebrate Zoology and Hydrobiology, University of Lodz, 90-237 Lodz, Poland
T. WILKINSON
Affiliation:
Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Ceredigion, UK
J. E. IRONSIDE
Affiliation:
Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Ceredigion, UK
T. RIGAUD
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS 5561 Biogéosciences, Université de Bourgogne, 21000 Dijon, France
R. A. WATTIER
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS 5561 Biogéosciences, Université de Bourgogne, 21000 Dijon, France
*
*Corresponding author: Witold Stefański Institute of Parasitology of the Polish Academy of Sciences, 51/55 Twarda Street, 00-818 Warsaw, Poland. Tel: +48 22 6978995. Fax: +48 22 620 62 27. E-mail: mykola@twarda.pan.pl
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Summary

Dikerogammarus villosus is an invasive amphipod that recently colonized the main rivers of Central and Western Europe. Two frequent microsporidian parasites were previously detected in this species, but their taxonomic status was unclear. Here we present ultrastructural and molecular data indicating that these two parasites are in fact a single microsporidian species. This parasite shares numerous characteristics of Nosema spp. It forms elongate spores (cucumiform), developing in direct contact with host cell cytoplasm; all developmental stages are diplokaryotic and the life cycle is monomorphic with disporoblastic sporogony. Initially this parasite was described as Nosema dikerogammariOvcharenko and Kurandina 1987. However, phylogenetic analysis based on the complete sequence of SSU rDNA places the parasite outside the genus Nosema and it is therefore ascribed to a new genus Cucumispora. The key features characteristic to this genus are: presence of a very well-developed, umbrella-shape anchoring disk covering the anterior part of polaroplast; arrangement of isofilar polar filament into 6–8 coils convoluted with different angles, voluminous diplokaryon, thin spore wall and relatively small posterior vacuole containing posterosome. The parasite infects most host tissues but mainly muscles. It showed high rates of horizontal trophic transmission and lower rates of vertical transmission.

Keywords

AmphipodaMicrosporidiabiological invasionNosema dikerogammariCucumispora gen. sp.Dikerogammarus villosusSSU rDNAphylogeny
Type
Research Article
Information
Parasitology , Volume 137 , Issue 2 , February 2010 , pp. 191 - 204
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Baker, M. D., Vossbrinck, C. R., Maddox, J. V. and Undeen, A. H. (1994). Phylogenetic relationships among Vairimorpha and Nosema species (Microspora) based on ribosomal RNA sequence data. Journal of Invertebrate Pathology 30, 509–518.Google Scholar
Bij de Vaate, A., Jazdzewski, K., Ketelaars, H. A. M., Gollasch, S., Van der Velde, G. (2002). Geographical patterns in range extension of Ponto-caspian macroinvertebrate species in Europe. Canadian Journal of Fisheries and Aquatic Sciences 59, 1159–1174.CrossRefGoogle Scholar
Bollache, L., Gambade, G. and Cezilly, F. (2000). The influence of micro-habitat segregation on size assortative pairing in Gammarus pulex (L.) (Crustacea, Amphipoda) Archiv für Hydrobiologie 147, 547–558.CrossRefGoogle Scholar
Bollache, L., Devin, S., Wattier, R. A., Chovet, M., Beisel, J. N., Moreteau, J. C. and Rigaud, T. (2004). Rapid range extension of the pontocaspian amphipod D. villosus (Crustacea, Amphipoda) in France: potential consequences. Archiv für Hydrobiologie 160, 57–66.CrossRefGoogle Scholar
