Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-22T14:52:42.233Z Has data issue: false hasContentIssue false
  • English
  • Français

The ecology and evolution of microsporidian parasites

Published online by Cambridge University Press:  08 December 2009

J. E. SMITH
J. E. SMITH*
Affiliation:
Institute of Integrative and Comparative Biology, Faculty of Biological Sciences, The University of Leeds, Leeds LS2 9JT, UK
*
Corresponding author: Judith E. Smith, Institute of Integrative and Comparative Biology, Miall Building, Faculty of Biological Sciences, The University of Leeds, Leeds LS2 9JT, UK Tel: 0044 (0) 113 343 2892. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The phylum Microspora is ancient and diverse and affects a wide range of hosts. There is unusually high use of vertical transmission and this has significant consequences for transmission and pathogenicity. Vertical transmission is associated with low pathogenesis but nevertheless can have significant impact through associated traits such as sex ratio distortion. The majority of microsporidia have mixed transmission cycles and it is not clear whether they are able to modify their phenotype according to environmental circumstances. There is a great need to understand the mechanisms controlling transmission and one of the first challenges for the genomics era is to find genes associated with life cycle stages. Similarly we cannot currently predict the ease with which these parasites might switch between host groups. Phylogenetic analysis suggests that there are strong relationships between Microsporidia and their hosts. However closer typing of parasite isolates, in relation to host range and disease phenotype, is required to assess future environmental risk from these pathogens.

Keywords

MicrosporidiaMicrosporavertical transmissionecologyevolution
Type
Research Article
Information
Parasitology , Volume 136 , Special Issue 14: Transmission cycles in protozoan parasites , December 2009 , pp. 1901 - 1914
Copyright
Copyright © Cambridge University Press 2009

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

Andreadis, T. G. (1985). Experimental transmission of a microsporidian pathogen from mosquitoes to an alternate copepod host. Proceedings of the National Academy of Sciences, USA 82, 5574–5577.Google Scholar
Andreadis, T. G. (1987). Horizontal transmission of Nosema pyrausta (Microsporidia: Nosematidae) in the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae). Environmental Entomology 16, 1124–1129.CrossRefGoogle Scholar
Andreadis, T. G. (1990). Epizootiology of Amblyospora connecticus (Microsporida) in field populations of the saltmarsh mosquito, Aedes cantator, and the cyclopoid copepod, Acantocyclops vernalis. Journal of Protozoology 37, 174–182.Google Scholar
Akiyoshi, D. E., Morrison, H. G., Lei, S., Feng, X., Zhang, Q., Corradi, N., Mayanja, H., Tumwine, J. K., Keeling, P. J., Weiss, L. M. and Tzipori, S. (2009). Genomic survey of the non-cultivatable opportunistic human pathogen, Enterocytozoon bieneusi. PLoS Pathogens 5, e1000261.CrossRefGoogle ScholarPubMed
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 sequences. Journal of Invertebrate Pathology 61, 100–106.CrossRefGoogle Scholar
Baneux, J. R. and Pognan, F. (2003). In utero transmission of Encephalitozoon cuniculi strain type I in rabbits. Laboratory Animal 37, 132–138.Google Scholar
Becnel, J. J. and Andreadis, T. G. (2001). Microsporidia in Insects. In Microsporidia and Microsporidiosis (ed. Wittner, M. and Weiss, L. M.) pp. 447–501. ASM press, Washington DC.Google Scholar
Becnel, J. J., Sprague, V., Fukada, T. and Hazard, E. (1989). Development of Edharzardia aedis (Kudo, 1930) n.g.n. comb. (Microsporidia:Amblyosoridae) in the mosquito Aedes aegypti (L.) (Diptera:Culicidae). Journal of Protozoology 36, 119–130.Google Scholar
