The ecology and evolution of microsporidian parasites

Parasitology

Volumn 136, Issue 14, 2009, Pages 1901-1914

  Smith, J E ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

ecology; evolution; Microspora; Microsporidia; vertical transmission

Indexed keywords

ADAPTIVE IMMUNITY; ECOLOGY; EUROPEAN CORN BORER; EVOLUTION; GENE ASSIGNMENT; GENOMICS; HOST; HOST PARASITE INTERACTION; HOST RANGE; LIFE CYCLE; MICROSPORIDIA; MICROSPORIDIOSIS; NONHUMAN; PARASITE ISOLATION; PHENOTYPE; PHYLOGENY; PHYLUM; PRIORITY JOURNAL; REVIEW; SEX RATIO; VERTICAL TRANSMISSION; ANIMAL; CLASSIFICATION; DISEASE TRANSMISSION; ECOSYSTEM; GENETICS; HUMAN; INVERTEBRATE; MOLECULAR EVOLUTION; PARASITOLOGY; PHYSIOLOGY;

MICROSPORIDIA;

ANIMALS; DISEASE TRANSMISSION, INFECTIOUS; ECOSYSTEM; EVOLUTION, MOLECULAR; HOST-PARASITE INTERACTIONS; HUMANS; INVERTEBRATES; LIFE CYCLE STAGES; MICROSPORIDIA; MICROSPORIDIOSIS; PHYLOGENY;

EID: 77449139075     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182009991818     Document Type: Review

References (137)