Bulnheim, H. P. and Vávra, J. (1968). Infection by the microsporidian Octosporea effeminans sp. n., and its sex determining influence in the amphipod Gammarus duebeni. Journal of Parasitology 54, 241–248.CrossRefGoogle Scholar
Canning, E. U., Refardt, D., Vossbrinck, C. R., Okamura, B. and Curry, A. (2002). New diplokaryotic microsporidia (Phylum Microsporidia) from freshwater bryozoans (Bryozoa, Phylactolaemata). European Journal for Protistology 38, 247–265.CrossRefGoogle Scholar
Devin, S., Piscart, C., Beisel, J. N. and Moreteau, J. C. (2003). Ecological impacts of the amphipod invader Dikerogammarus villosus on a mesohabitat scale. Archiv für Hydrobiologie 158, 43–56.CrossRefGoogle Scholar
Dick, J. T. A. and Platvoet, D. (2000). Invading predatory crustacean Dikerogammarus villosus eliminates both native and exotic species. Proceedings of the Royal Society of London, B 267, 977–983.CrossRefGoogle ScholarPubMed
Franzen, C., Fischer, S., Schroeder, J., Scholmerich, J. and Schneuwly, S. (2005). Morphological and molecular investigations of Tubulinosema ratisbonensis gen. nov., sp. nov. (Microsporidia: Tubulinosematidae fam. nov.), a parasite infecting a laboratory colony of Drosophila melanogaster (Diptera: Drosophilidae). Journal of Eukaryotic Microbiology 52, 141–152.CrossRefGoogle ScholarPubMed
Franzen, C., Nassonova, E. S., Scholmerich, J. and Issi, I. V. (2006). Transfer of the members of the genus Brachiola (microsporidia) to the genus Anncaliia based on ultrastructural and molecular data. Journal Eukaryotic Microbiology 53, 26–35.CrossRefGoogle Scholar
Gatehouse, H. S. and Malone, L. A. (1998). The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence of large tandem repeat unit size. Journal of Invertebrate Pathology 71, 97–105.CrossRefGoogle ScholarPubMed
Grabowski, M., Jazdzewski, K. and Konopacka, A. (2007). Alien Crustacea in Polish waters – Amphipoda. Aquatic Invasions 2, 25–38.CrossRefGoogle Scholar
Guindon, S. and Gascuel, O. (2003). Simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Haine, E. R., Brondani, E., Hume, K. D., Perrot-Minnot, M. J., Gaillard, M. and Rigaud, T. (2004). Coexistence of three microsporidia parasites in populations of the freshwater amphipod Gammarus roeseli: Evidence for vertical transmission and positive effect on reproduction. International Journal for Parasitology 34, 1137–1146.CrossRefGoogle ScholarPubMed
Haine, E. R., Motreuil, S. and Rigaud, T. (2007). Infection by a vertically-transmitted microsporidian parasite is associated with a female-biased sex ratio and survival advantage in the amphipod Gammarus roeseli. Parasitology 134, 1363–1367.CrossRefGoogle ScholarPubMed
Hall, T. A. (1999). BioEdit: a user friendly biological sequence alignment editor and analysis frogram for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Henry, J. E. and Oma, E. A. (1981). Pest control by Nosema locustae, a pathogen of grasshoppers and crickets. In Microbial Control of Pests and Plant diseases (ed. Burges, H. D.) pp 573–586. Academic Press, New York, USA.Google Scholar
Hillis, D. M., Moritz, C. and Mable, B. K. (1996). Molecular Systematics. 2nd Edn. Sinauer Associates, Inc., Sunderland, MA, USA.Google Scholar
Kelly, D. W., Dick, J. T A. and Montgomery, W. I. (2002). The functional role of Gammarus (Crustacea, Amphipoda): shredders, predators or both? Hydrobiologia 485, 199–203.CrossRefGoogle Scholar
Kinzler, W. and Maier, G. (2003). Asymmetry in mutual predation: possible reason for the replacement of native gammarids by invasives. Archive für Hydrobiologie 157, 473–481.CrossRefGoogle Scholar