Belkorchia, A., Biderre, C., Militon, C., Polonais, V., Wincker, P., Jubin, C., Delbac, F., Peyretaillade, E. and Peyret, P. (2008). In vitro propagation of the microsporidian pathogen Brachiola algerae and studies of its chromosome and ribosomal DNA organization in the context of the complete genome sequencing project. Parasitology International 57, 62–71.CrossRefGoogle ScholarPubMed
Bigliardi, E., Riparbelli, M. G., Selmi, M. G., Lanzarini, P., Corona, S., Gatti, S., Scaglia, M. and L. Sacchi, L. (1998). Mechanisms of microsporidial cell division: ultrastructural study on Encephalitozoon hellem. Journal of Eukaryotic Microbiology 45, 347–351.CrossRefGoogle Scholar
Briano, J. S., Patterson, R. S., Becnel, J. J. and Cordo, H. A. (1996). The black imported fire ant, Solenopsis richteri, infected with Thelohania solenopsae: Intracolonial prevalence of infection and evidence for transovarial transmission. Journal of Invertebrate Pathology 67, 178–179.CrossRefGoogle Scholar
Cali, A., Weiss, L. M. and Takvorian, P. M. (2004). An analysis of the microsporidian genus Brachiola, with comparisons of human and insect isolates of Brachiola algerae. Journal of Eukaryotic Microbiology 51, 678–685.CrossRefGoogle ScholarPubMed
Canning, E. U. (1953). A new microsporidian Nosema locusta n. sp. from the fat body of the African migratory locust, Locusta migratoria migrattoroides R and F. Parasitology 43, 297–290.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 of Protistology 38 247–265.Google Scholar
Corradi, N., Gangaeva, A. and Keeling, P. J. (2008). Comparative profiling of overlapping transcription in the compacted genomes of microsporidia Antonospora locustae and Encephalitozoon cuniculi. Genomics 91, 388–393.CrossRefGoogle ScholarPubMed
Cox-Foster, D. L., Conlan, S., Holmes, E. C., Palacios, G., Evans, J. D., Moran, N. A., Quan, P.-L., Briese, T., Hornig, M., Geiser, D. M., Martinson, V., Vanengelsdorp, D., Kalkstein, A. L., Drysdale, A., Hui, J., Zhai, J., Cui, L., Hutchison, S. K., Simons, J. F., Egholm, M., Pettis, J. S. and Lipkin, W. I. (2007). A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318, 283–287.Google Scholar
Crawford, G. I. (1937). An amphipod, Eucrangonyx gracilis S.I. Smith, new to Britain. Nature 139, 327.CrossRefGoogle Scholar
Curgy, J. J., Vavra, J. and Vivares, C. (1980). Presence of Ribosomal-RNAs with prokaryotic properties in microsporidia, eukaryotic origins. Biologie Cellulaire 38, 49–51.Google Scholar
Czekonska, K. (2000). The influence of Nosema apis on young honeybee queens and transmission of the disease from queens to workers. Apidologie 31, 701–706.CrossRefGoogle Scholar
Didier, E. S. (2005), Microsporidiosis: An emerging and opportunistic infection in humans and animals. Acta Tropica 94, 61–76.CrossRefGoogle ScholarPubMed
Dissanaike, A. S. and Canning, E. U. (1957). The mode of emergence of the protoplasm in Microsporidia and its relation to the structure of the spore. Parasitology 47, 92–99.CrossRefGoogle Scholar
Down, R. E., Bell, H. A., Kirkbride-Smith, A. E. and Edwards, J. P. (2004). The pathogenicity of Vairimorpha necatrix (Microspora: Microsporidia) against the tomato moth, Lacanobia oleracea (Lepidoptera: Noctuidae) and its potential use for the control of lepidopteran glasshouse pests. Pest Management Science 60, 755–764.Google Scholar
Dunn, A. M., Adams, J. and Smith, J. E. (1993). Transovarial transmission and sex ratio distortion by a microsporidian parasite in a shrimp. Journal of Invertebrate Pathology 61, 248–252.Google Scholar
Dunn, A. M., Hogg, J. C. and Hatcher, M. J. (2006). Transmission and burden and the impact of temperature on two species of vertically transmitted microsporidia. International Journal for Parasitology 36, 409–414.Google Scholar
Dunn, A. M. and Smith, J. E. (2001). Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes and Infection 3, 381–388.Google Scholar
Dunn, A. M., Terry, R. S. and Smith, J. E. (2001). Transovarial transmission in the Microsporidia. Advances in Parasitology 48, 57–101.Google Scholar
