Folia Parasitologica 52[1/2] 41-50 (2005) | DOI: 10.14411/fp.2005.006

Review of microsporidia-mosquito relationships: from the simple to the complex

James J. Becnel, Susan E. White, Alexandra M. Shapiro
USDA/ARS Center for Medical, Agricultural and Veterinary Entomology, P.O. Box 14565, Gainesville, Florida 32604, USA

Microsporidia in mosquitoes can be divided into two categories based on their life cycles and host-parasite relationships. Some species of microsporidia exhibit simple life cycles with one spore type responsible for oral (horizontal) transmission. They affect only one generation of the mosquito and are not usually host or tissue specific. Brachiola algerae (Vavra et Undeen, 1970) and Vavraia culicis (Weiser, 1947) are examples of species isolated from mosquitoes with relatively straightforward life cycles (one spore type) and simple host-parasite relationships. B. algerae and a close relative of V. culicis have also been isolated from a vertebrate (human) host but sources for these infections are unknown. In contrast to B. algerae and V. culicis, polymorphic (heterosporous) microsporidia in mosquitoes are characterized by complex life cycles involving multiple spore types responsible for horizontal and vertical transmission. They affect two generations of the mosquito and some involve an obligate intermediate host. These microsporidia are generally very host and tissue specific with complex developmental sequences comprised of unique stages and events. The microsporidium Edhazardia aedis (Kudo, 1930) is a pathogen of Aedes aegypti and does not require an intermediate host. The developmental cycle of E. aedis is characterized by four sporulation sequences, two in the parental host and two in the filial generation. Recent speculation relative to the source of B. algerae human infection have implicated infected mosquitoes and raised concerns about the safety of mosquito microsporidia in general. The subject of this review is to compare and contrast three species of microsporidia from mosquitoes, two with broad host ranges (B. algerae and V. culicis) and one specific to mosquitoes (E. aedis). This review describes features that distinguish mosquito-parasitic microsporidia with simple life cycles and broad host ranges from truly mosquito-specific microsporidian parasites with complex life cycles.

Keywords: Microsporidia, mosquito, Brachiola algerae, Vavraia culicis, Edhazardia aedis

Received: September 14, 2004; Accepted: December 17, 2004; Published: May 1, 2005  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Becnel, J.J., White, S.E., & Shapiro, A.M. (2005). Review of microsporidia-mosquito relationships: from the simple to the complex. Folia Parasitologica52(1-2), 41-50. doi: 10.14411/fp.2005.006
Download citation

References

  1. ALGER N.E., MADDOX J.V., SHADDUCK J.A. 1980: Nosema algerae: infectivity and immune response in normal and nude mice. WHO/VBC/80.778.7
  2. ANDREADIS T.G. 1985: Experimental transmission of a microsporidian pathogen from mosquitoes to an alternate copepod host. Proc. Natl. Acad. Sci. U.S.A. 82: 5574- 5577 Go to original source... Go to PubMed...
  3. ANDREADIS T.G. 1988: Amblyospora connecticus sp. nov. (Microsporida: Amblyosporidae): horizontal transmission studies in the mosquito Aedes cantator and formal description. J. Invertebr. Pathol. 52: 90-101 Go to original source...
  4. ANDREADIS T.G. 1994: Host range tests with Edhazardia aedis (Microsporida: Culicosporidae) against northern Nearctic mosquitoes. J. Invertebr. Pathol. 64: 46-51 Go to original source... Go to PubMed...
  5. ANDREADIS T.G. 1999: Epizootiology of Amblyospora stimuli (Microsporida: Amblyosporidae) infections in field populations of a univoltine mosquito, Aedes stimulans (Diptera: Culicidae), inhabiting a temporary vernal pool. J. Invertebr. Pathol. 74: 198-205 Go to original source... Go to PubMed...
  6. ANDREADIS T.G. 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 Go to original source... Go to PubMed...
  7. ANDREADIS T.G., VOSSBRINCK C.R. 2002: Life cycle, ultrastructure and molecular phylogeny of Hyalinocysta chapmani (Microsporidia: Thelohaniidae), a parasite of Culiseta melanura (Diptera: Culicidae) and Orthocyclops modestus (Copepoda: Cyclopidae). J. Eukaryot. Microbiol. 49: 350-364 Go to original source... Go to PubMed...
