Chapter 5 : Microsporidia: Obligate Intracellular Pathogens Within the Fungal Kingdom

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Microsporidia were initially described about 150 years ago with the identification of as the organism responsible for the disease pébrine in silkworms ( ). Microsporidia are ubiquitous in the environment and infect almost all invertebrates and vertebrates, as well as some protists ( ). Spores from microsporidia are commonly found in surface water ( ). These organisms are eukaryotes that have a nucleus with a nuclear envelope, an intracytoplasmic membrane system, chromosome separation on mitotic spindles, vesicular Golgi, and a mitochondrial remnant organelle lacking a genome termed a mitosome ( ). For insects, fish, laboratory rodents, and rabbits microsporidia are important pathogens, and they have been investigated as biological control agents for destructive species of insects ( ). Several species of microsporidia have caused significant agricultural economic losses including and in honeybees ( ), in salmonid fish ( ), and species in shrimp ( ). Franzen ( ) published an excellent review of the history of research on these pathogens, and a recent textbook by Weiss and Becnel ( ) provides a comprehensive examination of what is known about these organisms. In 1977 Sprague elevated the class or order Microsporidia to the phylum Microspora ( ), and a decade later Sprague and Becnel ( ) suggested that the term Microsporidia should instead be used for the phylum name. These organisms were previously considered “primitive” protozoa ( ), but molecular phylogenetic analysis has resulted in the insight that these organisms are not primitive but instead are degenerate, and that Microsporidia are related to the Fungi, either as a basal branch of the Fungi or as a sister group ( ).

Citation: Han B, Weiss L. 2017. Microsporidia: Obligate Intracellular Pathogens Within the Fungal Kingdom, p 97-113. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0018-2016
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Image of Figure 1
Figure 1

Microsporidian life cycles. The initial phase of infection involves spores being exposed to the proper environmental conditions that cause germination of the spores and polar tube extrusion. The polar tube pierces the plasma membrane (solid black line) of the host cell, and the sporoplasm travels through the polar tube into the host cell. The sporoplasm then divides during the proliferative phase, and the morphology of this division is used for determination of microsporidian genera. The sporoplasm on the left is uninucleate, and the cells that are produced from it represent the developmental patterns of several microsporidia with isolated nuclei. The sporoplasm on the right is diplokaryotic, and it similarly produces the various diplokaryotic developmental patterns. Cells containing either type of nucleation will produce one of three basic developmental forms. Some cycles have cells that divide immediately after karyokinesis by binary fission (e.g., ). A second type forms elongated moniliform multinucleate cells that divide by multiple fission (e.g., some species). The third type forms rounded plasmodial multinucleate cells that divide by plasmotomy (e.g., species). Cells may repeat their division cycles one to several times in the proliferative phase. The intracellular stages in this phase are usually in direct contact with the host cell cytoplasm or closely abutted to the host endoplasmic reticulum; however, the proliferative cells of (and probably ) are surrounded by a host-formed parasitophorous vacuole throughout their development, and the proliferative plasmodium of the genus is surrounded by a thick layer of parasite secretions that becomes the sporophorous vesicle in the sporogonic phase. The sporogonic phase is illustrated below the dashed line. Some of the microsporidian genera maintain direct contact with the host cell cytoplasm during sporogony, i.e., , , , , and probably . The remaining genera form a sporophorous vesicle as illustrated by the circles around developing sporogonial stages. It should be noted that in the cycle and the -like part of the cycle, the diplokarya separate and continue their development as cells with isolated nuclei. Adapted with permission from reference .

Citation: Han B, Weiss L. 2017. Microsporidia: Obligate Intracellular Pathogens Within the Fungal Kingdom, p 97-113. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0018-2016
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Image of Figure 2
Figure 2

Diagram of a microsporidian spore. Spores range in size from 1 to 10 μm. The spore coat consists of an electron-dense exospore (Ex), an electron-lucent endospore (En), and a plasma membrane (Pm). It is thinner at the anterior end of the spore. The sporoplasm (Sp) contains a single nucleus (Nu), the posterior vacuole (PV), and ribosomes. The polar filament is attached to the anterior end of the spore by an anchoring disc (AD) and is divided into two regions: the manubroid, or straight portion (M), and the posterior region forming five coils (PT) around the sporoplasm. The manubroid polar filament is surrounded by the lamellar polaroplast (Pl) and vesicular polaroplast (VPl). The insert depicts a cross section of the polar tube coils (five coils in this spore), demonstrating the various concentric layers of different electron density and electron-dense core present in such cross sections. Reprinted with permission from reference .

Citation: Han B, Weiss L. 2017. Microsporidia: Obligate Intracellular Pathogens Within the Fungal Kingdom, p 97-113. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0018-2016
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Image of Figure 3
Figure 3

Scanning electron micrograph of microsporidia infection of a host cell shows the extruded polar tube of a spore of piercing and infecting Vero E6 green monkey kidney cells in tissue culture. Reprinted with permission from reference and with the kind permission of N. P. Kock, C. Schmetz, and J. Schottelius, Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany; published in Kock NP. 1998. Diagnosis of human pathogen microsporidia (dissertation).

Citation: Han B, Weiss L. 2017. Microsporidia: Obligate Intracellular Pathogens Within the Fungal Kingdom, p 97-113. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0018-2016
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1. Pasteur L . 1870. Études sur la maladie des vers à soie [M]. Paris, Gauthier-Villars, successeur de Mallet-Bachelier 1870 : 148 168.
2. Weiss LM,, Becnel JJ (ed) . 2014. Microsporidia: Pathogens of Opportunity. Wiley-Blackwell, Oxford, United Kingdom.[CrossRef]
3. Izquierdo F,, Castro Hermida JA,, Fenoy S,, Mezo M,, González-Warleta M,, del Aguila C . 2011. Detection of microsporidia in drinking water, wastewater and recreational rivers. Water Res 45 : 4837 4843.[CrossRef] [PubMed]
4. Williams BA,, Hirt RP,, Lucocq JM,, Embley TM . 2002. A mitochondrial remnant in the microsporidian Trachipleistophora hominis . Nature 418 : 865 869.[CrossRef] [PubMed]
5. Fries I . 1993. Nosema apis: a parasite in the honey bee colony. Bee World 74 : 5 19.[CrossRef]
6. Kent ML,, Elliott DG,, Groff JM,, Hedrick RP . 1989. Loma salmonae (Protozoa: Microspora) infections in seawater reared coho salmon Oncorhynchus kisutch . Aquaculture 80 : 211 222.[CrossRef]
7. Overstreet RM . 1973. Parasites of some penaeid shrimps with emphasis on reared hosts. Aquaculture 2 : 105 140.[CrossRef]
8. Franzen C . 2008. Microsporidia: a review of 150 years of research. Open Parasitol J 2 : 1 34.[CrossRef]
9. Sprague V . 1977. Systematics of the Microsporidia, vol. 2. Biology of the Microsporidia. Comparative Biology series. Plenum Press, New York, NY.