Dunn, J. C., McClymont, H. E., Christmas, M. and Dunn, A. M. (2009). Competition and parasitism in the native White Clawed Crayfish Austropotamobius pallipes and the invasive Signal Crayfish Pacifastacus leniusculus in the UK. Biological Invasions 11, 315–324.Google Scholar
Duron, O., Bouchon, D., Boutin, S., Bellamy, L., Zhou, L., Engelstädter, J. and Hurst, G. D. D. (2008). The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biology 6, 27.Google Scholar
Fantham, H. B. and Porter, A. (1912). Microsporidiosis, a protozoal disease of bees due to Nosema apis and popularly known as the Isle of Wight Disease. Annals of Tropical Medcine and Parasitology 6, 145–60.CrossRefGoogle Scholar
Fokin, S. I., Di Giuseppe, G., Erra, F. and Dini, F. (2008). Euplotespora binucleata n. gen., n. sp (Protozoa: Microsporidia), a parasite infecting the hypotrichous ciliate Euplotes woodruffi, with observations on microsporidian infections in Ciliophora. Journal of Eukaryotic Microbiology 55, 214–228.Google Scholar
Fries, I. (1989). Observations on the development and transmission of Nosema apis Z. in the ventriculus of the honeybee. Journal of Apiculture Research 28, 107–117.CrossRefGoogle Scholar
Fries, I. and Camazine, S. (2001). Implications of horizontal and vertical pathogen transmission for honey bee epidemiology. Apidologie 32, 199–214.Google Scholar
Fries, I., De Ruijter, A., Paxton, R. J., Da Silva, A. J., Slemenda, S. B. and Pieniazek, N. J. (2001). Molecular characterization of Nosema bombi (Microsporidia: Nosematidae) and a note on its sites of infection in Bombus terrestris (Hymenoptera: Apoidea). Journal of Apiculture Research 40, 91–96.CrossRefGoogle Scholar
Fries, I., Feng, F., Da Silva, A., Slemenda, S. B. and Pieniazek, N. J. (1996). Nosema ceranae n. sp. (Microspora, Nosemaditae), morphological and molecular characterisation of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). European Journal of Protistology 32, 356–365.Google Scholar
Fries, I., Granados, R. R. and Morse, R. A. (1992). Intracellular germination of Nosema apis Z. Apidologie 23, 61–70.Google Scholar
Fuxa, J. R., Milks, M. L., Sokolova, Y. Y. and Richter, A. R. (2005). Interaction of an entomopathogen with an insect social form: an epizootic of Thelohania solenopsae (Microsporidia) in a population of the red imported fire ant, Solenopsis invicta. Journal of Invertebrate Pathology 88, 79–82.CrossRefGoogle Scholar
Gill, E. E., Becnel, J. J. and Fast, N. M. (2008). ESTs from the microsporidian Edhazardia aedis. BMC Genomics 9, 296.Google Scholar
Goertz, D. and Hoch, G. (2008). Vertical transmission and overwintering of microsporidia in the gypsy moth, Lymantria dispar. Journal of Invertebrate Pathology 99, 43–48.Google Scholar
Goertz, D. and Hoch, G. (2009). Three microsporidian pathogens infecting Lymantria dispar larvae do not differ in their success in horizontal transmission. Journal of Applied Entomology 133, 568–570.Google Scholar
Goldberg, A. V., Molik, S., Tsaousis, A. D., Neumann, K., Kuhnke, G., Delbac, F., Vivares, C. P., Hirt, R. P., Lill, R. and Embley, T. M. (2008). Localization and functionality of microsporidian iron–sulphur cluster assembly proteins. Nature 452, 624–628.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.Google Scholar
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.Google Scholar
Han, M.-S. and Watanabe, H. (1988). Transovarial transmission of two microsporidia in the silkworm Bombyx mori and disease occurance in the progeny population. Journal of Invertebrate Pathology 51, 41–45.Google Scholar
Hatakeyama, Y. and Hayasaka, S. (2003). A new method of pebrine inspection of silkworm egg using multiprimer PCR. Journal of Invertebrate Pathology 82, 148–151.Google Scholar
Higes, M., Martín-Hernández, R., Botías, C., Bailón, E. G., González-Porto, A. V., Barrios, L., Del Nozal, M. J., Bernal, J. L., Jiménez, J. J., Palencia, P. G. and Meana, A. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology 10, 2659–2669.Google Scholar