Kinzler, W., Kley, A., Mayer, G., Waloszek, D. and Maier, G. (2009). Mutual predation between and cannibalism within several freshwater gammarids: Dikerogammarus villosus versus one native and three invasives. Aquatic Ecology 43, 457–464.CrossRefGoogle Scholar
Larsson, J. I. R. (1983). On two Microsporidia of the amphipod Rivulogammarus pulex, light microscopical and ultrastructural observations on Thelohania muelleri (Pfeiffer, 1895) and Nosema rivulogammari n. sp. (Microspora, Thelohaniidae and Nosematidae). Zoologischer Anzeiger 211, 299–323.Google Scholar
Larsson, J. I. R. (1999). Identification of microsporidia. Acta Protozoologica 38, 161–197.Google Scholar
MacNeil, C., Dick, J. T. A., Hatcher, M. J., Fielding, N. J., Hume, K. D. and Dunn, A. M. (2003). Parasite transmission and cannibalism in an amphipod (Crustacea). International Journal for Parasitology 33, 795–798.CrossRefGoogle Scholar
Mautner, S. I., Cook, K. A., Forbes, M. R., McCurdy, D. G. and Dunn, A. M. (2007). Evidence for sex ratio distortion by a new microsporidian parasite of a Corophiid amphipod. Parasitology 134, 1567–1573.CrossRefGoogle ScholarPubMed
Müller, A., Trammer, T., Chioralia, G., Seitz, H. M., Diehl, V. and Franzen, C. (2000). Ribosomal RNA of Nosema algerae and phylogenetic relationship to other microsporidia. Parasitology Research 86, 18–23.CrossRefGoogle ScholarPubMed
Ovcharenko, M., Codreanu-Bălcescu, D., Grabowski, M., Konopacka, A., Wita, I. and Czaplińska, U. (2009). Unicellular parasites of native and invasive gammaridean crustaceans (Amphipoda, Gammaroidea) occurring in the Baltic Basin. Wiadomości Parazytologiczne (in the Press).Google Scholar
Ovcharenko, N. A. and Kurandina, D. P. (1987). New species of Microsporidia from amphipods of the Dnieper basin. Parazitologija 21, 710–715.Google Scholar
Ovcharenko, N. A. and Vita, I. (1996). New data on microsporidium Nosema dikerogammari. Parazitologija 30, 333–338.Google Scholar
Pfeiffer, L. (1895). Die Infektion mit Glugea mülleri nov. spec. im Muskel von Gammarus pulex. In Die Protozoen als Krankheitserreger (ed. Pffeifer, L.), pp. 54–60. Gustaw Fisher Verlag, Jena, Germany.CrossRefGoogle Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Sato, R., Kobayashi, M., Watanabe, Y. (1982). Internal ultrastructure of spores of microsporidians isolated from the silkworm, Bombyx mori. Journal of Invertebrate Pathology 40, 260–265.CrossRefGoogle Scholar
Seutin, G., White, B. N. and Boag, P. T. (1991). Preservation of avian blood and tissue samples for DNA analysis. Canadian Journal of Zoology 69, 82–90.CrossRefGoogle Scholar
Silveira, H. and Canning, E. U. (1995). Vittaforma corneae n. comb. for the human microsporidium Nosema corneum Shadduck, Meccoli, Davis and Font, 1990, based on its ultrastructure in the liver of experimentally infected athymic mice. Journal of Eukaryotic Microbiology 42, 158–165.CrossRefGoogle ScholarPubMed
Slamovits, C. H., Slamovits, B. A., Williams, P. and Keeling, P. J. (2004). Transfer of Nosema locustae (Microsporidia) to Antonospora locustae n comb based on molecular and ultrastructural data. Journal of Eukaryotic Microbiology 51, 207–213.CrossRefGoogle ScholarPubMed
Slothouber-Galbreath, J. G. M., Smith, J. E., Terry, R. S., Becnel, J. J. and Dunn, A. M. (2004). Invasion success of Fibrillanosema crangonycis, n.sp., n.g.: a novel vertically transmitted microsporidian parasite from the invasive amphipod host Crangonyx pseudogracilis. International Journal for Parasitology 34, 235–244.Google Scholar