10. Sprague V,, Becnel JJ . 1998. Note on the name-author-date combination for the taxon Microsporidies Balbiani, 1882, when ranked as a phylum. J Invertebr Pathol 71 : 91 94.[CrossRef] [PubMed]
11. Vossbrinck CR,, Maddox JV,, Friedman S,, Debrunner-Vossbrinck BA,, Woese CR . 1987. Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326 : 411 414.[CrossRef] [PubMed]
12. Weiss LM,, Edlind TD,, Vossbrinck CR,, Hashimoto T . 1999. Microsporidian molecular phylogeny: the fungal connection. J Eukaryot Microbiol 46 : 17S 18S.[PubMed]
13. Capella-Gutiérrez S,, Marcet-Houben M,, Gabaldón T . 2012. Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi. BMC Biol 10 : 47.[CrossRef] [PubMed]
14. Lee SC,, Corradi N,, Byrnes EJ III,, Torres-Martinez S,, Dietrich FS,, Keeling PJ,, Heitman J . 2008. Microsporidia evolved from ancestral sexual fungi. Curr Biol 18 : 1675 1679.[CrossRef] [PubMed]
15. Corsaro D,, Michel R,, Walochnik J,, Venditti D,, Müller KD,, Hauröder B,, Wylezich C . 2016. Molecular identification of Nucleophaga terricolae sp. nov. (Rozellomycota), and new insights on the origin of the Microsporidia. Parasitol Res 115 : 3003 3011.[CrossRef]
16. James TY , , et al . 2006. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443 : 818 822.[CrossRef] [PubMed]
17. Weber R,, Bryan RT,, Schwartz DA,, Owen RL . 1994. Human microsporidial infections. Clin Microbiol Rev 7 : 426 461.[CrossRef] [PubMed]
18. Troemel ER,, Félix M-A,, Whiteman NK,, Barrière A,, Ausubel FM . 2008. Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans . PLoS Biol 6 : e309.[CrossRef] [PubMed]
19. Ma Z,, Li C,, Pan G,, Li Z,, Han B,, Xu J,, Lan X,, Chen J,, Yang D,, Chen Q,, Sang Q,, Ji X,, Li T,, Long M,, Zhou Z . 2013. Genome-wide transcriptional response of silkworm ( Bombyx mori) to infection by the microsporidian Nosema bombycis . PLoS One 8 : e84137.[CrossRef] [PubMed]
20. Antúnez K,, Martín-Hernández R,, Prieto L,, Meana A,, Zunino P,, Higes M . 2009. Immune suppression in the honey bee ( Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ Microbiol 11 : 2284 2290.[CrossRef]
21. Weber R,, Deplazes P,, Schwartz D . 2000. Diagnosis and clinical aspects of human microsporidiosis. Contrib Microbiol 6 : 166 192.[CrossRef] [PubMed]
22. Coyle CM,, Weiss LM,, Rhodes LV III,, Cali A,, Takvorian PM,, Brown DF,, Visvesvara GS,, Xiao L,, Naktin J,, Young E,, Gareca M,, Colasante G,, Wittner M . 2004. Fatal myositis due to the microsporidian Brachiola algerae, a mosquito pathogen. N Engl J Med 351 : 42 47.[CrossRef] [PubMed]
23. Texier C,, Vidau C,, Viguès B,, El Alaoui H,, Delbac F . 2010. Microsporidia: a model for minimal parasite-host interactions. Curr Opin Microbiol 13 : 443 449.[CrossRef] [PubMed]
24. Desportes I,, Le Charpentier Y,, Galian A,, Bernard F,, Cochand-Priollet B,, Lavergne A,, Ravisse P,, Modigliani R . 1985. Occurrence of a new microsporidan: Enterocytozoon bieneusi n.g., n. sp., in the enterocytes of a human patient with AIDS. J Protozool 32 : 250 254.[CrossRef]
25. Weiss LM,, Vossbrinck CR . 1998. Microsporidiosis: molecular and diagnostic aspects. Adv Parasitol 40 : 351 395.[CrossRef]
26. Didier ES,, Weiss LM . 2011. Microsporidiosis: not just in AIDS patients. Curr Opin Infect Dis 24 : 490 495.[CrossRef] [PubMed]
27. Didier ES,, Varner PW,, Didier PJ,, Aldras AM,, Millichamp NJ,, Murphey-Corb M,, Bohm R,, Shadduck JA . 1994. Experimental microsporidiosis in immunocompetent and immunodeficient mice and monkeys. Folia Parasitol (Praha) 41 : 1 11.[PubMed]
28. Ghosh K,, Weiss LM . 2012. T cell response and persistence of the microsporidia. FEMS Microbiol Rev 36 : 748 760.[CrossRef] [PubMed]
29. Khan IA,, Moretto M,, Weiss LM . 2001. Immune response to Encephalitozoon cuniculi infection. Microbes Infect 3 : 401 405.[CrossRef]
30. Mathews A,, Hotard A,, Hale-Donze H . 2009. Innate immune responses to Encephalitozoon species infections. Microbes Infect 11 : 905 911.[CrossRef] [PubMed]
31. Ombrouck C,, Gneragbe T,, Charlotte F,, Rénia L,, Desportes-Livage I,, Mazier D . 1996. Experimental model for human intestinal microsporidiosis in interferon gamma receptor knockout mice infected by Encephalitozoon intestinalis . Parasite Immunol 18 : 387 392.[CrossRef] [PubMed]
32. Khan IA,, Schwartzman JD,, Kasper LH,, Moretto M . 1999. CD8+ CTLs are essential for protective immunity against Encephalitozoon cuniculi infection. J Immunol 162 : 6086 6091.[PubMed]
33. Moretto MM,, Khan IA,, Weiss LM . 2012. Gastrointestinal cell mediated immunity and the microsporidia. PLoS Pathog 8 : e1002775.[CrossRef] [PubMed]
34. Moretto MM,, Lawlor EM,, Khan IA . 2010. Lack of interleukin-12 in p40-deficient mice leads to poor CD8+ T-cell immunity against Encephalitozoon cuniculi infection. Infect Immun 78 : 2505 2511.[CrossRef] [PubMed]
35. Hermánek J,, Koudela B,, Kucerová Z,, Ditrich O,, Trávnícek J . 1993. Prophylactic and therapeutic immune reconstitution of SCID mice infected with Encephalitozoon cuniculi . Folia Parasitol (Praha) 40 : 287 291.
36. Schmidt EC,, Shadduck JA . 1984. Mechanisms of resistance to the intracellular protozoan Encephalitozoon cuniculi in mice. J Immunol 133 : 2712 2719.[PubMed]
37. Wong P,, Pamer EG . 2003. CD8 T cell responses to infectious pathogens. Annu Rev Immunol 21 : 29 70.[CrossRef] [PubMed]
38. Moretto M,, Weiss LM,, Khan IA . 2004. Induction of a rapid and strong antigen-specific intraepithelial lymphocyte response during oral Encephalitozoon cuniculi infection. J Immunol 172 : 4402 4409.[CrossRef] [PubMed]
39. Moretto MM,, Weiss LM,, Combe CL,, Khan IA . 2007. IFN-γ-producing dendritic cells are important for priming of gut intraepithelial lymphocyte response against intracellular parasitic infection. J Immunol 179 : 2485 2492.[CrossRef]
40. Moretto MM,, Lawlor EM,, Khan IA . 2008. Aging mice exhibit a functional defect in mucosal dendritic cell response against an intracellular pathogen. J Immunol 181 : 7977 7984.[CrossRef]
41. Schmidt EC,, Shadduck JA . 1983. Murine encephalitozoonosis model for studying the host-parasite relationship of a chronic infection. Infect Immun 40 : 936 942.