Hirt, R. P., John, M., Logsdon, J., Healy, B., Dorey, M. W., Doolittle, W. F. and Embley, T. M. (1999). Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proceedings of the National Acadamy of Sciences, USA 96, 580–585.CrossRefGoogle ScholarPubMed
Ironside, J., Dunn, A. M., Rollinson, D. R. and Smith, J. E. (2003). Association with host mitochondrial haplotypes suggests that feminizing microsporidia lack horizontal transmission. Journal of Evolutionary Biology 16, 1077–1083.CrossRefGoogle ScholarPubMed
Ironside, J. E., Wilkinson, T. J. and Rock, J. (2008). Distribution and host range of the microsporidian Pleistophora mulleri. Journal of Eukaryotic Microbiology 55, 355–362.Google Scholar
Ishihara, R. (1969). Life cycle of Nosema bombycis as revealed in tissue culture cells of Bombyx mori. Journal of Invertebrate Pathology 14, 316–320.Google Scholar
Ishihara, R. and Fujiwava, T. (1965). The spread of pebrine within a colony of the Silkworm, Bombyx mori (Linnaeus). Journal of Invertebrate Pathology 7, 126–131.Google Scholar
Iwano, H. and Ishihara, R. (1991). Dimorphic development of Nosema bombycis spores in the gut epithelium of the larvae of the silkworm Bombyx mori. Journal of Sericulture Science Japan 60, 249–256.Google Scholar
Iwano, H. and Kurtti, T. J. (1995). Identification and Isolation of Dimorphic Spores from Nosema furnacalis (Microspora: Nosematidae). Journal of Invertebrate Pathology 65, 230–236.CrossRefGoogle Scholar
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 443, 818–822.CrossRefGoogle ScholarPubMed
Johnson, M. A., Becnel, J. J. and Undeen, A. H. (1997). A new sporulation sequence in Edhazardia aedis (Microsporidia: Culicosporidae), a parasite of the mosquito Aedes aegypti (Diptera: Culicidae). Journal of Invertebrate Pathology 70, 69–75.CrossRefGoogle Scholar
Kashkarova, L. F. and Khakhanov, A. I. (1980). Range of hosts of the agent of Microsporidiosis Nosema bombycis of the Chinese silkworm. Parazitologiya (St. Petersburg) 14 164–167.Google Scholar
Katinka, M. D., Duprat, S., Cornillot, E., Metenier, G., Thomarat, F., Prensier, G., Barbe, V. A., Peyretaillade, E., Brottier, P., Wincker, P., Delbac, F., El Alaoui, H., Peyret, P., Saurin, W., Gouy, M., Weissenbach, J. and Vivares, C. P. (2001). Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414, 450–453.Google Scholar
Katznelson, H. and Jamieson, C. A. (1952). Control of Nosema disease in honey bees with fumagillin. Science 115, 70–71.Google Scholar
Keeling, P. J. and Fast, N. M. (2002). Microsporidia: Biology and evolution of highly reduced intracellular parasites. Annual Review of Microbiology 56, 93–116.Google Scholar
Keeling, P. J., Luker, M. A. and Palmer, J. D. (2000). Evidence from beta-tubulin phylogeny that Microsporidia evolved from the Fungi. Molecular Biology and Evolution 17, 23–31.Google Scholar
Kent, M. L. and Bishop-Stewart, J. K. (2003). Transmission and tissue distribution of Pseudoloma neurophilia (Microsporidia) of zebrafish, Danio rerio (Hamilton). Journal of Fish Diseases 26, 423–426.CrossRefGoogle ScholarPubMed
Klee, J., Besana, A. M., Genersch, E., Gisder, S., Nanetti, A., Tam, D. Q., Chinh, T. X., Puerta, F., Ruz, J. M., Kryger, P., Message, D., Hatjina, F., Korpela, S., Fries, I. and Paxton, R. J. (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology 96, 1–10.Google Scholar
Lange, C. E. (2005). The host and geographical range of the grasshopper pathogen Paranosema (Nosema) locustae revisited. Journal of Orthopteran Research 14, 137–141.Google Scholar
Larsson, J. I. R. (2007). Cytological variation and pathogenicity of the bumble bee parasite Nosema bombi (Microspora, Nosematidae). Journal of Invertebrate Pathology 94, 1–11.CrossRefGoogle ScholarPubMed
Lee, S. C., Corradi, N., Byrnes, E. J., Torres-Martinez, S., Dietrich, F. H., Keeling, P. J. and Heitmam, J. (2008). Microsporidia evolved from ancestral sexual fungi. Current Biology 18, 1675–1679.Google Scholar
