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5 Microsporidia

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Systematics and Evolution

Part of the book series: The Mycota ((MYCOTA,volume 7A))

Abstract

The phylum Microsporidia comprises an interesting group of intracellular fungal parasites that infect vertebrate and invertebrate hosts of commercial and medical significance. Microsporidia are unique for their mode of infection, whereby the spore contents are propelled through an inverting polar filament and injected into the host cell. Believed to branch among the earliest eukaryotes, microsporidia are now considered more highly evolved for exhibiting gene reduction and compaction, which also are signs of extreme parasite efficiency. This chapter highlights the unusual mechanism of infection and current classification of the microsporidia and describes the morphology, life cycle, and culture of microsporidia species of importance to arthropod, aquatic, and mammalian hosts.

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References

  • Akiyoshi DE, Morrison HG, Lei S, Feng X, Zhang Q, Corradi N, Mayanja H, Tumwine JK, Keeling PJ, Weiss LM, Tzipori S (2009) Genomic survey of the non-cultivatable opportunistic human pathogen, Enterocytozoon bieneusi. PLoS Pathog 5:e1000261

    PubMed Central  PubMed  Google Scholar 

  • Andreadis TG (1984) Epizootiology of Nosema pyrausta in field populations of the European corn borer. Environ Entomol 13:882–887

    Google Scholar 

  • Andreadis TG (1988) Comparative susceptibility of the copepod Acanthocyclops vernalis to a microsporidian parasite, Amblyospora connecticus, from the mosquito Aedes cantator. J Invertebr Pathol 52:73–77

    Google Scholar 

  • Andreadis TG (2002) Epizootiology of Hyalinocysta chapmani (Microsporidia: Thelohaniidae) infections in field populations of Culiseta melanura (Diptera: Culicidae) and Orthocyclops modestus (Copepoda: Cyclopidae): a three-year investigation. J Invertebr Pathol 81:114–121

    PubMed  Google Scholar 

  • Avery SW, Undeen AH (1990) Horizontal transmission of Parathelohania anophelis to the copepod, Microcyclops varicans, and the mosquito, Anopheles quadrimaculatus. J Invertebr Pathol 56:98–105

    CAS  PubMed  Google Scholar 

  • Baxa-Antonio D, Groff JM, Hedrick RP (1992) Experimental horizontal transmission of Enterocytozoon salmonis to chinook salmon, Oncorhynchus tshawytscha. J Protozool 39:699–702

    CAS  PubMed  Google Scholar 

  • Beckers PJ, Derks GJ, van Gool T, Rietveld FJ, Sauerwein RW (1996) Encephalocytozoon intestinalis-specific monoclonal antibodies for laboratory diagnosis of microsporidiosis. J Clin Microbiol 34:282–285

    CAS  PubMed Central  PubMed  Google Scholar 

  • Becnel JJ (1992) Horizontal transmission and subsequent development of Amblyospora californica (Microsporida: Amblyosporiae) in the intermediate and definitive hosts. Dis Aquat Org 13:17–28

    Google Scholar 

  • Becnel JJ, Andreadis TG (1999) Microsporidia in insects. In: Wittner M, Weiss LM (eds) The microsporidia and microsporidiosis. American Society for Microbiology Press, Washington, DC, pp 447–501

    Google Scholar 

  • Becnel JJ, Hazard EI, Fukuda T, Sprague V (1987) Life cycle of Culicospora magna (Kudo, 1920) (Microsporida: Culicosporidae) in Culex restuans Theobald with special reference to sexuality. J Eukaryot Microbiol 34:313–322

    Google Scholar 

  • Becnel JJ, Sprague V, Fukuda T, Hazard EI (1989) Development of Edhazardia aedis (Kudo, 1930) n. g., n. comb. (Microsporida: Amblyosporidae) in the mosquito Aedes aegypti (L.) (Diptera: Culicidae). J Protozool 36:119–130

    CAS  PubMed  Google Scholar 

  • Becnel JJ, Jeyaprakash A, Hoy MA, Shapiro A (2002) Morphological and molecular characterization of a new microsporidian species from the predatory mite Metaseiulus occidentalis (Nesbitt) (Acari, Phytoseiidae). J Invertebr Pathol 79:163–172

    CAS  PubMed  Google Scholar 

  • Becnel JJ, White SE, Shapiro AM (2005) Review of microsporidia-mosquito relationships: from the simple to the complex. Folia Parasitol (Praha) 52:41–50

    Google Scholar 

  • Bigliardi E, Selmi MG, Lupetti P, Corona S, Gatti S, Scaglia M, Sacchi L (1996) Microsporidian spore wall: ultrastructural findings on Encephalitozoon hellem exospore. J Eukaryot Microbiol 43:181–186

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Braunfuchsová P, Kopecký J, Ditrich O, Koudela B (1999) Cytokine response to infection with the microsporidian, Encephalitozoon cuniculi. Folia Parasitol (Praha) 46:91–95