42. Sak B,, Salát J,, Horká H,, Saková K,, Ditrich O . 2006. Antibodies enhance the protective effect of CD4+ T lymphocytes in SCID mice perorally infected with Encephalitozoon cuniculi . Parasite Immunol 28 : 95 99.[CrossRef]
43. Bywater JE,, Kellett BS . 1979. Humoral immune response to natural infection with Encephalitozoon cuniculi in rabbits. Lab Anim 13 : 293 297.[CrossRef] [PubMed]
44. Silveira H,, Canning EU . 1995. Vittaforma corneae n. comb. for the human microsporidium Nosema corneum Shadduck, Meccoli, Davis & Font, 1990, based on its ultrastructure in the liver of experimentally infected athymic mice. J Eukaryot Microbiol 42 : 158 165.[CrossRef]
45. Cali A,, Takvorian PM,, Lewin S,, Rendel M,, Sian CS,, Wittner M,, Tanowitz HB,, Keohane E,, Weiss LM . 1998. Brachiola vesicularum, n. g., n. sp., a new microsporidium associated with AIDS and myositis. J Eukaryot Microbiol 45 : 240 251.[CrossRef]
46. Franzen C,, Nassonova ES,, Schölmerich J,, Issi IV . 2006. Transfer of the members of the genus Brachiola (microsporidia) to the genus Anncaliia based on ultrastructural and molecular data. J Eukaryot Microbiol 53 : 26 35.[PubMed] [CrossRef]
47. Cali A,, Weiss LM,, Takvorian PM . 2005. A review of the development of two types of human skeletal muscle infections from microsporidia associated with pathology in invertebrates and cold-blooded vertebrates. Folia Parasitol (Praha) 52 : 51 61.[CrossRef]
48. Weber R,, Bryan RT . 1994. Microsporidial infections in immunodeficient and immunocompetent patients. Clin Infect Dis 19 : 517 521.[CrossRef]
49. Didier ES,, Didier PJ,, Friedberg DN,, Stenson SM,, Orenstein JM,, Vee RW,, Tio FO,, Davis RM,, Vossbrinck C,, Millichamp N,, Shadduck JA . 1991. Isolation and characterization of a new human microsporidian, Encephalitozoon hellem (n. sp.), from three AIDS patients with keratoconjunctivitis. J Infect Dis 163 : 617 621.[CrossRef]
50. Cali A,, Kotler DP,, Orenstein JM . 1993. Septata intestinalis N. G., N. Sp., an intestinal microsporidian associated with chronic diarrhea and dissemination in AIDS patients. J Eukaryot Microbiol 40 : 101 112.[CrossRef]
51. Hartskeerl RA,, Van Gool T,, Schuitema AR,, Didier ES,, Terpstra WJ . 1995. Genetic and immunological characterization of the microsporidian Septata intestinalis Cali, Kotler and Orenstein, 1993: reclassification to Encephalitozoon intestinalis . Parasitology 110 : 277 285.[CrossRef] [PubMed]
52. Vávra J,, Yachnis AT,, Shadduck JA,, Orenstein JM . 1998. Microsporidia of the genus Trachipleistophora: causative agents of human microsporidiosis: description of Trachipleistophora anthropophthera n. sp. (Protozoa: Microsporidia). J Eukaryot Microbiol 45 : 273 283.[CrossRef]
53. Yachnis AT,, Berg J,, Martinez-Salazar A,, Bender BS,, Diaz L,, Rojiani AM,, Eskin TA,, Orenstein JM . 1996. Disseminated microsporidiosis especially infecting the brain, heart, and kidneys. Report of a newly recognized pansporoblastic species in two symptomatic AIDS patients. Am J Clin Pathol 106 : 535 543.[CrossRef]
54. Field AS,, Marriott DJ,, Milliken ST,, Brew BJ,, Canning EU,, Kench JG,, Darveniza P,, Harkness JL . 1996. Myositis associated with a newly described microsporidian, Trachipleistophora hominis, in a patient with AIDS. J Clin Microbiol 34 : 2803 2811.[PubMed]
55. Meissner EG,, Bennett JE,, Qvarnstrom Y,, da Silva A,, Chu EY,, Tsokos M,, Gea-Banacloche J . 2012. Disseminated microsporidiosis in an immunosuppressed patient. Emerg Infect Dis 18 : 1155 1158.[CrossRef] [PubMed]
56. Choudhary MM,, Metcalfe MG,, Arrambide K,, Bern C,, Visvesvara GS,, Pieniazek NJ,, Bandea RD,, Deleon-Carnes M,, Adem P,, Choudhary MM,, Zaki SR,, Saeed MU . 2011. Tubulinosema sp. microsporidian myositis in immunosuppressed patient. Emerg Infect Dis 17 : 1727 1730.[CrossRef] [PubMed]
57. Suankratay C,, Thiansukhon E,, Nilaratanakul V,, Putaporntip C,, Jongwutiwes S . 2012. Disseminated infection caused by novel species of Microsporidium, Thailand. Emerg Infect Dis 18 : 302 304.[CrossRef] [PubMed]
58. Costa SF,, Weiss LM . 2000. Drug treatment of microsporidiosis. Drug Resist Updat 3 : 384 399.[CrossRef] [PubMed]
59. Maggi P,, Larocca AM,, Quarto M,, Serio G,, Brandonisio O,, Angarano G,, Pastore G . 2000. Effect of antiretroviral therapy on cryptosporidiosis and microsporidiosis in patients infected with human immunodeficiency virus type 1. Eur J Clin Microbiol Infect Dis 19 : 213 217.[CrossRef] [PubMed]
60. Goguel J,, Katlama C,, Sarfati C,, Maslo C,, Leport C,, Molina JM . 1997. Remission of AIDS-associated intestinal microsporidiosis with highly active antiretroviral therapy. AIDS 11 : 1658 1659.[PubMed]
61. Akiyoshi DE,, Weiss LM,, Feng X,, Williams BA,, Keeling PJ,, Zhang Q,, Tzipori S . 2007. Analysis of the beta-tubulin genes from Enterocytozoon bieneusi isolates from a human and rhesus macaque. J Eukaryot Microbiol 54 : 38 41.[CrossRef]
62. Franzen C,, Salzberger B . 2008. Analysis of the beta-tubulin gene from Vittaforma corneae suggests benzimidazole resistance. Antimicrob Agents Chemother 52 : 790 793.[CrossRef]
63. Didier PJ,, Phillips JN,, Kuebler DJ,, Nasr M,, Brindley PJ,, Stovall ME,, Bowers LC,, Didier ES . 2006. Antimicrosporidial activities of fumagillin, TNP-470, ovalicin, and ovalicin derivatives in vitro and in vivo . Antimicrob Agents Chemother 50 : 2146 2155.[CrossRef]
64. Molina JM,, Tourneur M,, Sarfati C,, Chevret S,, de Gouvello A,, Gobert JG,, Balkan S,, Derouin F , Agence Nationale de Recherches sur le SIDA 090 Study Group . 2002. Fumagillin treatment of intestinal microsporidiosis. N Engl J Med 346 : 1963 1969.[CrossRef]
65. Bicart-Sée A,, Massip P,, Linas MD,, Datry A . 2000. Successful treatment with nitazoxanide of Enterocytozoon bieneusi microsporidiosis in a patient with AIDS. Antimicrob Agents Chemother 44 : 167 168.[CrossRef] [PubMed]