  8. AVERY S.W., ANTHONY D.W. 1983: Ultrastructural study of early development of Nosema algerae in Anopheles albimanus. J. Invertebr. Pathol. 42: 87-95 Go to original source... Go to PubMed...
  9. AVERY S.W., UNDEEN A.H. 1990: Horizontal transmission of Parathelohania anophelis to the copepod, Microcyclops varicans, and the mosquito, Anopheles quadrimaculatus. J. Invertebr. Pathol. 56: 98-105 Go to original source... Go to PubMed...
  10. BAKER M.D., VOSSBRINCK C.R., BECNEL J.J., ANDREADIS T.G. 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 Go to original source... Go to PubMed...
  11. BECNEL J.J. 1992a: Horizontal transmission and subsequent development of Amblyospora californica (Microsporida: Amblyosporidae) in the intermediate and definitive hosts. Dis. Aquat. Org. 13: 17-28 Go to original source...
  12. BECNEL J.J. 1992b: Safety of Edhazardia aedis (Microspora: Amblyosporidae) for nontarget aquatic organisms. J. Am. Mosq. Control Assoc. 8: 256-260
  13. BECNEL J.J. 1994: Life cycles and host-parasite relationships of microsporidia in culicine mosquitoes. Folia Parasitol. 41: 91-96 Go to PubMed...
  14. BECNEL J.J., ANDREADIS T.G. 1998: Amblyospora salinaria n. sp. (Microsporidia: Amblyosporidae), parasite of Culex salinarius (Diptera: Culicidae): its life cycle stages in an intermediate host. J. Invertebr. Pathol. 71: 258-262 Go to original source... Go to PubMed...
  15. BECNEL J.J., ANDREADIS T.G. 1999: Microsporidia in insects. In M. Wittner (Ed.), The Microsporidia and Microsporidiosis. ASM Press, Washington, DC, pp. 447- 501 Go to original source...
  16. BECNEL J.J., GARCIA J.J., JOHNSON M.A. 1995: Edhazardia aedis (Microspora: Culicosporidae) effects on the reproductive capacity of Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 32: 549-553 Go to original source... Go to PubMed...
  17. BECNEL J.J., HAZARD E.I., FUKUDA T., SPRAGUE V. 1987: Life cycle of Culicospora magna (Kudo, 1920) (Microsporida: Culicosporidae) in Culex restuans Theobald with special reference to sexuality. J. Protozool. 34: 313-322 Go to original source...
  18. BECNEL J.J., JOHNSON M.A. 1993: Mosquito host range and specificity of Edhazardia aedis (Microspora: Culicosporidae). J. Am. Mosq. Control Assoc. 9: 269-274
  19. BECNEL J.J., SPRAGUE V., FUKUDA T., HAZARD E.I. 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 Go to original source... Go to PubMed...
  20. BROOKS W.M. 1988: Entomogenous Protozoa. In C.M. Ignoffo and N.B. Mandava (Eds.), CRC Handbook of Natural Pesticides, Vol. 5, Microbial Insecticides, Part A, Entomogenous Protozoa and Fungi. CRC Press, Boca Raton, pp. 1-149 Go to original source...
  21. BROOKS W.M., HAZARD E.I., BECNEL J.J. 1985: Two new species of Nosema (Microsporida: Nosematidae) from the Mexican bean beetle Epilachna varivestis (Coleoptera: Coccinellidae). J. Protozool. 32: 525-535 Go to original source... Go to PubMed...
  22. CANNING E.U. 1957: Plistophora culicis Weiser (Protozoa, Microsporidia): its development in Anopheles gambiae. Trans. R. Soc. Trop. Med. Hyg. 51: 8
  23. CHENEY S.A., LAFRANCHI-TRISTEM N.J., CANNING E.U. 2000: Phylogenetic relationships of Pleistophora-like microsporidia based on small subunit ribosomal DNA sequences and implications for the source of Trachipleistophora hominis infections. J. Eukaryot. Microbiol. 47: 280-287 Go to original source... Go to PubMed...
  24. COYLE C.M., WEISS L.M., RHODES L.V. 3rd, CALI A., TAKVORIAN P.M., BROWN D.F., VISVESVARA G.S., 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 Go to original source... Go to PubMed...