    Google Scholar 

  • Brooks WM (1988) Entomogenous Protozoa. In: Ignoffo CM (ed) Handbook of natural pesticides, Vol. V, microbial insecticides Part A, entomogenous protozoa and fungi. CRC, Boca Raton, FL, pp 1–149

    Google Scholar 

  • Burri L, Williams BA, Bursac D, Lithgow T, Keeling PJ (2006) Microsporidian mitosomes retain elements of the general mitochondrial targeting system. Proc Natl Acad Sci USA 103:15916–15920

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cali A, Owen RL (1988) Microsporidiosis. In: Balows WJ, Hausler WJ, Ohashi M, Turano A (eds) Laboratory diagnosis of infectious diseases: principles and practice. Springer, New York, pp 929–946

    Google Scholar 

  • Cali A, Owen RL (1990) Intracellular development of Enterocytozoon, a unique microsporidian found in the intestine of AIDS patients. J Protozool 37:145–155

    CAS  PubMed  Google Scholar 

  • Cali A, Takvorian P (1999) Developmental morphology and life cycles of the microsporidia. In: Wittner M, Weiss LM (eds) The microsporidia and microsporidiosis. American Society for Microbiology, Washington, DC, pp 85–128

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Cali A, Weiss LM, Takvorian PM (2002) Brachiola algerae spore membrane systems, their activity during extrusion, and a new structural entity, the multilayered interlaced network, associated with the polar tube and the sporoplasm. J Eukaryot Microbiol 49:164–174

    PubMed  Google Scholar 

  • Canning EU, Lom J, Dyková I (1986) The microsporidia of vertebrates. Academic, London

    Google Scholar 

  • Chen Y, Evans JD, Smith IB, Pettis JS (2008) Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. J Invertebr Pathol 97:186–188

    PubMed  Google Scholar 

  • Chilmonczyk S, Cox WT, Hedrick RP (1991) Enterocytozoon salmonis n. sp.: an intranuclear microsporidium from salmonid fish. J Protozool 38:264–269

    CAS  PubMed  Google Scholar 

  • Chioralia G, Trammer T, Maier WA, Seitz HM (1998) Morphologic changes in Nosema algerae (Microspora) during extrusion. Parasitol Res 84:123–131

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • Corradi N, Keeling PJ (2009) Microsporidia: a journey through radical taxonomical revisions. Fungal Biol Rev 23:1–8

    Google Scholar 

  • Corradi N, Slamovits CH (2011) The intriguing nature of microsporidian genomes. Brief Funct Genomics 10:115–124

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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. doi:10.1038/ncomms1082

    PubMed  Google Scholar 

  • de Graaf DC, Raes H, Jacobs FJ (1994) Spore dimorphism in Nosema apis (Microsporida, Nosematidae) developmental cycle. J Invertebr Pathol 63:92–94

    Google Scholar 

  • de Kinkelin P (1980) Occurrence of a microsporidian infection in zebra danio Brachydanio rerio (Hamilton-Buchanan). J Fish Dis 3:71–73

    Google Scholar 

  • Delbac F, Duffieux F, David D, Méténier G, Vivarès CP (1998a) Immunocytochemical identification of spore proteins in two microsporidia, with emphasis on extrusion apparatus. J Eukaryot Microbiol 45:224–231

    CAS  PubMed  Google Scholar 

  • Delbac F, Peyret P, Méténier G, David D, Danchin A, Vivarès CP (1998b) On proteins of the microsporidian invasive apparatus: complete sequence of a polar tube protein of Encephalitozoon cuniculi. Mol Microbiol 29:825–834

    CAS  PubMed  Google Scholar 

  • Delbac F, Peuvel I, Méténier G, Peyretaillade E, Vivarès 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Didier ES, Weiss LM (2006) Microsporidiosis: current status. Curr Opin Infect Dis 19:485–492. doi:10.1097/01.qco.0000244055.46382.23

    PubMed Central  PubMed  Google Scholar 

  • Didier ES, Didier PJ, Friedberg DN, Stenson SM, Orenstein JM, Yee RW, Tio FO, Davis RM, Vossbrinck C, Millichamp N et al (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

    CAS  PubMed  Google Scholar 

  • Didier ES, Rogers LB, Orenstein JM, Baker MD, Vossbrinck CR, Van Gool T, Hartskeerl R, Soave R, Beaudet LM (1996) Characterization of Encephalitozoon (Septata) intestinalis isolates cultured from nasal mucosa and bronchoalveolar lavage fluids of two AIDS patients. J Eukaryot Microbiol 43:34–43

    CAS  PubMed  Google Scholar 

  • Didier ES, Snowden KF, Shadduck JA (1998) Biology of microsporidian species infecting mammals. Adv Parasitol 40:283–320

    CAS  PubMed  Google Scholar 

  • Dyer PS (2008) Evolutionary biology: microsporidia sex–a missing link to fungi. Curr Biol 18:R1012–R1014