66. Canning EU . 1970. Transmission of microsporida. Proc Int Colloq InsectPathol 4 : 415 424.
67. Canning EU . 1991. Phylum Microspora. Jones and Bartlett, Boston, MA.
68. Didier ES . 2005. Microsporidiosis: an emerging and opportunistic infection in humans and animals. Acta Trop 94 : 61 76.[CrossRef] [PubMed]
69. Vavra J, . 1976. Structure of the microsporidia, p 1 85. In Bulla LA,, Cheng TC,, Vavra J,, Sprague V (ed), Biology of the Microsporidia, Series: Comparative Biology, vol 1. Plenum Press, New York, NY.
70. Wittner MW L . 1999. The Microsporidia and Microsporidiosis, ASM Press, Washington, DC.
71. Lom J . 1972. On the structure of the extruded microsporidian polar filament. Z Parasitenkd 38 : 200 213.[CrossRef]
72. Weidner E . 1971. Cell invasion by microsporidian spores: an ultrastructural study. J Protozool 18( Suppl.) : 13 14.
73. Weidner E . 1972. Ultrastructural study of microsporidian invasion into cells. Z Parasitenkd 40 : 227 242.[PubMed]
74. Franzen C . 2005. How do microsporidia invade cells? Folia Parasitol (Praha) 52 : 36 40.[CrossRef] [PubMed]
75. Keohane E,, Weiss LM, . 1999. The structure, function, and composition of the microsporidian polar tube, p 196 224. In Wittner M,, Weiss LM (ed), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC.[CrossRef]
76. Undeen AH,, ElGazzar LM,, Vandermeer RK,, Narang S . 1987. Trehalose levels and trehalase activity in germinated and ungerminated spores of Nosema algerae (Microspora: nosematidae). J Invertebr Pathol 50 : 230 237.[CrossRef]
77. Frixione E,, Ruiz L,, Cerbón J,, Undeen AH . 1997. Germination of Nosema algerae (Microspora) spores: conditional inhibition by D2O, ethanol and Hg2+ suggests dependence of water influx upon membrane hydration and specific transmembrane pathways. J Eukaryot Microbiol 44 : 109 116.[CrossRef]
78. Undeen AH,, Vander Meer RK . 1999. Microsporidian intrasporal sugars and their role in germination. J Invertebr Pathol 73 : 294 302.[CrossRef]
79. Tuzet O,, Maurand J,, Fize JA,, Michel R,, Fenwick B . 1971. Proposition d’un nouveau cadre systematique pour les genres de Microsporidies. C R Acad Sci III 272 : 1268 1271.
80. Larsson JIR . 1988. Identification of micrsporidian genera (Protozoa, Microspora): a guide with comments on the taxonomy. Arch Protistenkd 136 : 1 37.[CrossRef]
81. Issi IV . 1986. Microsporidia as a phylum of parasitic protozoa. Protozoology 10 : 6 135. (In Russian.)
82. Weiser J . 1977. A proposal of the basis for microsporidian taxonomy. Proc Int Congr Protozool 5 : 267.
83. Sprague V,, Becnel JJ,, Hazard EI . 1992. Taxonomy of phylum microspora. Crit Rev Microbiol 18 : 285 395.[CrossRef] [PubMed]
84. Baker MD,, Vossbrinck CR,, Maddox JV,, Undeen AH . 1994. Phylogenetic relationships among Vairimorpha and Nosema species (Microspora) based on ribosomal RNA sequence data. J Invertebr Pathol 64 : 100 106.[CrossRef]
85. Franzen C,, Müller A . 1999. Molecular techniques for detection, species differentiation, and phylogenetic analysis of microsporidia. Clin Microbiol Rev 12 : 243 285.[PubMed]
86. Curgy JJ,, Vavra J,, Vivares C . 1980. Presence of ribosomal RNAs with prokaryotic properties in Microsporidia, eukaryotic organisms. Biol Cell 38 : 49 52.
87. Vossbrinck CR,, Woese CR . 1986. Eukaryotic ribosomes that lack a 5.8S RNA. Nature 320 : 287 288.[CrossRef] [PubMed]
88. Azevedo C,, Corral L,, Vivarès CP . 2000. Ultrastructure of the microsporidian Inodosporus octospora (Thelohaniidae), a parasite of the shrimp Palaemon serratus (Crustacea, Decapoda). Dis Aquat Organ 41 : 151 158.[CrossRef]
89. Weiss LM . 2000. Molecular phylogeny and diagnostic approaches to microsporidia. Contrib Microbiol 6 : 209 235.[CrossRef] [PubMed]
90. Ndikumana S,, Pelin A,, Williot A,, Sanders JL,, Kent M,, Corradi N . 2016. Genome analysis of Pseudoloma neurophilia: a microsporidian parasite of zebrafish (Danio rerio). J Eukaryot Microbiol. [Epub ahead of print.][CrossRef].