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. Baneux, J. R. and Pognan, F. (2003). In utero transmission of Encephalitozoon cuniculi strain type I in rabbits. Laboratory Animal 37, 132-138. (Pubitemid 36470101)
7. 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.
8. 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.
9. 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. (Pubitemid 350116687)
10. 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. (Pubitemid 28281555)
11. 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.
12. 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. (Pubitemid 40047804)
13. 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.
14. 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. (Pubitemid 35255325)
15. 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.
16. 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. (Pubitemid 47574857)
17. Crawford, G. I. (1937). An amphipod, Eucrangonyx gracilis S. I. Smith, new to Britain. Nature 139, 327.
18. 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. (Pubitemid 10010510)
19. 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.
20. Didier, E. S. (2005), Microsporidiosis: An emerging and opportunistic infection in humans and animals. Acta Tropica 94, 61-76.
21. 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.
22. 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.
23. 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. (Pubitemid 223036658)
24. 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.
25. 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.
26. Dunn, A. M., Terry, R. S. and Smith, J. E. (2001). Transovarial transmission in the Microsporidia. Advances in Parasitology 48, 57-101.
27. 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.
28. 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.
29. 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.
30. 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. (Pubitemid 351629915)
31. 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.
32. Fries, I. and Camazine, S. (2001). Implications of horizontal and vertical pathogen transmission for honey bee epidemiology. Apidologie 32, 199-214. (Pubitemid 32606080)
33. 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. (Pubitemid 33702819)
34. 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. (Pubitemid 26380633)
35. Fries, I., Granados, R. R. and Morse, R. A. (1992). Intracellular germination of Nosema apis Z. Apidologie 23, 61-70.
36. 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 populationofthe red importedfire ant, Solenopsis invicta. Journal of Invertebrate Pathology 88, 79-82.
37. Gill, E. E., Becnel, J. J. and Fast, N. M. (2008). ESTs from the microsporidian Edhazardia aedis. BMC Genomics 9, 296.
38. 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.
39. 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.
40. 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. (Pubitemid 351483354)
41. 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. (Pubitemid 39222047)
42. 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. (Pubitemid 47236800)
43. 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.
44. 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. (Pubitemid 36435040)
45. 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.
46. 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. (Pubitemid 29061251)
47. 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. (Pubitemid 37379275)
48. 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. (Pubitemid 351952018)
49. Ishihara, R. (1969). Life cycle of Nosema bombycis as revealed in tissue culture cells of Bombyx mori. Journal of Invertebrate Pathology 14, 316-320.
50. 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.
51. 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.
52. 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.
53. 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., Schü ssler, 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. (Pubitemid 44622687)
54. 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.
55. 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.
56. 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. (Pubitemid 34173726)
57. Katznelson, H. and Jamieson, C. A. (1952). Control of Nosema disease in honey bees with fumagillin. Science 115, 70-71.
58. Keeling, P. J. and Fast, N. M. (2002). Microsporidia: Biology and evolution of highly reduced intracellular parasites. Annual Review of Microbiology 56, 93-116.
59. 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.
60. 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.
61. 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. (Pubitemid 47260581)
62. Lange, C. E. (2005). The host and geographical range of the grasshopper pathogen Paranosema (Nosema) locustae revisited. Journal of Orthopteran Research 14, 137-141.
63. 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.
64. 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.
65. 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.
66. Liu, T. P. (1992). Oocytes degeneration in the queen honey bee after infection by Nosema apis. Tissue and Cell 24, 131-138.
67. 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.
68. Lom, J. and Nilsen, F. (2003). Fish microsporidia: fine structural diversity and phylogeny. International Journal for Parasitology 33, 107-127. (Pubitemid 36298982)
69. 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. (Pubitemid 32905587)
70. 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. (Pubitemid 32305003)
71. 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.
72. Malone, L. A. and McIvor, C. A. (1993). Pulsed-field electrophoresis of DNA from four microsporidian isolates. Journal of Invertebrate Pathology 61, 203-205. (Pubitemid 223036175)
73. 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.
74. 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.
75. 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. (Pubitemid 41219715)
76. Micieli, M. V., Garcia, J. J. and Becnel, J. J. (2000). Horizontal transmission of Amblyospora albifasciati Garćia 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.
77. 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.
78. 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.
79. 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.
80. Otti, O. and Schmid-Hempel, P. (2007). Nosema bombi: A pollinator parasite with detrimental fitness effects. Journal of Invertebrate Pathology 96, 118-124. (Pubitemid 47390699)
81. Otterstatter, M. C. and Thomson, J. D. (2008). Does pathogen spillover from commercially reared bumble bees threaten wild pollinators? PloS One 3, 1-9.
82. 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.
83. 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. (Pubitemid 351440007)
84. Paxton, R. J., Klee, J., Korpela, S. and Fries, I. (2007). Nosema ceranae has infected Apis mellifera in Europe sinceat least 1998 and may be more virulent than Nosema apis. Apidologie 38, 558-565. (Pubitemid 351282136)
85. 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.
86. 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. (Pubitemid 24363558)
87. 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. (Pubitemid 47595331)
88. 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. (Pubitemid 41223900)
89. 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.
90. 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. (Pubitemid 351961579)
91. 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.
92. 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.
93. 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. (Pubitemid 28153648)
94. 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.
95. 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.
96. 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. (Pubitemid 38231427)
97. 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.
98. 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.
99. 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.
100. 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.
101. 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.
102. 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.
103. Solter, L. F., Pilarska, D. K. and Vossbrinck, C. F. (2000). Host specificity of microsporidia pathogenic to forest Lepidoptera. Biological Control 19, 48-56.
104. 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.
105. 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.
106. Sprague, V., Becnel, J. J. and Hazard, E. I. (1992). Taxonomy of phylum Microspora. Critical Reviews in Microbiology 18, 285-395. (Pubitemid 23037202)
107. 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. (Pubitemid 46306237)
108. Streett, D. A. (1994). Analysis of Nosema locustae (microsporidia: Nosematidae) chromosomal DNA with pulsed-field gel electrophoresis. Journal of Invertebrate Pathology 63, 301-303.
109. 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.
110. Terry, R. S., Dunn, A. M. and Smith, J. E. (1999). Segregation of a cytoplasmic parasite during host cell mitosis. Parasitology 118, 43-48.
111. 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. (Pubitemid 29471721)
112. 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.
113. 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. (Pubitemid 40502731)
114. 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. (Pubitemid 351273723)
115. 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.
116. 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.
117. 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.
118. 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.
119. 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.
120. 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. (Pubitemid 43990871)
121. 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.
122. 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. (Pubitemid 40968544)
123. 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.
124. 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). Journalof Eukaryotic Microbiology 51, 88-95. (Pubitemid 38236024)
125. 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. (Pubitemid 17053774)
126. Vossbrinck, C. R. and Debrunner-Vossbrinck, B. A. (2005). Molecular phylogeny of the microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitologica 52, 131-142.
127. Watanabe, M. E. (2008). Colony collapse disorder: Many suspects, no smoking gun. Bioscience 58, 384-388.
128. 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. (Pubitemid 47568754)
129. 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. (Pubitemid 351571661)
130. 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. (Pubitemid 38143356)
131. 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. (Pubitemid 351440001)
132. 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. (Pubitemid 43866074)
133. 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.
134. 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.
135. Woese, C. R. (1987). Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326, 411-414.
136. 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. (Pubitemid 44164330)
137. Xu, Y. and Weiss, L. M. (2008). The microsporidian polar tube: A highly specialised invasion organelle. International Journal for Parasitology 35, 941-953. (Pubitemid 41074072)