    CAS  PubMed  Google Scholar 

  • Erickson BW Jr, Blanquet RS (1969) The occurrence of chitin in the spore wall of Glugea weissenbergi. J Invertebr Pathol 14:358–364

    CAS  PubMed  Google Scholar 

  • Fast NM, Keeling PJ (2001) Alpha and beta subunits of pyruvate dehydrogenase E1 from the microsporidian Nosema locustae: mitochondrion-derived carbon metabolism in microsporidia. Mol Biochem Parasitol 117:201–209

    CAS  PubMed  Google Scholar 

  • Fries I (1993) Nosema apis—a parasite in the honey bee colony. Bee World 74:5–19

    Google Scholar 

  • Frixione E, Ruiz L, Santillán M, de Vargas LV, Tejero JM, Undeen AH (1992) Dynamics of polar filament discharge and sporoplasm expulsion by microsporidian spores. Cell Motil Cytoskeleton 22:38–50

    Google Scholar 

  • Frixione E, Ruiz L, Cerbon 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

    CAS  PubMed  Google Scholar 

  • Geden CJ, Long SJ, Rutz DA, Becnel JJ (1995) Nosema disease of the parasitoid Muscidifurax raptor (Hymenoptera: Pteromalidae): prevalence, patterns of transmission, management, and impact. Biol Control 5:607–614

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ghosh K, Nieves E, Keeling P, Pombert JF, 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Graczyk TK, Majewska AC, Schwab KJ (2008) The role of birds in dissemination of human waterborne enteropathogens. Trends Parasitol 24:55–59

    PubMed  Google Scholar 

  • Haro M, Izquierdo F, Henriques-Gil N, Andrés I, Alonso F, Fenoy S, del Aguila C (2005) First detection and genotyping of human-associated microsporidia in pigeons from urban parks. Appl Environ Microbiol 71:3153–3157

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hazard EI, Weiser J (1968) Spores of Thelohania in adult female anopheles: development and transovarial transmission, and redescriptions of T. legeri Hesse and T. obesa Kudo. J Protozool 15:817–823

    CAS  PubMed  Google Scholar 

  • Henry JE, Oma EA (1981) Pest control by Nosema locustae, a pathogen of grasshoppers and crickets. In: Burges HD (ed) Microbial control of pests and plant diseases. Academic, London, pp 573–586

    Google Scholar 

  • Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lucking R, Thorsten Lumbsch H, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai YC, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Koljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo JM, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schussler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao YJ, Zhang N (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O'Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schussler A, Longcore JE, O'Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lucking R, Budel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818–822

    CAS  PubMed  Google Scholar 

  • Jaronski ST (1984) Microsporidia in cell culture. Adv Cell Culture 18:183–229

    Google Scholar 

  • Juarez SI, Putaporntip C, Jongwutiwes S, Ichinose A, Yanagi T, Kanbara H (2005) In vitro cultivation and electron microscopy characterization of Trachipleistophora anthropophthera isolated from the cornea of an AIDS patient. J Eukaryot Microbiol 52:179–190

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Keeling P (2009) Five questions about microsporidia. PLoS Pathog 5:e1000489

    PubMed Central  PubMed  Google Scholar 

  • Keeling PJ, Corradi N, Morrison HG, Haag KL, Ebert D, Weiss LM, Akiyoshi DE, Tzipori S (2010) The reduced genome of the parasitic microsporidian Enterocytozoon bieneusi lacks genes for core carbon metabolism. Genome Biol Evol 2:304–309

    PubMed Central  PubMed  Google Scholar 

  • Kellen WR, Lipa JJ (1960) Thelohania californica n.sp., a microsporidian parasite of Culex tarsalis Coquillet. J Invertebr Pathol 2:1–12

    Google Scholar 

  • Kent ML, Bishop-Stewart JK (2003) Transmission and tissue distribution of Pseudoloma neurophilia (Microsporidia) of zebrafish, Danio rerio (Hamilton). J Fish Dis 26:423–426

    CAS  PubMed  Google Scholar 

  • Kent ML, Poppe TT (1998) Diseases of seawater netpen-reared salmonid fishes. Pacific Biological Station, Department of Fisheries and Oceans, Nanimo, BC

    Google Scholar 

  • Kent ML, Speare DJ (2005) Review of the sequential development of Loma salmonae (Microsporidia) based on experimental infections of rainbow trout (Oncorhynchus mykiss) and Chinook salmon (O. tshawytscha). Folia Parasitol (Praha) 52:63–68

    Google Scholar 

  • Kent ML, Buchner C, Watral VG, Sander JL, LaDu J, Peterson TS, Tanguay RL (2011) Development and maintenance of a specific pathogen-free (SPF) zebrafish research facility for Pseudoloma neurophilia. Dis Aquat Org 95:73–79