91. Katinka MD,, Duprat S,, Cornillot E,, Méténier G,, Thomarat F,, Prensier G,, Barbe V,, Peyretaillade E,, Brottier P,, Wincker P,, Delbac F,, El Alaoui H,, Peyret P,, Saurin W,, Gouy M,, Weissenbach J,, Vivarès CP . 2001. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi . Nature 414 : 450 453.[CrossRef] [PubMed]
92. Corradi N . 2015. Microsporidia: eukaryotic intracellular parasites shaped by gene loss and horizontal gene transfers. Annu Rev Microbiol 69 : 167 183.[CrossRef] [PubMed]
93. Corradi N,, Akiyoshi DE,, Morrison HG,, Feng X,, Weiss LM,, Tzipori S,, Keeling PJ . 2007. Patterns of genome evolution among the microsporidian parasites Encephalitozoon cuniculi, Antonospora locustae and Enterocytozoon bieneusi . PLoS One 2 : e1277.[CrossRef]
94. Corradi N,, Pombert JF,, Farinelli L,, Didier ES,, Keeling PJ . 2010. The complete sequence of the smallest known nuclear genome from the microsporidian Encephalitozoon intestinalis . Nat Commun 1 : 77.[CrossRef]
95. Corradi N,, Selman M . 2013. Latest progress in microsporidian genome research. J Eukaryot Microbiol 60 : 309 312.[CrossRef] [PubMed]
96. Corradi N,, Slamovits CH . 2011. The intriguing nature of microsporidian genomes. Brief Funct Genomics 10 : 115 124.[CrossRef] [PubMed]
97. Brugère JF,, Cornillot E,, Méténier G,, Bensimon A,, Vivarès CP . 2000. Encephalitozoon cuniculi (Microspora) genome: physical map and evidence for telomere-associated rDNA units on all chromosomes. Nucleic Acids Res 28 : 2026 2033.[CrossRef]
98. Brugère JF,, Cornillot E,, Méténier G,, Vivarès CP . 2000. Occurence of subtelomeric rearrangements in the genome of the microsporidian parasite Encephalitozoon cuniculi, as revealed by a new fingerprinting procedure based on two-dimensional pulsed field gel electrophoresis. Electrophoresis 21 : 2576 2581.[CrossRef]
99. Selman M,, Sak B,, Kváč M,, Farinelli L,, Weiss LM,, Corradi N . 2013. Extremely reduced levels of heterozygosity in the vertebrate pathogen Encephalitozoon cuniculi . Eukaryot Cell 12 : 496 502.[CrossRef] [PubMed]
100. Cuomo CA,, Desjardins CA,, Bakowski MA,, Goldberg J,, Ma AT,, Becnel JJ,, Didier ES,, Fan L,, Heiman DI,, Levin JZ,, Young S,, Zeng Q,, Troemel ER . 2012. Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Res 22 : 2478 2488.[CrossRef]
101. Pelin A,, Selman M,, Aris-Brosou S,, Farinelli L,, Corradi N . 2015. Genome analyses suggest the presence of polyploidy and recent human-driven expansions in eight global populations of the honeybee pathogen Nosema ceranae . Environ Microbiol 17 : 4443 4458.[CrossRef] [PubMed]
102. Aurrecoechea C,, Barreto A,, Brestelli J,, Brunk BP,, Caler EV,, Fischer S,, Gajria B,, Gao X,, Gingle A,, Grant G,, Harb OS,, Heiges M,, Iodice J,, Kissinger JC,, Kraemer ET,, Li W,, Nayak V,, Pennington C,, Pinney DF,, Pitts B,, Roos DS,, Srinivasamoorthy G,, Stoeckert CJ Jr,, Treatman C,, Wang H . 2011. AmoebaDB and MicrosporidiaDB: functional genomic resources for Amoebozoa and Microsporidia species. Nucleic Acids Res 39( Database) : D612 D619.[CrossRef]
103. Vossbrinck CR,, Debrunner-Vossbrinck BA . 2005. Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitol (Praha) 52 : 131 142, discussion 130.[CrossRef]
104. Pieniazek NJ,, da Silva AJ,, Slemenda SB,, Visvesvara GS,, Kurtti TJ,, Yasunaga C . 1996. Nosema trichoplusiae is a synonym of Nosema bombycis based on the sequence of the small subunit ribosomal RNA coding region. J Invertebr Pathol 67 : 316 317.[CrossRef]
105. Zhu X,, Wittner M,, Tanowitz HB,, Cali A,, Weiss LM . 1994. Ribosomal RNA sequences of Enterocytozoon bieneusi, Septata intestinalis and Ameson michaelis: phylogenetic construction and structural correspondence. J Eukaryot Microbiol 41 : 204 209.[CrossRef]
106. Shafer AB,, Williams GR,, Shutler D,, Rogers RE,, Stewart DT . 2009. Cophylogeny of Nosema (Microsporidia: Nosematidae) and bees (Hymenoptera: Apidae) suggests both cospeciation and a host-switch. J Parasitol 95 : 198 203.[CrossRef]
107. Zhu F,, Shen Z,, Xu X,, Tao H,, Dong S,, Tang X,, Xu L . 2010. Phylogenetic analysis of complete rRNA gene sequence of Nosema philosamiae isolated from the lepidopteran Philosamia cynthia ricini . J Eukaryot Microbiol 57 : 294 296.[PubMed]
108. Baker MD,, Vossbrinck CR,, Becnel JJ,, Andreadis TG . 1998. Phylogeny of amblyospora (Microsporida: amblyosporidae) and related genera based on small subunit ribosomal DNA data: a possible example of host parasite cospeciation. J Invertebr Pathol 71 : 199 206.[CrossRef] [PubMed]
109. Andreadis TG,, Simakova AV,, Vossbrinck CR,, Shepard JJ,, Yurchenko YA . 2012. Ultrastructural characterization and comparative phylogenetic analysis of new microsporidia from Siberian mosquitoes: evidence for coevolution and host switching. J Invertebr Pathol 109 : 59 75.[CrossRef]
110. Bell AS,, Aoki T,, Yokoyama H . 2001. Phylogenetic relationships among microsporidia based on rDNA sequence data, with particular reference to fish-infecting Microsporidium balbiani 1884 species. J Eukaryot Microbiol 48 : 258 265.[PubMed] [CrossRef]
111. Lom J . 2002. A catalogue of described genera and species of microsporidians parasitic in fish. Syst Parasitol 53 : 81 99.[CrossRef] [PubMed]
112. Müller A,, Trammer T,, Chioralia G,, Seitz HM,, Diehl V,, Franzen C . 2000. Ribosomal RNA of Nosema algerae and phylogenetic relationship to other microsporidia. Parasitol Res 86 : 18 23.[CrossRef] [PubMed]
113. Chen Y,, Evans JD,, Zhou L,, Boncristiani H,, Kimura K,, Xiao T,, Litkowski AM,, Pettis JS . 2009. Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. J Invertebr Pathol 101 : 204 209.[CrossRef] [PubMed]
114. Becnel J . 1994. Life cycles and host-parasite relationships of Microsporidia in culicine mosquitoes. Folia Parasitol (Praha) 41 : 91 96.[PubMed]
115. Refardt D,, Canning EU,, Mathis A,, Cheney SA,, Lafranchi-Tristem NJ,, Ebert D . 2002. Small subunit ribosomal DNA phylogeny of microsporidia that infect Daphnia (Crustacea: cladocera). Parasitology 124 : 381 389.[CrossRef]
116. Ebert D . 2008. Host-parasite coevolution: insights from the Daphnia-parasite model system. Curr Opin Microbiol 11 : 290 301.[CrossRef] [PubMed]
117. Keeling PJ,, Luker MA,, Palmer JD . 2000. Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. Mol Biol Evol 17 : 23 31.[PubMed] [CrossRef]
118. Edlind T,, Katiyar S,, Visvesvara G,, Li J . 1996. Evolutionary origins of Microsporidia and basis for benzimidazole sensitivity: an update. J Eukaryot Microbiol 43 : 109S.[PubMed] [CrossRef]
119. Hirt RP,, Healy B,, Vossbrinck CR,, Canning EU,, Embley TM . 1997. A mitochondrial Hsp70 orthologue in Vairimorpha necatrix: molecular evidence that microsporidia once contained mitochondria. Curr Biol 7 : 995 998.[CrossRef]
120. Hirt RP,, Logsdon JM Jr,, Healy B,, Dorey MW,, Doolittle WF,, Embley TM . 1999. Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc Natl Acad Sci USA 96 : 580 585.[CrossRef] [PubMed]
121. Keeling PJ,, Doolittle WF . 1996. Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. Mol Biol Evol 13 : 1297 1305.[CrossRef] [PubMed]
122. Arisue N,, Sánchez LB,, Weiss LM,, Müller M,, Hashimoto T . 2002. Mitochondrial-type hsp70 genes of the amitochondriate protists, Giardia intestinalis, Entamoeba histolytica and two microsporidians. Parasitol Int 51 : 9 16.[CrossRef]
123. Germot A,, Philippe H . 1999. Critical analysis of eukaryotic phylogeny: a case study based on the HSP70 family. J Eukaryot Microbiol 46 : 116 124.[CrossRef]
124. Germot A,, Philippe H,, Le Guyader H . 1997. Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae . Mol Biochem Parasitol 87 : 159 168.[CrossRef]
125. Peyretaillade E,, Broussolle V,, Peyret P,, Méténier G,, Gouy M,, Vivarès CP . 1998. Microsporidia, amitochondrial protists, possess a 70-kDa heat shock protein gene of mitochondrial evolutionary origin. Mol Biol Evol 15 : 683 689.[CrossRef]
126. Fast NM,, Logsdon JM Jr,, Doolittle WF . 1999. Phylogenetic analysis of the TATA box binding protein (TBP) gene from Nosema locustae: evidence for a microsporidia-fungi relationship and spliceosomal intron loss. Mol Biol Evol 16 : 1415 1419.[CrossRef]
127. Vivares C,, Biderre C,, Duffieux F,, Peyretaillade E,, Peyret P,, Metenier G,, Pages M . 1996. Chromosomal localization of five genes in Encephalitozoon cuniculi (Microsporidia). J Eukaryot Microbiol 43 : 97S.[CrossRef]
128. Edlind T, . 1998. Phylogenetics of protozoan tubulin with reference to the amitochondriate eukaryotes, p 91 108. In Coombs GH,, Vickerman K,, Sleigh MA,, Warren A (ed), Evolutionary Relationships Among Protozoa. Chapman & Hall, London, United Kingdom.