Lewis, L. C., Bruck, D. J., Prasifka, J. R. and Raun, E. S. (2009). Nosema pyrausta: Its biology, history, and potential role in a landscape of transgenic insecticidal crops. Biological Control 48, 223–231.Google Scholar
Liu, T. P. (1992). Oocytes degeneration in the queen honey bee after infection by Nosema apis. Tissue and Cell 24, 131–138.Google Scholar
Liu, J. P., Cao, Y., Smith, J. E. and Xu, X. (2004). Studies of the application of PCR molecular diagnosis to silkworms with simulated pebrine disease. Scientia Agricultura Sinica 37, 1925–1931.Google Scholar
Lom, J. and Nilsen, F. (2003). Fish microsporidia: fine structural diversity and phylogeny. International Journal for Parasitology 33, 107–127.Google Scholar
Lom, J., Nilsen, F. and Dykova, I. (2001). Thelohania contejeani Henneguy, 1892: dimorphic life cycle and taxonomic affinities, as indicated by ultrastructural and molecular study. Parasitology Research 87, 860–872.Google Scholar
Lomer, C. L., Bateman, P. P., Johnson, D. L., Langewald, J. and Thomas, M. B. (2001). Biological control of locusts and grasshoppers. Annual Review of Entomology 46, 667–702.Google Scholar
Malone, L. A. and Giacon, H. A. (1996). Effects of Nosema apis Zander on inbred New Zealand honey bees (Apis mellifera ligustica L). Apidologie 27, 479–486.CrossRefGoogle Scholar
Malone, L. A. and McIvor, C. A. (1993). Pulsed-field electrophoresis of DNA from four microsporidian isolates. Journal of Invertebrate Pathology 61, 203–205.Google Scholar
Martin-Hernandez, R., Meana, A., Garcia-Palencia, P., Marin, P., Botias, C., Garido-Bailon, E., Barrios, L. and Higes, M. (2009). Effect of temperature on the biotic potential of Honeybee microsporidia. Applied and Environmental Microbiology 75, 2554–2557.CrossRefGoogle ScholarPubMed
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
McClymont, E. H., Dunn, A. M., Terry, R. S., Rollinson, D., Littlewood, D. T. J. and Smith, J. E. (2005). Molecular data suggest that microsporidian parasites in freshwater snails are diverse. International Journal for Parasitology 35, 1071–1078.Google Scholar
Micieli, M. V., Garcia, J. J. and Becnel, J. J. (2000). Horizontal transmission of Amblyospora albifasciati García and Becnel, 1994 (Microsporidia: Amblyosporidae), to a copepod intermediate host and the neotropical mosquito Aedes albifasciatus (Macquart, 1837). Journal of Invertebrate Pathology 75, 76–83.Google Scholar
Micieli, M. V., Marti, G. A., Garcia, J. J., Tranchida, M. C. and Becnel, J. J. (2007). Epizootiological studies of Amblyospora camposi (Microsporidia: Amblyosporidae) in Culex renatoi (Diptera: Culicidae) and Paracyclops fimbriatus fimbriatus (Copepoda: Cyclopidae) in a bromeliad habitat. Journal of Invertebrate Pathology 194, 31–37.CrossRefGoogle Scholar
Morris, D. J., Terry, R. S., Ferguson, K. D., Smith, J. and Adams, A. (2005). Ultrastructural and molecular characterization of Bacillidium vesiculoformis n. sp. (Microspora: Mrazekiidae) in the freshwater oligochaete Nais simplex (Oligochaeta: Naididae). Parasitology 30, 31–45.Google Scholar
Olivares, C. A. (2005). Evidence of a parasite protist in Eurhomalea lenticularis (Sowerby, 1835) (Mollusca: Bivalvia): A case of intraoocytarian parasitism. Journal of Natural History 39, 2073–2082.Google Scholar
Otti, O. and Schmid-Hempel, P. (2007). Nosema bombi: A pollinator parasite with detrimental fitness effects. Journal of Invertebrate Pathology 96, 118–124.Google Scholar
Otterstatter, M. C. and Thomson, J. D. (2008). Does pathogen spillover from commercially reared bumble bees threaten wild pollinators? PloS One 3, 1–9.Google Scholar
Pasteur, L. (1870). Etudes sur la maladie des vers à soie, moyen pratique assuré de la combattre et d'en prévenir le retour. Paris, Gauthier-Villars, 327 pp.Google Scholar
Pajuelo, A. G., Torres, C. and Bermejo, F. J. O. (2008). Colony losses: a double blind trial on the influence of supplementary protein nutrition and preventative treatment with fumagillin against Nosema ceranae. Journal of Apiculture Research 47, 84–86.Google Scholar