  25. FUKUDA T., WILLIS O.R., BARNARD D.R. 1997: Parasites of the Asian tiger mosquito and other container-inhabiting mosquitoes (Diptera: Culicidae) in northcentral Florida. J. Med. Entomol. 34: 226-233 Go to original source... Go to PubMed...
  26. HAZARD E.I., OLDACRE S.W. 1975: Revision of Microsporidia (Protozoa) close to Thelohania, with descriptions of one new family, eight new genera and thirteen new species. U. S. Dept. Agric. Tech. Bull. No. 1530, 104 pp
  27. HAZARD E.I., 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 Go to original source... Go to PubMed...
  28. HEMBREE S.C. 1982: Dose-response studies of a new species of per os and vertically transmittable microsporid-ian pathogen of Aedes aegypti from Thailand. Mosq. News 42: 55-61
  29. HEMBREE S.C., RYAN J.R. 1982: Observations on the vertical transmission of a new microsporidian pathogen of Aedes aegypti from Thailand. Mosq. News 42: 49-54
  30. HESSE E. 1904: Thelohania legeri n. sp., microsporidie nouvelle, parasite des larves d'Anopheles maculipennis Meig. C. R. Soc. Biol. 57: 570-571
  31. JOHNSON M.A., BECNEL J.J., UNDEEN A.H. 1997: A new sporulation sequence in Edhazardia aedis (Microsporidia: Culicosporidae), a parasite of the mosquito Aedes aegypti (Diptera: Culicidae). J. Invertebr. Pathol. 70: 69-75 Go to original source...
  32. KELLEN W.R., CHAPMAN H.C., CLARK T.B., LINDEGREN J.E. 1966a: Transovarian transmission of some Thelohania (Nosematidae: Microsporidia) in mosquitoes of California and Louisiana. J. Invertebr. Pathol. 8: 355- 359 Go to original source...
  33. KELLEN W.R., CLARK T.B., LINDEGREN J.E. 1967: Two previously undescribed Nosema from mosquitoes of California (Nosematidae: Microsporidia). J. Invertebr. Pathol. 9: 19-25 Go to original source...
  34. KELLEN W.R., CLARK T.B., LINDEGREN J.E., SANDERS R.D. 1966b: Development of Thelohania californica in two hybrid mosquitoes. Exp. Parasitol. 18: 251-254 Go to original source...
  35. KELLEN W.R., LIPA J. 1960: Thelohania californica n. sp., a microsporidian parasite of Culex tarsalis Coquillett. J. Insect Pathol. 2: 1-12
  36. KELLEN W.R., WILLS W. 1962a: New Thelohania from Californian mosquitoes (Nosematidae: Microsporidia). J. Insect Pathol. 4: 41-56
  37. KELLEN W.R., WILLS W. 1962b: The transovarian transmission of Thelohania californica Kellen and Lipa in Culex tarsalis Coquillett. J. Insect Pathol. 4: 321-326
  38. KOELLA J.C., AGNEW P. 1997: Blood-feeding success of the mosquito Aedes aegypti depends on the transmission route of its parasite Edhazardia aedis. Oikos 78: 311-316 Go to original source...
  39. KOUDELA B., VISVESVARA G.S., MOURA H., VAVRA J. 2001: The human isolate of Brachiola algerae (Phylum Microspora): development in SCID mice and description of its fine structure features. Parasitology 123: 153-162 Go to original source... Go to PubMed...
  40. KUCEROVA Z., MOURA H., VISVESVARA G.S., LEITCH G.J. 2004: Differences between Brachiola (Nosema) algerae isolates of human and insect origin when tested using an in vitro spore germination assay and a cultured cell infection assay. J. Eukaryot. Microbiol. 51: 339-343 Go to original source... Go to PubMed...
  41. KUDO R. 1920: Cnidosporidia in the vicinity of Urbana. Trans. Ill. State. Acad. Sci. 13: 298-303
  42. KUDO R. 1921: Studies on microsporidia with special reference to those parasitic in mosquitoes. J. Morphol. 35: 153-193 Go to original source...
  43. KUDO R. 1922: Studies on microsporidia parasitic in mosquitoes. II. On the effect of the parasites upon the host body. J. Parasitol. 8: 70-77 Go to original source...