129. Lee SC,, Weiss LM,, Heitman J . 2009. Generation of genetic diversity in microsporidia via sexual reproduction and horizontal gene transfer. Commun Integr Biol 2 : 414 417.[CrossRef] [PubMed]
130. Lee SC,, Corradi N,, Doan S,, Dietrich FS,, Keeling PJ,, Heitman J . 2010. Evolution of the sex-related locus and genomic features shared in microsporidia and fungi. PLoS One 5 : e10539.[CrossRef] [PubMed]
131. Weiss LM,, Vossbrinck CR, . 1999. Molecular biology, molecular phylogeny, and molecular diagnostic approaches to the microsporidia, p 129 171. In Wittner M,, Weiss LM (ed), The Microsporidia and Microsporidia. ASM Press, Washington, DC.[CrossRef]
132. Kamaishi T,, Hashimoto T,, Nakamura Y,, Nakamura F,, Murata S,, Okada N,, Okamoto K,, Shimizu M,, Hasegawa M . 1996. Protein phylogeny of translation elongation factor EF-1 alpha suggests microsporidians are extremely ancient eukaryotes. J Mol Evol 42 : 257 263.[CrossRef]
133. Keeling PJ,, Corradi N . 2011. Shrink it or lose it: balancing loss of function with shrinking genomes in the microsporidia. Virulence 2 : 67 70.[CrossRef] [PubMed]
134. Desportes I . 1976. Ultrastructure de Stempellia mutabilis Leger et Hesse, microsporidie parasite de l’ephemere Ephemera vulgata L. Protistologica (Paris) 12 : 121 150.
135. Flegel TW,, Pasharawipas T . 1995. A proposal for typical eukaryotic meiosis in microsporidians. Can J Microbiol 41 : 1 11.[CrossRef]
136. Xu Y,, Takvorian PM,, Cali A,, Orr G,, Weiss LM . 2004. Glycosylation of the major polar tube protein of Encephalitozoon hellem, a microsporidian parasite that infects humans. Infect Immun 72 : 6341 6350.[CrossRef] [PubMed]
137. Keeling PJ . 2003. Congruent evidence from alpha-tubulin and beta-tubulin gene phylogenies for a zygomycete origin of microsporidia. Fungal Genet Biol 38 : 298 309.[CrossRef]
138. James TY,, Pelin A,, Bonen L,, Ahrendt S,, Sain D,, Corradi N,, Stajich JE . 2013. Shared signatures of parasitism and phylogenomics unite Cryptomycota and microsporidia. Curr Biol 23 : 1548 1553.[CrossRef] [PubMed]
139. Jones MD,, Forn I,, Gadelha C,, Egan MJ,, Bass D,, Massana R,, Richards TA . 2011. Discovery of novel intermediate forms redefines the fungal tree of life. Nature 474 : 200 203.[CrossRef] [PubMed]
140. Jones MD,, Richards TA,, Hawksworth DL,, Bass D . 2011. Validation and justification of the phylum name Cryptomycota phyl. nov. IMA Fungus 2 : 173 175.[CrossRef] [PubMed]
141. Evans TN,, Seviour RJ . 2012. Estimating biodiversity of fungi in activated sludge communities using culture-independent methods. Microb Ecol 63 : 773 786.[CrossRef]
142. Livermore JA,, Mattes TE . 2013. Phylogenetic detection of novel Cryptomycota in an Iowa (United States) aquifer and from previously collected marine and freshwater targeted high-throughput sequencing sets. Environ Microbiol 15 : 2333 2341.[CrossRef]
143. Manohar CS,, Raghukumar C . 2013. Fungal diversity from various marine habitats deduced through culture-independent studies. FEMS Microbiol Lett 341 : 69 78.[CrossRef]
144. Haag KL,, James TY,, Pombert JF,, Larsson R,, Schaer TM,, Refardt D,, Ebert D . 2014. Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites. Proc Natl Acad Sci USA 111 : 15480 15485. [Erratum, 112:E1162, doi:10.1073/pnas.1502848112.][CrossRef]
145. Corsaro D,, Walochnik J,, Venditti D,, Müller KD,, Hauröder B,, Michel R . 2014. Rediscovery of Nucleophaga amoebae, a novel member of the Rozellomycota. Parasitol Res 113 : 4491 4498.[CrossRef] [PubMed]
146. Corsaro D,, Walochnik J,, Venditti D,, Steinmann J,, Müller KD,, Michel R . 2014. Microsporidia-like parasites of amoebae belong to the early fungal lineage Rozellomycota. Parasitol Res 113 : 1909 1918.[CrossRef]
147. Vávra J,, Ronny Larsson J, . 2014. Structure of microsporidia, p 1 70. In Weiss LM,, Becnel J (ed), Microsporidia: Pathogens of Opportunity. Wiley Blackwell, Oxford, United Kingdom.
148. Vavra JCJ . 1982. Fluorescence staining of microsporidian spores with the brightener “Calcofluor White M2k”. J Protozool 29 : 503.