    PubMed Central  PubMed  Google Scholar 

  • Keohane EM, Weiss LM (1998) Characterization and function of the microsporidian polar tube: a review. Folia Parasitol (Praha) 45:117–127

    CAS  Google Scholar 

  • Keohane E, Takvorian PM, Cali A, Tanowitz HB, Wittner M, Weiss LM (1994) The identification and characterization of a polar tube reactive monoclonal antibody. J Eukaryot Microbiol 41:48S

    CAS  PubMed  Google Scholar 

  • Keohane EM, Orr GA, Takvorian PM, Cali A, Tanowitz HB, Wittner M, Weiss LM (1996a) Purification and characterization of a microsporidian polar tube protein. Mol Biochem Parasitol 79:255–2559

    CAS  PubMed  Google Scholar 

  • Keohane EM, Orr GA, Takvorian PM, Cali A, Tanowitz HB, Wittner M, Weiss LM (1996b) Purification and characterization of human microsporidian polar tube proteins. J Eukaryot Microbiol 43:100S

    CAS  PubMed  Google Scholar 

  • Keohane EM, Takvorian PM, Cali A, Tanowitz HB, Wittner M, Weiss LM (1996c) Identification of a microsporidian polar tube protein reactive monoclonal antibody. J Eukaryot Microbiol 43:26–31

    CAS  PubMed  Google Scholar 

  • 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 from Encephalitozoon hellem, a microsporidian parasite of humans. Mol Biochem Parasitol 94:227–2236

    CAS  PubMed Central  PubMed  Google Scholar 

  • Keohane EM, Orr GA, Takvorian PM, Cali A, Tanowitz HB, Wittner M, Weiss LM (1999a) Analysis of the major microsporidian polar tube proteins. J Eukaryot Microbiol 46:29S–30S

    CAS  PubMed  Google Scholar 

  • Keohane EM, Orr GA, Takvorian PM, Cali A, Tanowitz HB, Wittner M, Weiss LM (1999b) Polar tube proteins of microsporidia of the family encephalitozoonidae. J Eukaryot Microbiol 46:1–5

    CAS  PubMed  Google Scholar 

  • Koestler T, Ebersberger I (2011) Zygomycetes, microsporidia, and the evolutionary ancestry of sex determination. Genome Biol Evol 3:186–194

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kotler DP, Orenstein JM (1998) Clinical syndromes associated with microsporidiosis. Adv Parasitol 40:321–349

    CAS  PubMed  Google Scholar 

  • Kou G-H, Wang C-H, Hung H-W, Jang Y-S, Chou C-M, Lo C-F (1995) A cell line (EP-1 cell line) derived from “Beko disease” affected Japanese eel elver (Anguilla japonica) persistently infected with Pleistophora anguillarum. Aquaculture 132:161–173

    Google Scholar 

  • Lafranchi-Tristem NJ, Curry A, Cheney SA, Canning EU (2001) Growth of Trachipleistophora hominis (Microsporidia: Pleistophoridae) in C2, C12 mouse myoblast cells and response to treatment with albendazole. Folia Parasitol (Praha) 48:192–200

    CAS  Google Scholar 

  • Larsson R (1986) Ultrastructure, function, and classification of microsporidia. Prog Protistol 1:325–390

    Google Scholar 

  • Larsson JI (2005) Molecular versus morphological approach to microsporidian classification. Folia Parasitol (Praha) 52:143–144

    Google Scholar 

  • Lee SC, Corradi N, Byrnes EJ 3rd, Torres-Martinez S, Dietrich FS, Keeling PJ, Heitman J (2008) Microsporidia evolved from ancestral sexual fungi. Curr Biol 18:1675–1679

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lee RC, Gill EE, Roy SW, Fast NM (2010a) Constrained intron structures in a microsporidian. Mol Biol Evol 27:1979–1982

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lee SC, Corradi N, Doan S, Dietrich FS, Keeling PJ, Heitman J (2010b) Evolution of the sex-related locus and genomic features shared in microsporidia and fungi. PLoS One 5:e10539

    PubMed Central  PubMed  Google Scholar 

  • Lom J (1972) On the structure of the extruded microsporidian polar filament. Parasitol Res 38:200–213

    Google Scholar 

  • Lom J (2002) A catalogue of described genera and species of microsporidians parasitic in fish. Syst Parasitol 53:81–99

    PubMed  Google Scholar 

  • Lom J, Dyková I (1992) Protozoan parasites of fishes. Elsevier, Amsterdam

    Google Scholar 

  • Lom J, Dyková I (2005) Microsporidian xenomas in fish seen in wider perspective. Folia Parasitol (Praha) 52:69–81

    Google Scholar 

  • Lom J, Nilsen F (2003) Fish microsporidia: fine structural diversity and phylogeny. Int J Parasitol 33:107–127

    PubMed  Google Scholar 

  • Lom J, Vávra J (1963) The mode of sporoplasm extrusion in microsporidian spores. Acta Protozool 1:81–89