Paxton, R. J., Klee, J., Korpela, S. and Fries, I. (2007). Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 38, 558–565.Google Scholar
Phelps, N. B. D. and Goodwin, A. E. (2008). Vertical transmission of Ovipleistophora ovariae (Microspora) within the eggs of the golden shiner. Journal of Aquatic Animal Health 20, 45–53.CrossRefGoogle ScholarPubMed
Raina, S. K., Das, S., Rai, M. M. and Khurad, A. M. (1995). Transovarial transmission of Nosema locustae (Microsporida: Nosematidae) in the migratory locust Locusta migratoria migratorioides. Parasitology Research 81, 38–44.CrossRefGoogle ScholarPubMed
Rao, S. N., Nath, B. S., Bhuvaneswari, G. and Urs, S. R. (2007). Genetic diversity and phylogenetic relationships among microsporidia infecting the silkworm, Bombyx mori, using random amplification of polymorphic DNA: Morphological and ultrastructural characterization. Journal of Invertebrate Pathology 96, 193–204.Google Scholar
Rao, S. N., Nath, B. S. and Saratchandra, B. (2005). Characterization and phylogenetic relationships among microsporidia infecting silkworm, Bombyx mori, using inter simple sequence repeat (ISSR) and small subunit rRNA (SSU-rRNA) sequence analysis. Genome 48, 355–366.Google Scholar
Rodgers-Gray, T. P., Smith, J. E., Ashcroft, A. E., Isaac, R. E. and Dunn, A. M. (2004). Mechanisms of parasite-induced sex reversal in Gammarus duebeni. International Journal for Parasitology 34, 747–753.Google Scholar
Ronnebaumer, K., Gross, U. and Bonhe, W. (2008). The nascent parasitophorous vacuole membrane of Encephalitozoon cuniculi is formed by host cell lipids and contains pores which allow nutrient uptake. Eukaryotic Cell 7, 1001–1008.Google Scholar
Rutrecht, S. T. and Brown, M. J. F. (2007). Within colony dynamics of Nosema bombi infections: disease establishment, epidemiology and potential vertical transmission. Apidologie 39, 504–514.Google Scholar
Rutrecht, S. T. and Brown, M. J. F. (2009). Differential virulence in a multiple-host parasite of bumble bees: resolving the paradox of parasite survival. OIKOS 118, 941–949.Google Scholar
Sagrista, E., Bozzo, M. G., Bigas, M., Poquet, M. and Durfort, M. (1998). Developmental cycle and ultrastructure of Steinhausia mytilovum, a microsporidian parasite of oocytes of the mussel, Mytilus galloprovincialis (Mollusca, Bivalvia). European Journal of Protistology 34, 58–68.Google Scholar
Sajap, A. S. and Lewis, L. C. (1988). Histopathology of transovarial transmission of Nosema pyrausta in the European corn borer, Ostrinia nubilalis. Journal of Invertebrate Pathology 52, 147–153.Google Scholar
Sajap, A. S. and Lewis, L. C. (1992). Chronology of infection of European corn borer (Lepidoptera: Pyralidae) with the microsporidium Nosema pyrausta: effect on development and vertical transmission. Environmental Entomology 21, 178–182.Google Scholar
Scanlon, M., Leitch, G. J., Visvesvara, G. S. and Shaw, A. P. (2004). Relationship between the host cell mitochondria and the parasitophorous vacuole in cells infected with Encephalitozoon Microsporidia. Journal of Eukaryotic Microbiology 51, 81–87.Google Scholar
Sinden, R. E. and Canning, E. U. (1974). The ultrastructure of the spore of Nosema algerae (Protozoa, Microsporida), in relation to the hatching mechanism of Microsporidian spores. Journal of General Microbiology 85, 350–357.CrossRefGoogle Scholar
Slothouber-Galbreath, J. G. N., Smith, J. E., Becnel, J. J., Butlin, R. J. and Dunn, A. M. (2009). Reduction in post-invasion genetic diversity in Crangonyx pseudogracilis (Amphipoda: Crustacea): a genetic bottleneck or the work of hitchhiking vertically transmitted microparasites? Biological Invasions, online doi: 10.1007/s10530-009-9442-3.Google Scholar
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
Solter, L. F. (2006). Transmission as a predictor of ecological host specificity with a focus on vertical transmission of Microsporidia. Journal of Invertebrate Pathology 92, 132–140.Google Scholar