149. Brosson D,, Kuhn L,, Prensier G,, Vivarès CP,, Texier C . 2005. The putative chitin deacetylase of Encephalitozoon cuniculi: a surface protein implicated in microsporidian spore-wall formation. FEMS Microbiol Lett 247 : 81 90.[CrossRef]
150. Han B,, Zhou K,, Li Z,, Sun B,, Ni Q,, Meng X,, Pan G,, Li C,, Long M,, Li T,, Zhou C,, Li W,, Zhou Z . 2016. Characterization of the first fungal glycosyl hydrolase family 19 chitinase (NbchiA) from Nosema bombycis (Nb). J Eukaryot Microbiol 63 : 37 45.[CrossRef]
151. Southern TR,, Jolly CE,, Lester ME,, Hayman JR . 2007. EnP1, a microsporidian spore wall protein that enables spores to adhere to and infect host cells in vitro . Eukaryot Cell 6 : 1354 1362.[CrossRef] [PubMed]
152. Undeen AH,, Frixione E . 1990. The role of osmotic pressure in the germination of Nosema algerae spores. J Protozool 37 : 561 567.[CrossRef]
153. Bohne W,, Ferguson DJ,, Kohler K,, Gross U . 2000. Developmental expression of a tandemly repeated, glycine- and serine-rich spore wall protein in the microsporidian pathogen Encephalitozoon cuniculi . Infect Immun 68 : 2268 2275.[CrossRef]
154. Hayman JR,, Hayes SF,, Amon J,, Nash TE . 2001. Developmental expression of two spore wall proteins during maturation of the microsporidian Encephalitozoon intestinalis . Infect Immun 69 : 7057 7066.[CrossRef]
155. Polonais V,, Mazet M,, Wawrzyniak I,, Texier C,, Blot N,, El Alaoui H,, Delbac F . 2010. The human microsporidian Encephalitozoon hellem synthesizes two spore wall polymorphic proteins useful for epidemiological studies. Infect Immun 78 : 2221 2230.[CrossRef]
156. Peuvel-Fanget I,, Polonais V,, Brosson D,, Texier C,, Kuhn L,, Peyret P,, Vivarès C,, Delbac F . 2006. EnP1 and EnP2, two proteins associated with the Encephalitozoon cuniculi endospore, the chitin-rich inner layer of the microsporidian spore wall. Int J Parasitol 36 : 309 318.[CrossRef] [PubMed]
157. Xu Y,, Takvorian P,, Cali A,, Wang F,, Zhang H,, Orr G,, Weiss LM . 2006. Identification of a new spore wall protein from Encephalitozoon cuniculi . Infect Immun 74 : 239 247.[CrossRef] [PubMed]
158. Hayman JR,, Southern TR,, Nash TE . 2005. Role of sulfated glycans in adherence of the microsporidian Encephalitozoon intestinalis to host cells in vitro . Infect Immun 73 : 841 848.[CrossRef]
159. Ghosh K,, Nieves E,, Keeling P,, Pombert J-F,, Henrich PP,, Cali A,, Weiss LM . 2011. Branching network of proteinaceous filaments within the parasitophorous vacuole of Encephalitozoon cuniculi and Encephalitozoon hellem. Infect Immun 79 : 1374 1385.[CrossRef]
160. Wu Z,, Li Y,, Pan G,, Zhou Z,, Xiang Z . 2009. SWP25, a novel protein associated with the Nosema bombycis endospore. J Eukaryot Microbiol 56 : 113 118.[PubMed] [CrossRef]
161. Wang JY,, Chambon C,, Lu CD,, Huang KW,, Vivarès CP,, Texier C . 2007. A proteomic-based approach for the characterization of some major structural proteins involved in host-parasite relationships from the silkworm parasite Nosema bombycis (Microsporidia). Proteomics 7 : 1461 1472.[CrossRef]
162. Yang D,, Pan G,, Dang X,, Shi Y,, Li C,, Peng P,, Luo B,, Bian M,, Song Y,, Ma C,, Chen J,, Ma Z,, Geng L,, Li Z,, Tian R,, Wei C,, Zhou Z . 2015. Interaction and assembly of two novel proteins in the spore wall of the microsporidian species Nosema bombycis and their roles in adherence to and infection of host cells. Infect Immun 83 : 1715 1731.[CrossRef] [PubMed]
163. Chen J,, Geng L,, Long M,, Li T,, Li Z,, Yang D,, Ma C,, Wu H,, Ma Z,, Li C,, Pan G,, Zhou Z . 2013. Identification of a novel chitin-binding spore wall protein (NbSWP12) with a BAR-2 domain from Nosema bombycis (microsporidia). Parasitology 140 : 1394 1402.[CrossRef] [PubMed]
164. Li Z,, Pan G,, Li T,, Huang W,, Chen J,, Geng L,, Yang D,, Wang L,, Zhou Z . 2012. SWP5, a spore wall protein, interacts with polar tube proteins in the parasitic microsporidian Nosema bombycis . Eukaryot Cell 11 : 229 237.[CrossRef]
165. Thelohan P . 1894. Sur la presence d’une capsule a filament dans les spores des microsporidies. CR Acad Sci 118 : 1425 1427.
166. Thelohan P . 1892. Observations sur les Myxosporidies et essai de classification de ces organismes. Bull Soc Philomath Paris 4 : 173 174.
167. Sanders JL,, Watral V,, Kent ML . 2012. Microsporidiosis in zebrafish research facilities. ILAR J 53 : 106 113.[CrossRef] [PubMed]
168. Lom J,, Vavra J . 1963. The mode of sporoplasm extrusion in microsporidian spores. Acta Protozool 1 : 81 89.
169. Weidner E . 1976. The microsporidian spore invasion tube. The ultrastructure, isolation, and characterization of the protein comprising the tube. J Cell Biol 71 : 23 34.[CrossRef] [PubMed]
170. Ohshima K . 1937. On the function of the polar filament of Nosema bombycis . Parasitology 29 : 220 224.[CrossRef]
171. Weidner E . 1982. The microsporidian spore invasion tube. III. Tube extrusion and assembly. J Cell Biol 93 : 976 979.[CrossRef] [PubMed]
172. Undeen AH,, Epsky ND . 1990. In vitro and in vivo germination of Nosema locustae (Microspora: Nosematidae) spores. J Invertebr Pathol 56 : 371 379.[CrossRef]
173. Keohane EM,, Orr GA,, Takvorian PM,, Cali A,, Tanowitz HB,, Wittner M,, Weiss LM . 1996. Purification and characterization of a microsporidian polar tube protein. Mol Biochem Parasitol 79 : 255 259.[CrossRef] [PubMed]
174. Keohane EM,, Orr GA,, Takvorian PM,, Cali A,, Tanowitz HB,, Wittner M,, Weiss LM . 1996. Purification and characterization of human microsporidian polar tube proteins. J Eukaryot Microbiol 43 : 100S.[PubMed] [CrossRef]
175. Keohane EM,, Orr GA,, Takvorian PM,, Cali A,, Tanowitz HB,, Wittner M,, Weiss LM . 1999. Polar tube proteins of microsporidia of the family encephalitozoonidae. J Eukaryot Microbiol 46 : 1 5.[CrossRef] [PubMed]
176. Keohane EM,, Orr GA,, Takvorian PM,, Cali A,, Tanowitz HB,, Wittner M,, Weiss LM . 1999. Analysis of the major microsporidian polar tube proteins. J Eukaryot Microbiol 46 : 29S 30S.[CrossRef] [PubMed]