    Google Scholar 

  • Lores B, Rosales MJ, Mascaro C, Osuna A (2003) In vitro culture of Glugea sp. Vet Parasitol 112:185–196

    CAS  PubMed  Google Scholar 

  • Lowman PM, Takvorian PM, Cali A (2000) The effects of elevated temperatures and various time-temperature combinations on the development of Brachiola (Nosema) algerae N. Comb in mammalian cell culture. J Eukaryot Microbiol 47:221–234

    CAS  PubMed  Google Scholar 

  • Matos E, Corral L, Azevedo C (2003) Ultrastructural details of the xenoma of Loma myrophis (phylum Microsporidia) and extrusion of the polar tube during autoinfection. Dis Aquat Org 54:203–207

    CAS  PubMed  Google Scholar 

  • Matthews JL, Brown AM, Larison K, Bishop-Stewart JK, Rogers P, Kent ML (2001) Pseudoloma neurophilia n. g., n. sp., a new microsporidium from the central nervous system of the zebrafish (Danio rerio). J Eukaryot Microbiol 48:227–233

    CAS  PubMed  Google Scholar 

  • McVicar AH (1975) Infection of plaice Pleuronectes platessa L. with Glugea (Nosema) stephani (Hagenmüller 1899) (Protozoa: Microsporidia) in a fish farm and under experimental conditions. J Fish Biol 7:611–619

    Google Scholar 

  • Monaghan SR, Kent ML, Watral VG, Kaufman RJ, Lee LE, Bols NC (2009) Animal cell cultures in microsporidial research: their general roles and their specific use for fish microsporidia. In Vitro Cell Dev Biol Anim 45:135–147

    PubMed  Google Scholar 

  • Monaghan SR, Rumney RL, Vo NT, Bols NC, Lee LE (2011) In vitro growth of microsporidia Anncaliia algerae in cell lines from warm water fish. In Vitro Cell Dev Biol Anim 47:104–113

    PubMed  Google Scholar 

  • Morrison CM, Sprague V (1983) Loma salmonae (Putz, Hoffman and Dunbar, 1965) in the rainbow trout, Salmo gairdneri Richardson, and L. fontinalis sp. nov. (Microsporida) in the brook trout, Salvelinus fontinalis (Mitchill). J Fish Dis 6:345–353

    Google Scholar 

  • Muller MG, Kinne J, Schuster RK, Walochnik J (2008) Outbreak of microsporidiosis caused by Enterocytozoon bieneusi in falcons. Vet Parasitol 152:67–78

    CAS  PubMed  Google Scholar 

  • Nylund S, Nylund A, Watanabe K, Arnesen CE, Karlsbakk E (2010) Paranucleospora theridion n. gen., n. sp. (Microsporidia, Enterocytozoonidae) with a life cycle in the salmon louse (Lepeophtheirus salmonis, Copepoda) and Atlantic salmon (Salmo salar). J Eukaryot Microbiol 57:95–114

    PubMed  Google Scholar 

  • Ohshima K (1937) On the function of the polar filament of Nosema bombycis. Parasitology 29:220–224

    Google Scholar 

  • Oi DH, Valles SM, Pereira RM (2004) Prevalence of Thelohania solenopsae (Microsporidia: Thelohaniidae) infection in monogyne and polygyne red imported fire ants (Hymenoptera: Formicidae). Environ Entomol 33:340–345

    Google Scholar 

  • Pasteur L (1870) Etudes sur la Maladie des vers a Soie. Gauthier-Villars, Paris

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Phelps NBD, Goodwin AE (2008) Vertical transmission of Ovipleistophora ovariae (Microspora) within the eggs of the golden shiner. J Aquat Anim Health 20:45–53

    PubMed  Google Scholar 

  • Prigneau O, Achbarou A, Bouladoux N, Mazier D, Desportes-Livage I (2000) Identification of proteins in Encephalitozoon intestinalis, a microsporidian pathogen of immunocompromised humans: an immunoblotting and immunocytochemical study. J Eukaryot Microbiol 47:48–56

    CAS  PubMed  Google Scholar 

  • Ramsay JM, Watral V, Schreck CB, Kent ML (2009) Pseudoloma neurophilia infections in zebrafish Danio rerio: effects of stress on survival, growth, and reproduction. Dis Aquat Org 88:69–84

    PubMed  Google Scholar 

  • Ratnieks FL, Carreck NL (2010) Ecology. Clarity on honey bee collapse? Science 327:152–153

    CAS  PubMed  Google Scholar 

  • Redhead SA, Kirk P, Keeling PJ, Weiss LM (2009) Proposals to exclude the phylum Microsporidia from the code. Taxon 58:10–11

    Google Scholar 

  • Reetz J, Rinder H, Thomschke A, Manke H, Schwebs M, Bruderek A (2002) First detection of the microsporidium Enterocytozoon bieneusi in non-mammalian hosts (chickens). Int J Parasitol 32:785–787