Solter, L. F. and Maddox, J. V. (1998). Physiological host specificity of microsporidia as an indicator of ecological host specificity. Journal of Invertebrate Pathology 71, 207–216.CrossRefGoogle ScholarPubMed
Solter, L. F., Maddox, J. V. and McManus, M. L. (1997). Host specificity of Microsporidia (Protista: Microspora) from European populations of Lymantria dispar (Lepidoptera: Lymantriidae) to indigenous North American Lepidoptera. Journal of Invertebrate Pathology 69, 135–150.Google Scholar
Solter, L. F., Pilarska, D. K. and Vossbrinck, C. F. (2000). Host specificity of microsporidia pathogenic to forest Lepidoptera. Biological Control 19, 48–56.CrossRefGoogle Scholar
Sokolova, Y. Y., Dolgikh, V. V., Morzhina, E. V., Nassonova, E. S., Issi, I. V., Terry, R. S., Ironside, J. E., Smith, J. E. and Vossbrinck, C. R. (2003). Establishment of the new genus Paranosema based on the ultrastructure and molecular phylogeny of the type species Paranosema grylli Gen. Nov., Comb. Nov. (Sokolova, Selezniov, Dolgikh, Issi 1994), from the cricket Gryllus bimaculatus Deg. Journal of Invertebrate Pathology 84, 159–172.CrossRefGoogle ScholarPubMed
Soklova, Y. Y., Issi, I. V., Morzina, E. V., Tokarev, Y. S. and Vossbrink, 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
Sprague, V., Becnel, J. J. and Hazard, E. I. (1992). Taxonomy of phylum Microspora. Critical Reviews in Microbiology 18, 285–395.CrossRefGoogle ScholarPubMed
Stanimirovic, Z., Stevanovic, J., Bajic, V. and Radovic, I. (2007). Evaluation of genotoxic effects of fumagillin by cytogenetic tests in vivo. Mutation Research-Genetic Toxicology and Environmental Mutagenesis 628, 1–10.CrossRefGoogle ScholarPubMed
Streett, D. A. (1994). Analysis of Nosema locustae (microsporidia:Nosematidae) chromosomal DNA with pulsed-field gel electrophoresis. Journal of Invertebrate Pathology 63, 301–303.CrossRefGoogle Scholar
Terry, R. S., Dunn, A. M. and Smith, J. E. (1997). Cellular distribution of a feminizing microsporidian parasite: A strategy for transovarial transmission. Parasitology 115, 157–163.Google Scholar
Terry, R. S., Dunn, A. M. and Smith, J. E. (1999). Segregation of a cytoplasmic parasite during host cell mitosis. Parasitology 118, 43–48.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.Google Scholar
Terry, R. S., Smith, J. E. and Dunn, A. M. (1998). Impact of a novel feminizing microsporidian parasite on its crustacean host. Journal of Eukaryotic Microbiology 45, 497–501.Google Scholar
Terry, R. S., Smith, J. E., Sharpe, R. G., Rigaud, T., Littlewood, D. T., Ironside, J. E., Rollinson, D., Bouchon, D., MacNeil, C., Dick, J. T. and Dunn, A. M. (2004). Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora. Proceedings of the Royal Society Series B, Biological Sciences 271, 1783–1789.Google Scholar
Tounou, A. K., Kooyman, C., Douro-Kplndou, O. K. and Poehling, H.-M. (2008). Interaction between Paranosema locustae and Metarhizium anisopliae var. acridum, two pathogens of the desert locust, Schistocerca gregaria under laboratory conditions. Journal of Invertebrate Pathology 97, 203–210.Google Scholar
Troemel, E. R., Felix, M.-A., Whiteman, N. K., Barriere, A. and Asubel, F. M. (2008). Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans. PLoS Biology 6, 2736–52.Google Scholar
Tsaousis, A. D., Kunji, E. R., Goldberg, A. V., Lucocq, J. M., Hirt, R. P. and Embley, T. M. (2008). A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453, 553–556.Google Scholar
Undeen, A. H. and Vandermeer, R. K. (1994). Conversion of intrasporal trehalose into reducing sugars during germination of Nosema algerae (Protista: Microspora) spores—a quantitative study. Journal of Eukaryotic Microbiology 41, 129–132.CrossRefGoogle Scholar
Vavra, J. and Undeen, A. H. (1970). Nosema algerae n. sp. (Cnidospora, Microsporidia) a pathogen in a laboratory colony of Anopheles Stephensi Liston (Diptera:Culicidae). Journal of Protozoology 17, 240–249.CrossRefGoogle Scholar