Sokolova, Y. Y., Issi, I. V., Morzhina, E. V., Tokarev, Y. S. and Vossbrinck, C. R. (2005). Ultrastructural analysis supports transferring Nosema whitei Weiser 1953 to the genus Paranosema and creation a new combination, Paranosema whitei. Journal of Invertebrate Pathology 90, 122–126.CrossRefGoogle Scholar
Spraque, V. (1977). Annotated list of species of Microsporidia. In Comparative Pathology. Vol. 2. Systematic of the Microsporidia, pp. 31–462. Plenum Press, New York, USA and London, UK.Google Scholar
Sweeney, A. W. and Becnel, J. J. (1991). Potential of microsporidia for the biological control of mosquitoes. Parasitology Today 7, 217–220.CrossRefGoogle ScholarPubMed
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, 1596–1599.CrossRefGoogle ScholarPubMed
Terry, R. S., Smith, J. E., Bouchon, D., Rigaud, T., Duncanson, P., Sharpe, R. G. and Dunn, A. M. (1999). Ultrastructural characterisation and molecular taxonomic identification of Nosema granulosis n. sp., a transovarially transmitted feminising (TTF) microsporidium. Journal of Eukaryotic Microbiology 46, 492–499.CrossRefGoogle Scholar
Terry, R. S., MacNeil, C., Dick, J. T. A., Smith, J. E. and Dunn, A. M. (2003). Resolution of a taxonomic conumdrum: an ultrastructural and molecular description of the life cycle of Pleistophora mulleri (Pfeiffer). Journal of Eukaryotic Microbiology 50, 266–273.CrossRefGoogle Scholar
Terry, R. S., Smith, J. E., Sharpe, R. G., Rigaud, T., Littlewood, T. J., Ironside, J. E., Rollinson, D., Bouchon, D., MacNeil, C., Dick, J. T. A. and Dunn, A. M. (2004). Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora. Proceedings of the Royal Society of London, B 271, 1783–1789.CrossRefGoogle ScholarPubMed
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle Scholar
Van Riel, M. C., Van der Velde, G., Rajagopal, S., Marguiller, S., Dehairs, F. and Bij de Vaate, A. (2006). Trophic relationships in the Rhine food web during invasion and after establishment of the Ponto-Caspian invader Dikerogammarus villosus. Hydrobiologia 565, 39–58.CrossRefGoogle Scholar
Vávra, J. and Maddox, J. V. (1976). Methods in microsporidiology. In Comparative Pathobiology (ed. Bulla, L. A. and Cheng, T. C.), pp. 281–319. Plenum Press, New York, USA.Google Scholar
Vossbrinck, C. R., Baker, M. D., Didier, E. S., Debrunner-Vossbrinck, B. A. and Shadduck, J. A. (1993). Ribosomal DNA sequences of Encephalitozoon hellem and Encephalitozoon cuniculi: species identification and phylogenetic construction. Journal of Eukaryotic Microbiology 40, 354–362.CrossRefGoogle ScholarPubMed
Vossbrinck, C. R. and Debrunner-Vossbrinck, B. A. (2005). Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitilogica 52, 131–142.CrossRefGoogle ScholarPubMed
Weiss, L. M. and Vossbrinck, C. R. (1998). Ribosomal microsporidiosis: molecular and diagnostic aspects. Advanced Parasitology 40, 351–395.CrossRefGoogle ScholarPubMed
Weiss, L. M., Zhu, X., Cali, A., Tanowitz, H. B. and Wittner, M. (1994). Utility of microsporidian rRNA in diagnosis and phylogeny: a review. Folia Parasitologica 41, 81–90.Google ScholarPubMed
Wattier, R. A., Haine, E. R., Beguet, J., Martin, G., Bollache, L., Musko, I. B., Platvoet, D. and Rigaud, T. (2007). No genetic bottleneck or associated microparasite loss in invasive populations of a freshwater amphipod. Oikos. 116, 1941–1953.CrossRefGoogle Scholar
Woolhouse, M. E. J. (2002). Population biology of emerging and re-emerging pathogens. Trends in Microbiology 10 (Suppl.), S3–S7.CrossRefGoogle ScholarPubMed