    PubMed  Google Scholar 

  • Rich SM, Ayala FJ (2000) Population structure and recent evolution of Plasmodium falciparum. Proc Natl Acad Sci USA 97:6994–7001

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rodriguez-Tovar LE, Wadowska DW, Wright GM, Groman DB, Speare DJ, Whelan DS (2003) Ultrastructural evidence of autoinfection in the gills of Atlantic cod Gadus morhua infected with Loma sp. (phylum Microsporidia). Dis Aquat Org 57:227–230

    PubMed  Google Scholar 

  • Rönnebäumer K, Gross U, Bohne W (2008) The nascent parasitophorous vacuole membrane of Encephalitozoon cuniculi is formed by host cell lipids and contains pores which allow nutrient uptake. Eukaryot Cell 7:1001–1008

    PubMed Central  PubMed  Google Scholar 

  • Sanchez JG, Speare DJ, Markham RJ, Wright GM, Kibenge FS (2001) Localization of the initial developmental stages of Loma salmonae in rainbow trout (Oncorhynchus mykiss). Vet Pathol 38:540–546

    CAS  PubMed  Google Scholar 

  • Sanders JL, Kent ML (2011) Development of a sensitive assay for the detection of Pseudoloma neurophilia and laboratory populations of the zebrafish, Danio rerio. Dis Aquat Org 96:145–156

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sanders JL, Lawrence C, Nichols DK, Brubaker JF, Peterson TS, Murray KN, Kent ML (2010) Pleistophora hyphessobryconis (Microsporidia) infecting zebrafish Danio rerio in research facilities. Dis Aquat Org 91:47–56

    CAS  PubMed  Google Scholar 

  • Santín M, Fayer R (2009a) Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. J Eukaryot Microbiol 56:34–38

    PubMed  Google Scholar 

  • Santín M, Fayer R (2009b) A longitudinal study of Enterocytozoon bieneusi in dairy cattle. Parasitol Res 105:141–144

    PubMed  Google Scholar 

  • Schäperclaus W (1991) Plistophora disease of neon and other aquarium fish (Pleistophorosis). In: Schäperclaus W, Kulow H, Schreckenbach K (eds) Fish Diseases (vol 2, 5th ed.), Amerind, New Delh, 1,398 pp

    Google Scholar 

  • Shadduck JA (1969) Nosema cuiculi: in vitro isolation. Science 166:516–517

    CAS  PubMed  Google Scholar 

  • Shaw R, Kent ML (1999) Fish microsporidia. In: Wittner M, Weiss LM (eds) The microsporidia and microsporidiosis. American Society for Microbiology Press, Washington, DC, pp 418–444

    Google Scholar 

  • Shaw RW, Kent ML, Adamson ML (1998) Modes of transmission of Loma salmonae (Microsporidia). Dis Aquat Org 33:151–156

    CAS  PubMed  Google Scholar 

  • Shaw RW, Kent ML, Brown AM, Whipps CM, Adamson ML (2000) Experimental and natural host specificity of Loma salmonae (Microsporidia). Dis Aquat Org 40:131–136

    CAS  PubMed  Google Scholar 

  • Siegel JP, Maddox JV, Ruesink WG (1986) Lethal and sublethal effects of Nosema pyrausta on the European corn borer (Ostrinia nubilalis) in central Illinois. J Invertebr Pathol 48:167–173

    Google Scholar 

  • Sinden RE, Canning EU (1974) The ultrastructure of the spore of Nosema algerae (Protozoa, Microsporida), in relation to the hatching mechanism of microsporidian spores. J Gen Microbiol 85:350–357

    Google Scholar 

  • Snowden K, Logan K (1999) Molecular identification of Encephalitozoon hellem in an ostrich. Avian Dis 43:779–782

    CAS  PubMed  Google Scholar 

  • Snowden KF, Logan K, Phalen DN (2000) Isolation and characterization of an avian isolate of Encephalitozoon hellem. Parasitology 121(Pt 1):9–14

    PubMed  Google Scholar 

  • Sokolova YY, Fuxa JR (2008) Biology and life-cycle of the microsporidium Kneallhazia solenopsae Knell Allan Hazard 1977 gen. n., comb. n., from the fire ant Solenopsis invicta. Parasitology 135:903–929

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sprague V (1977) Systematics of the Microsporidia. In: Bulla LA Jr, Cheng TC (eds) Comparative pathobiology. Plenum, New York

    Google Scholar 

  • Sprague V, Becnel JJ (1999) Appendix: checklist of available generic names for microsporidia with type species and type hosts. In: Wittner M, Weiss LM (eds) The microsporidia and microsporidiosis. American Society for Microbiology Press, Washington, DC, pp 531–539

    Google Scholar 

  • Sprague V, Hussey KL (1980) Observations on Ichthyosporidium giganteum (Microsporida) with particular reference to the host-parasite relations during merogony. J Protozool 27:169–175