Vavra, J. (1976). Structure of the Microsporidia. In Comparative Pathobiology (ed. Bulla, L. A. and Cheng, T. C.), pp. 1–85, Vol. 1, Plenum Press, New York, NY.Google Scholar
Vavra, J., Hylis, M., Vossbrinck, C. R., Pilarska, D. K., Weiser, J., McManus, M. L., Hoch, G. and Solter, L. F. (2006). Vairimorpha disparis n. comb. (Microsporidia: Burenellidae): A redescription and taxonomic revision of Thelohania disparis timofejeva 1956, a microsporidian parasite of the gypsy moth Lymantria dispar (L.) (Lepidoptera: Lymantriidae). Journal of Eukaryotic Microbiology 53, 292–304.Google Scholar
Vavra, J. and Larsson, J. I. R. (2001). In Microsporidia and Microsporidiosis (ed. Wittner, M. and Weiss, L. M.), pp. 447–501, 7–84. ASM press, Washington DC.Google Scholar
Vizoso, D. B. and Ebert, D. (2005). Phenotypic plasticity of host-parasite interactions in response to the route of infection. Journal of Evolutionary Biology 18, 911–921.Google Scholar
Vorontsova, L., Tokarev, S., Sokolova, Y. Y. and Glupov, V. V. (2004). Microsporidiosis in the wax moth Galleria mellonella (Lepidoptera: Pyralidae) caused by Vairimorpha ephestiae (Microsporidia: Burenellidae). Parazitologiia 38, 239–50.Google ScholarPubMed
Vossbrinck, C. R., Maddox, J. V., Friedman, S., Debruner-Vossbrink, B. A., Vossbrinck, C. R., Andreadis, T. G., Vavra, J. and Becnel, J. J. (2004). Molecular phylogeny and evolution of mosquito parasitic Microsporidia (Microsporidia: Amblyosporidae). Journal of Eukaryotic Microbiology 51, 88–95.Google Scholar
Vossbrinck, C. R., Maddox, T. J., Friedman, S., Debrunner-Vossbrinck, B. A. and Woese, C. R. (1987). Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326, 411–414.Google Scholar
Vossbrinck, C. R. and Debrunner-Vossbrinck, B. A. (2005). Molecular phylogeny of the microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitologica 52, 131–142.Google Scholar
Watanabe, M. E. (2008). Colony collapse disorder: Many suspects, no smoking gun. Bioscience 58, 384–388.Google Scholar
Wattier, R. A., Haine, E. R., Beguet, J., Martin, G., Bollache, L., Muskó, 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.Google Scholar
Webster, J. D., Miller, M. A. and Vemulapalli, R. (2008). Encephalitozoon cuniculi-associated placentitis and perinatal death in an alpaca (Lama pacos). Veterinary Parasitology 45, 255–259.Google Scholar
Webster, T. C., Pomper, K. W., Hunt, G., Thacker, E. M. and Jones, S. C. (2004). Nosema apis infection in worker and queen Apis mellifera. Apidologie 35, 49–54.CrossRefGoogle Scholar
Webster, T. C., Thacker, E. M., Pomper, K., Lowe, J. and Hunt, G. (2008). Nosema apis infection in honey bee (Apis mellifera) queens. Journal of Apiculture Research 47, 53–57.Google Scholar
Weedall, R. T., Robinson, M., Smith, J. E. and Dunn, A. M. (2006). Distribution of two vertically transmitted, feminising microsporidia during host embryogenesis. International Journal for Parasitology 36, 749–756.Google Scholar
Williams, B. A., Hirt, R. P., Lucocq, J. M. and Embley, T. M. (2002). A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418, 865–869.CrossRefGoogle ScholarPubMed
Williams, B. A., Slamovits, C. H., Patron, N. J., Fast, N. M. and Keeling, P. J. (2005). A high frequency of overlapping gene expression in compacted eukaryotic genomes. Proceedings of the National Academy of Sciences, USA 102, 10936–10941.CrossRefGoogle ScholarPubMed
Woese, C. R. (1987). Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326, 411–414.Google Scholar
Xu, J., Pan, G., Fang, L., Li, J., Tian, X., Li, T., Zhou, Z. and Xiang, Z. (2006). The varying microsporidian genome: Existence of long-terminal repeat retrotransposon in domesticated silkworm parasite Nosema bombycis. International Journal for Parasitology 36, 1049–1056.CrossRefGoogle ScholarPubMed
Xu, Y. and Weiss, L. M. (2008). The microsporidian polar tube: A highly specialised invasion organelle. International Journal for Parasitology 35, 941–953.Google Scholar