  44. KUDO R. 1924a: Studies on microsporidia parasitic in mosquitoes. III. On Thelohania legeri Hesse (=Th. illinoisensis Kudo). Arch. Protistenkd. 49: 147-162
  45. KUDO R. 1924b: Studies on microsporidia parasitic in mosquitoes. VI. On the development of Thelohania opacita, a culicine parasite. J. Parasitol. 11: 84-89 Go to original source...
  46. KUDO R. 1925a: Studies on microsporidia parasitic in mosquitoes. IV. Observations upon the microsporidia found in the mosquitoes of Georgia, USA. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. Abt. 1, Orig. 96: 428-440
  47. KUDO R. 1925b: Studies on microsporidia parasitic in mosquitoes. V. Further observations upon Stempellia (Thelohania) magna Kudo, parasitic in Culex pipiens and C. territans. Biol. Bull. 48: 112-127 Go to original source...
  48. KUDO R. 1929: Studies on microsporidia parasitic in mosquitoes. VII. Notes on microsporidia of some Indian mosquitoes. Arch. Protistenkd. 67: 1-10
  49. KUDO R. 1930: Studies on microsporidia parasitic in mosquitoes. VIII. On a microsporidan, Nosema aedis nov. spec., parasitic in a larva of Aedes aegypti of Porto Rico. Arch. Protistenkd. 69: 23-38
  50. LOWMAN P.M., TAKVORIAN P.M., 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. Go to original source... Go to PubMed...
  51. MICIELI M.V., GARCIA J.J., BECNEL J.J. 1998: Horizontal transmission of Amblyospora dolosi (Microsporidia: Amblyosporidae) to the copepod Metacyclops mendocinus (Wierzejski, 1892). J. Invertebr. Pathol. 72 : 330-335 Go to original source... Go to PubMed...
  52. MICIELI M.V., GARCIA J.J., BECNEL J.J. 2000a: Horizontal transmission of Amblyospora albifasciati Garcia and Becnel, 1994 (Microsporidia: Amblyosporidae), to a copepod intermediate host and the neotropical mosquito, Aedes albifasciatus (Macquart, 1837). J. Invertebr. Pathol. 75: 76-83 Go to original source... Go to PubMed...
  53. MICIELI M.V., GARCIA J.J., BECNEL J.J. 2000b: Life cycle and description of Amblyospora camposi n. sp (Microspo-ridia: Amblyosporidae) in the mosquito Culex renatoi (Diptera, Culicidae) and the copepod Paracyclops fimbriatus fimbriatus (Copepoda, Cyclopidae). J. Eukaryot. Microbiol. 47: 575-580 Go to original source... Go to PubMed...
  54. SMITH J.E., BARKER R.J., LAIP.F. 1982: Culture of microsporidia from invertebrates in vertebrate cells. Parasitology 85: 427-435 Go to original source...
  55. SWEENEY A.W., BECNEL J.J. 1991: Potential of microsporidia for the biological control of mosquitoes. Parasitol. Today 7: 217-220 Go to original source... Go to PubMed...
  56. SWEENEY A.W., DOGGETT S.L., PIPER R.G. 1990: Life cycle of Amblyospora indicola (Microspora: Amblyosporidae), a parasite of the mosquito Culex sitiens and of Apocyclops sp. copepods. J. Invertebr. Pathol. 55: 428- 434 Go to original source... Go to PubMed...
  57. SWEENEY A.W., DOGGETT S.L., PIPER R.G. 1993: Life cycle of a new species of Duboscqia (Microsporida: Thelohaniidae) infecting the mosquito Anopheles hilli and an intermediate copepod host, Apocyclops dengizicus. J. Invertebr. Pathol. 62: 137-146 Go to original source... Go to PubMed...
  58. SWEENEY A.W., GRAHAM M.F., HAZARD E.I. 1988: Life cycle of Amblyospora dyxenoides sp. nov. in the mosquito Culex annulirostris and the copepod Mesocyclops albicans. J. Invertebr. Pathol. 51: 46-57 Go to original source... Go to PubMed...
  59. SWEENEY A.W., HAZARD E.I., GRAHAM M.F. 1985: Intermediate host for an Amblyospora sp. (Microspora) infecting the mosquito, Culex annulirostris. J. Invertebr. Pathol. 46: 98-102 Go to original source... Go to PubMed...