    CAS  PubMed  Google Scholar 

  • Sprague V, Becnel JJ, Hazard EI (1992) Taxonomy of phylum microspora. Crit Rev Microbiol 18:285–395

    CAS  PubMed  Google Scholar 

  • Steffens W (1962) The current status of distribution of Plistophora hyphessobryconis Schaperclaus 1941 (Sporozoa, Microsporidia). Z Parasitenkd 21:535–541

    CAS  PubMed  Google Scholar 

  • Sweeney AW, Hazard EI, Graham MF (1985) Intermediate host for an Amblyospora sp. (microspora) infecting the mosquito, Culex annulirostris. J Invertebr Pathol 46:98–102

    CAS  PubMed  Google Scholar 

  • Takvorian PM, Cali A (1986) The ultrastructure of spores (Protozoa: Microsporida) from Lophius americanus, the angler fish. J Protozool 33:570–575

    CAS  PubMed  Google Scholar 

  • Texier C, Vidau C, Vigues B, El Alaoui H, Delbac F (2010) Microsporidia: a model for minimal parasite-host interactions. Curr Opin Microbiol 13:443–449

    PubMed  Google Scholar 

  • Trammer T, Chioralia G, Maier WA, Seitz HM (1999) In vitro replication of Nosema algerae (Microsporidia), a parasite of anopheline mosquitoes, in human cells above 36 degrees C. J Eukaryot Microbiol 46:464–468

    CAS  PubMed  Google Scholar 

  • Troemel ER (2011) New models of microsporidiosis: infections in zebrafish, C. elegans, and honey bees. PLoS Pathog 7:e1001243

    CAS  PubMed Central  PubMed  Google Scholar 

  • Undeen AH (1975) Growth of Nosema algerae in pig kidney cell cultures. J Protozool 22:107–110

    CAS  PubMed  Google Scholar 

  • Undeen AH (1990) A proposed mechanism for the germination of microsporidian (Protozoa: Microspora) spores. J Theor Biol 142:223–235

    Google Scholar 

  • Undeen AH, Avery SW (1988) Ammonium chloride inhibition of the germination of spores of Nosema algerae (Microspora: Nosematidae). J Invertebr Pathol 52:326–334

    CAS  Google Scholar 

  • Undeen AH, Epsky ND (1990) In vitro and in vivo germination of Nosema locustae (Microspora: Nosematidae) spores. J Invertebr Pathol 56:371–379

    Google Scholar 

  • Undeen AH, Frixione E (1990) The role of osmotic pressure in the germination of Nosema algerae spores. J Protozool 37:561–567

    CAS  PubMed  Google Scholar 

  • Undeen AH, Frixione E (1991) Structural alteration of the plasma membrane in spores of the microsporidium Nosema algerae on germination. J Protozool 38:511–518

    CAS  PubMed  Google Scholar 

  • Vavrá J (1976) Structure of the microsporidia. In: Bulla LA Jr, Cheng TC (eds) Comparative pathology. Plenum, New York, pp 1–85

    Google Scholar 

  • Vavrá J, Becnel JJ (2007) Vavraia culicis (Weiser, 1947) Weiser, 1977 revisited: cytological characterisation of a Vavraia culicis-like microsporidium isolated from mosquitoes in Florida and the establishment of Vavraia culicis floridensis subsp. n. Folia Parasitol (Praha) 54:259–271

    Google Scholar 

  • Vavrá J, Larsson JIR (1999) Structure of the microsporidia. In: Wittner M, Weiss LM (eds) The microsporidia and microsporidiosis. American Society for Microbiology Press, Washington, DC, pp 7–84

    Google Scholar 

  • Visvesvara GS (2002) In vitro cultivation of microsporidia of clinical importance. Clin Microbiol Rev 15:401–413

    PubMed Central  PubMed  Google Scholar 

  • Vossbrinck CR, Debrunner-Vossbrinck BA (2005) Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitol (Praha) 52:131–142, discussion p130

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Vossbrinck CR, Andreadis TG, Weiss LM (2004) Phylogenetics: taxonomy and the microsporidia as derived fungi. In: Lindsay DS, Weiss LM (eds) Opportunistic infections: toxoplasma, sarcocystis and microsporidia. Springer, New York, pp 189–213

    Google Scholar 

  • Walters VA (1958) Structure, hatching and size variation of the spores in a species of Nosema (Microsporidia) found in Hyalophora cecropia (Lepidoptera). Parasitology 48:113–120

    CAS  PubMed  Google Scholar 

  • Watral VG, Kauffmann RB, Kent ML (2006) In vitro culture of Pseudoloma neurophilia, a common microsporidian of zebrafish (Danio rerio). In: IX International workshops on opportunistic protists and the international society of protistologists 57th annual meeting, Lisbon, Portugal

    Google Scholar 

  • Weber R, Deplazes P, Schwartz D (2000) Diagnosis and clinical aspects of human microsporidiosis. Contrib Microbiol 6:166–192