177. Keohane EM,, Orr GA,, Zhang HS,, Takvorian PM,, Cali A,, Tanowitz HB,, Wittner M,, Weiss LM . 1998. The molecular characterization of the major polar tube protein gene from Encephalitozoon hellem, a microsporidian parasite of humans. Mol Biochem Parasitol 94 : 227 236.[CrossRef]
178. Keohane EM,, Takvorian PM,, Cali A,, Tanowitz HB,, Wittner M,, Weiss LM . 1996. Identification of a microsporidian polar tube protein reactive monoclonal antibody. J Eukaryot Microbiol 43 : 26 31.[CrossRef] [PubMed]
179. Keohane EM,, Takvorian PM,, Cali A,, Tanowitz HB,, Wittner M,, Weiss LM . 2001. Monoclonal antibodies to cytoplasmic antigens of Nosema locustae (Microsporida: nosematidae). J Invertebr Pathol 77 : 81 82.[CrossRef]
180. Delbac F,, Peuvel I,, Metenier G,, Peyretaillade E,, Vivares CP . 2001. Microsporidian invasion apparatus: identification of a novel polar tube protein and evidence for clustering of ptp1 and ptp2 genes in three Encephalitozoon species. Infect Immun 69 : 1016 1024.[CrossRef] [PubMed]
181. Peuvel I,, Delbac F,, Metenier G,, Peyret P,, Vivares CP . 2000. Polymorphism of the gene encoding a major polar tube protein PTP1 in two microsporidia of the genus Encephalitozoon . Parasitology 121 : 581 587.[CrossRef] [PubMed]
182. Peuvel I,, Peyret P,, Méténier G,, Vivarès CP,, Delbac F . 2002. The microsporidian polar tube: evidence for a third polar tube protein (PTP3) in Encephalitozoon cuniculi . Mol Biochem Parasitol 122 : 69 80.[CrossRef] [PubMed]
183. Xu Y,, Takvorian P,, Cali A,, Weiss LM . 2003. Lectin binding of the major polar tube protein (PTP1) and its role in invasion. J Eukaryot Microbiol 50( Suppl) : 600 601.[PubMed] [CrossRef]
184. Polonais V,, Prensier G,, Méténier G,, Vivarès CP,, Delbac F . 2005. Microsporidian polar tube proteins: highly divergent but closely linked genes encode PTP1 and PTP2 in members of the evolutionarily distant Antonospora and Encephalitozoon groups. Fungal Genet Biol 42 : 791 803.[CrossRef]
185. Bouzahzah B,, Nagajyothi F,, Ghosh K,, Takvorian PM,, Cali A,, Tanowitz HB,, Weiss LM . 2010. Interactions of Encephalitozoon cuniculi polar tube proteins. Infect Immun 78 : 2745 2753.[CrossRef] [PubMed]
186. Bouzahzah B,, Weiss LM . 2010. Glycosylation of the major polar tube protein of Encephalitozoon cuniculi . Parasitol Res 107 : 761 764.[CrossRef] [PubMed]
187. Hatjina F,, Tsoktouridis G,, Bouga M,, Charistos L,, Evangelou V,, Avtzis D,, Meeus I,, Brunain M,, Smagghe G,, de Graaf DC . 2011. Polar tube protein gene diversity among Nosema ceranae strains derived from a Greek honey bee health study. J Invertebr Pathol 108 : 131 134.[CrossRef] [PubMed]
188. Delbac F,, David D,, Méténter G,, Vivarès C . 1997. First complete amino acid sequence of a polar tube protein in a microsporidian species, Encephalitozoon cuniculi . J Eukaryot Microbiol 44( s6) : 77s.[CrossRef]
189. van Gool T,, Vetter JC,, Weinmayr B,, Van Dam A,, Derouin F,, Dankert J . 1997. High seroprevalence of Encephalitozoon species in immunocompetent subjects. J Infect Dis 175 : 1020 1024.[CrossRef] [PubMed]
190. Keohane EM,, Weiss LM . 1998. Characterization and function of the microsporidian polar tube: a review. Folia Parasitol (Praha) 45 : 117 127.[PubMed]
191. Peek R,, Delbac F,, Speijer D,, Polonais V,, Greve S,, Wentink-Bonnema E,, Ringrose J,, van Gool T . 2005. Carbohydrate moieties of microsporidian polar tube proteins are targeted by immunoglobulin G in immunocompetent individuals. Infect Immun 73 : 7906 7913.[CrossRef] [PubMed]
192. Dolgikh VV,, Semenov PB . 2003. The spore wall and polar tube proteins of the microsporidian Nosema grylli: the major spore wall protein is released before spore extrusion. Tsitologiia 45 : 324 329.[PubMed]
193. Peyretaillade E,, Parisot N,, Polonais V,, Terrat S,, Denonfoux J,, Dugat-Bony E,, Wawrzyniak I,, Biderre-Petit C,, Mahul A,, Rimour S,, Gonçalves O,, Bornes S,, Delbac F,, Chebance B,, Duprat S,, Samson G,, Katinka M,, Weissenbach J,, Wincker P,, Peyret P . 2012. Annotation of microsporidian genomes using transcriptional signals. Nat Commun 3 : 1137.[CrossRef] [PubMed]
194. Cornman RS,, Chen YP,, Schatz MC,, Street C,, Zhao Y,, Desany B,, Egholm M,, Hutchison S,, Pettis JS,, Lipkin WI,, Evans JD . 2009. Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS Pathog 5 : e1000466.[CrossRef] [PubMed]
195. Pan G,, Xu J,, Li T,, Xia Q,, Liu SL,, Zhang G,, Li S,, Li C,, Liu H,, Yang L,, Liu T,, Zhang X,, Wu Z,, Fan W,, Dang X,, Xiang H,, Tao M,, Li Y,, Hu J,, Li Z,, Lin L,, Luo J,, Geng L,, Wang L,, Long M,, Wan Y,, He N,, Zhang Z,, Lu C,, Keeling PJ,, Wang J,, Xiang Z,, Zhou Z . 2013. Comparative genomics of parasitic silkworm microsporidia reveal an association between genome expansion and host adaptation. BMC Genomics 14 : 186.[CrossRef]
196. Polonais V,, Belkorchia A,, Roussel M,, Peyretaillade E,, Peyret P,, Diogon M,, Delbac F . 2013. Identification of two new polar tube proteins related to polar tube protein 2 in the microsporidian Antonospora locustae . FEMS Microbiol Lett 346 : 36 44.[CrossRef] [PubMed]
197. Slamovits CH,, Fast NM,, Law JS,, Keeling PJ . 2004. Genome compaction and stability in microsporidian intracellular parasites. Curr Biol 14 : 891 896.[CrossRef] [PubMed]
198. Brosson D,, Kuhn L,, Delbac F,, Garin J,, P Vivarès C,, Texier C . 2006. Proteomic analysis of the eukaryotic parasite Encephalitozoon cuniculi (microsporidia): a reference map for proteins expressed in late sporogonial stages. Proteomics 6 : 3625 3635.[CrossRef]
199. Foucault C,, Drancourt M . 2000. Actin mediates Encephalitozoon intestinalis entry into the human enterocyte-like cell line, Caco-2. Microb Pathog 28 : 51 58.[CrossRef] [PubMed]


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Table 1

Species of microsporidia infecting humans

Citation: Han B, Weiss L. 2017. Microsporidia: Obligate Intracellular Pathogens Within the Fungal Kingdom, p 97-113. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0018-2016

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