  60. TRAMMER T., CHIORALIA G., MAIER W.A., SEITZ H.M. 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 Go to original source... Go to PubMed...
  61. TRAMMER T., DOMBROWSKI F., DOEHRING M., MAIER W.A., SEITZ H.M. 1997: Opportunistic properties of Nosema algerae (Microspora), a mosquito parasite, in immunocompromised mice. J. Eukaryot. Microbiol. 44: 258-262 Go to original source... Go to PubMed...
  62. UNDEEN A.H. 1975: Growth of Nosema algerae in pig kidney cell cultures. J. Protozool. 22: 107-110 Go to original source... Go to PubMed...
  63. UNDEEN A.H., ALGER N.E. 1976: Nosema algerae: infection of the white mouse by a mosquito parasite. Exp. Parasitol. 40: 86-88 Go to original source... Go to PubMed...
  64. UNDEEN A.H., MADDOX J.V. 1973: The infection of nonmosquito hosts by injection with spores of the microsporidian Nosema algerae. J. Invertebr. Pathol. 22: 258- 265 Go to original source... Go to PubMed...
  65. VAVRA J., UNDEEN A.H. 1970: Nosema algerae n. sp. (Cnidospora, Microsporida) a pathogen in a laboratory colony of Anopheles stephensi Liston (Diptera: Culicidae). J. Protozool. 17: 240-249 Go to original source... Go to PubMed...
  66. VISVESVARA G.S., BELLOSO M., MOURA H., DA SILVA A.J., MOURA I.N., LEITCH G.J., SCHWARTZ D.A., CHEVEZ-BARRIOS P., WALLACE S., PIENIAZEK N.J., GOOSEY J.D. 1999: Isolation of Nosema algerae from the cornea of an immunocompetent patient. J. Eukaryot. Microbiol. 46: 10S Go to PubMed...
  67. VOSSBRINCK C.R., ANDREADIS T.G., DEBRUNNERVOSSBRINCK B.A. 1998: Verification of intermediate hosts in the life cycles of microsporidia by small subunit rDNA sequencing. J. Eukaryot. Microbiol. 45: 290-292 Go to original source... Go to PubMed...
  68. VOSSBRINCK C.R., ANDREADIS T.G., VAVRA J., BECNEL J.J. 2004a: Molecular phylogeny and evolution of mosquito parasitic microsporidia (Microsporidia: Amblyosporidae). J. Eukaryot. Microbiol. 51: 88-95 Go to original source... Go to PubMed...
  69. VOSSBRINCK C.R., ANDREADIS T.G., VAVRA J., BECNEL J.J. 2004b: Molecular phylogeny and evolution of mosquito parasitic microsporidia (Microsporidia: Amblyosporidae) (errata). J. Eukaryot. Microbiol. 51: 259- 261 Go to original source... Go to PubMed...
  70. WANG B. 1982: The pathobiology of the mosquito parasite, Vavraia culicis (Weiser). Ph.D. Thesis, University of California, Los Angeles, 151 pp
  71. WEIDNER E., CANNING E.U., RUTLEDGE C.R., MEEK C.L. 1999: Mosquito (Diptera: Culicidae) host compatibility and vector competency for the human myositic parasite Trachipleistophora hominis (Phylum Microspora). J. Med. Entomol. 36: 522-525 Go to original source... Go to PubMed...
  72. WEISER J. 1947: Klic k urcovani Mikrosporidii. Acta Soc. Sci. Nat. Moravicae 18: 1-64
  73. WEISER J. 1978: Production of the microsporidian Plistophora culicis Weiser in substitute host. Folia Parasitol. 25: 365
  74. WEISER J., COLUZZI M. 1972: The microsporidian Plistophora culicis Weiser, 1946 in different mosquito hosts. Folia Parasitol. 19: 197-202 Go to PubMed...
  75. WEISER J., ZIZKA Z. 2004: Brachiola gambiae sp. n. the microsporidian parasite of Anopheles gambiae and A melas in Liberia. Acta Protozool. 43: 73-80
  76. WHITE S.E., FUKUDA T., UNDEEN A.H. 1994: Horizontal transmission of Amblyospora opacita (Microspora: Amblyosporidae) between the mosquito, Culex territans, and the copepod, Paracyclops fimbriatus chiltoni. J. Invertebr. Pathol. 63: 19-25 Go to original source...