    CAS  PubMed  Google Scholar 

  • Weidner E (1972) Ultrastructural study of microsporidian invasion into cells. Z Parasitenkd 40:227–242

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Weidner E (1982) The microsporidian spore invasion tube. III. Tube extrusion and assembly. J Cell Biol 93:976–979

    CAS  PubMed  Google Scholar 

  • Weidner E, Byrd W (1982) The microsporidian spore invasion tube. II. Role of calcium in the activation of invasion tube discharge. J Cell Biol 93:970–975

    CAS  PubMed  Google Scholar 

  • Weidner E, Manale SB, Halonen SK, Lynn JW (1995) Protein-membrane interaction is essential to normal assembly of the microsporidian spore invasion tube. Biol Bull 188:128–135

    Google Scholar 

  • Weiser J (1977) Contribution to the classification of Microsporidia. Vestnik Ceskoslovenske Spolecnosti Zoologicke 41:308–320

    Google Scholar 

  • Weiss LM (2001) Microsporidia: emerging pathogenic protists. Acta Trop 78:89–102

    CAS  PubMed  Google Scholar 

  • Weissenberg R (1968) Intracellular development of the Microsporidan Glugea anomala Moniez in hypertrophying migratory cells of the fish Gasterosteus aculeatus L., an example of the formation of “xenoma” tumors. J Eukaryot Microbiol 15:44–57

    Google Scholar 

  • Wiklund T, Lounasheimo L, Lom J, Bylund G (1996) Gonadal impairment in roach Rutilus rutilus from Finnish coastal areas of the northern Baltic Sea. Dis Aquat Org 26:163–171

    Google Scholar 

  • Williams BA, Keeling PJ (2005) Microsporidian mitochondrial proteins: expression in Antonospora locustae spores and identification of genes coding for two further proteins. J Eukaryot Microbiol 52:271–276

    CAS  PubMed  Google Scholar 

  • Williams BA, Hirt RP, Lucocq JM, Embley TM (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865–869

    CAS  PubMed  Google Scholar 

  • Williams BA, Lee RC, Becnel JJ, Weiss LM, Fast NM, Keeling PJ (2008) Genome sequence surveys of Brachiola algerae and Edhazardia aedis reveal microsporidia with low gene densities. BMC Genomics 9:200

    PubMed Central  PubMed  Google Scholar 

  • Wilson GG (1973) Incidence of microsporidia in a field population of spruce budworm. Can For Serv Bi-Mon Res Notes 29:35

    Google Scholar 

  • Wilson GG (1981) Nosema fumiferanae, a natural pathogen of forest pests: potential for pest management. In: Burges HD (ed) Microbial control of pests and plant diseases. Academic, London, pp 595–602

    Google Scholar 

  • Wittner M, Weiss LM (1999) The microsporidia and microsporidiosis. American Society for Microbiology Press, Washington, DC

    Google Scholar 

  • Wongtavatchai J, Conrad PA, Hedrick RP (1994) In vitro cultivation of the microsporidian: Enterocytozoon salmonis using a newly developed medium for salmonid lymphocytes. J Tissue Cult Methods 16:125

    Google Scholar 

  • Wright JH, Craighead EM (1922) Infectious motor paralysis in young rabbits. J Exp Med 36:135–140

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgements

The authors gratefully acknowledge funding from the US National Institutes of Health (AI37188 to LMW, RR017386 to JLS and MLK, and OD011104 and AI071778 subcontract to ESD) that supported research results reported in this chapter. We also recognize the excellent technical assistance of Neil Sanscrainte (to JJB) and Lisa Bowers (to ESD).

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Authors and Affiliations

  1. Division of Microbiology, Tulane National Primate Research Center, 18703 Three Rivers Road, Covington, LA, 70433, USA

    Elizabeth S. Didier

  2. USDA, ARS, CMAVE, 1600 S.W. 23rd Drive, Gainesville, FL, 32608, USA

    James J. Becnel

  3. Department of Microbiology, Oregon State University, 220 Nash Hall, Corvallis, OR, 97331, USA

    Michael L. Kent & Justin L. Sanders

  4. Department of Biomedical Sciences, Oregon State University, Corvallis, OR, 97331, USA

    Michael L. Kent

  5. Departments of Medicine and Pathology, Albert Einstein College of Medicine, 1300 Morris Park Avenue, Room 504 Forchheimer, Bronx, NY, 10461, USA

    Louis M. Weiss

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Correspondence to Elizabeth S. Didier .

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  1. Dept. Plant Biology, University of Minesota, St. Paul, Minnesota, USA

    David J. McLaughlin

  2. Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, USA

    Joseph W. Spatafora

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Didier, E.S., Becnel, J.J., Kent, M.L., Sanders, J.L., Weiss, L.M. (2014). 5 Microsporidia. In: McLaughlin, D., Spatafora, J. (eds) Systematics and Evolution. The Mycota, vol 7A. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-55318-9_5

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