Parasitology Research

, Volume 108, Issue 6, pp 1565–1573

Opportunistic nature of the mammalian microsporidia: experimental transmission of Trachipleistophora extenrec (Fungi: Microsporidia) between mammalian and insect hosts

  • Jiří Vávra
  • Martin Kamler
  • David Modrý
  • Břetislav Koudela
Original Paper

Abstract

Spores of Trachipleistophora extenrec, originally isolated from the muscles of the Madagascan insectivore Hemicentetes semispinosus and maintained by serial passage in severe combined immunodeficiency (SCID) mice, were fed to larvae of the Egyptian cotton leafworm Spodoptera littoralis. Extensive infection of larval tissues ensued and caused larval and pupal mortality. The development of T. extenrec in the insect host, studied both by light and electron microscopy, followed generally the same life cycle as in the mammalian host. However, some differences in the fine structure of the parasite grown in both types of hosts were found. Spores isolated from the insect host caused infection of SCID mice when injected intramuscularly. Our results suggest that T. extenrec may be originally an insect microsporidian. This likelihood is corroborated by its structural similarity and phylogenetic relationship to two other microsporidia having insects either as unique hosts (Vavraia culicis) or being able to infect both mammalian and insect host (Trachipleistophora hominis).

References

  1. Cali A, Neafie R, Weiss LM, Ghosh K, Vergara RB, Gupta R, Takvorian PM (2010) Human vocal cord infection with the microsporidium Anncaliia algerae. J Eukaryot Microbiol 57:562–567PubMedCrossRefGoogle Scholar
  2. Canning EU, Hulls RH (1970) A microsporidian infection of Anopheles gambiae Giles, from Tanzania, interpretation of its mode of transmission and notes on Nosema infections in mosquitoes. J Protozool 17:531–539PubMedGoogle Scholar
  3. Cheney SA, Lafranchi-Tristem NJ, Canning EU (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 47:280–287PubMedCrossRefGoogle Scholar
  4. Cheney SA, Lafranchi-Tristem NJ, Bourges D, Canning EU (2001) Relationships of microsporidian genera, with emphasis on the polysporous genera, revealed by sequences of the largest subunit of RNA polymerase II (RPB 1). J Eukaryot Microbiol 48:111–117PubMedCrossRefGoogle Scholar
  5. Coyle CM, Weiss LM, Rhodes LV, 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. New Engl J Med 351:42–47PubMedCrossRefGoogle Scholar
  6. Didier ES, Bessinger GT (1999) Host-parasite relationships in microsporidiosis: animal models and immunology. In: Wittner M, Weiss LM (eds) Microsporidia and microsporidiosis. Washington D.C, ASM, pp 225–257Google Scholar
  7. 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 34:2803–2811PubMedGoogle Scholar
  8. Franzen C, Nassonova ES, Scholmerich J, Issi IV (2006) Tranfer of the members of the genus Brachiola (Microsporidia) to the genus Anncaliia based on ultrastructural and molecular data. J Eukaryot Microbiol 53:26–35PubMedCrossRefGoogle Scholar
  9. Hirsch JG, Fedorko ME (1968) Ultrastructure of human leukocytes after simultaneous fixation with glutaraldehyde and osmium tetroxide and “postfixation” in uranyl acetate. J Cell Biol 38:615–627PubMedCrossRefGoogle Scholar
  10. Hollister WS, Canning EU, Weidner E, Field AS, Kench J, Marriott DJ (1996) Development and ultrastructure of Trachipleistophora hominis n.g., n.sp. after in vitro isolation from an AIDS patient and inoculation into athymic mice. Parasitology 112:143–154PubMedCrossRefGoogle Scholar
  11. Juarez SI, Putaporntip C, Jongwutiwes S, Ichinose A, Yanagi T, Kanbara H (2005) In vitro cultivation and electron microscopy characterization Trachipleistophora anthropophthera isolated from the cornea of an AIDS patient. J Eukaryot Microbiol 52:179–190PubMedCrossRefGoogle Scholar
  12. Kucerova Z, Moura H, Visvesvara GS, Leitch GJ (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 51:339–343PubMedCrossRefGoogle Scholar
  13. 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 47:221–234PubMedCrossRefGoogle Scholar
  14. Malone LA, Wigley PJ, Dhana SD (1987) Identity of a microsporidium from three New Zealand pasture insects: Costelytra zealandica (Coleoptera, Scarabeidae), Wiseana spp. (Lepidoptera, Hepialidae), and Listronotus bonariensis (Coleoptera, Curculionidae). J Invertebr Pathol 49:135–144Google Scholar
  15. Mathis A, Weber R, Deplazes P (2005) Zoonotic potential of the microsporidia. Clin Microbiol Rev 18:423–445PubMedCrossRefGoogle Scholar
  16. Müller A, Stellermann K, Hartmann P, Schrppe M, Fätkenheuer G, Salzberger B, Diehl V, Franzen C (1999) A powerful DNA extraction method and PCR for detection of microsporidia in clinical stool specimens. Clin Diagn Lab Immun 6:243–246Google Scholar
  17. Undeen AH, Krueger CM (1992) Effect of Nosema algerae on the house fly Musca domestica (Diptera: Muscidae). J Am Mosquito Contr 8:268–271Google Scholar
  18. Undeen AH, Maddox JV (1973) The infection of nonmosquito hosts by injection with spores of the microsporidian Nosema algerae. J Invertebr Pathol 22:258–263PubMedCrossRefGoogle Scholar
  19. Vávra J, Undeen AH (1970) Nosema algerae n. sp. (Cnidospora, Microsporida) a pathogen in a laboratory colony of Anopheles stephensi Liston (Diptera, Culicidae). J Protozool 17:240–249PubMedGoogle Scholar
  20. Vávra J, Maddox JV (1976) Methods in microsporidiology. In: Bulla LA Jr, Cheng TC (eds) Comparative pathobiology of the microsporidia. Plenum, New York, pp 281–319Google Scholar
  21. Vávra 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 Parasit 54:259–271Google Scholar
  22. 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 45:273–283PubMedCrossRefGoogle Scholar
  23. Vávra J, Horák A, Modrý D, Lukeš J, Koudela B (2006) Trachipleistophora extenrec n. sp. a new microsporidian (Fungi: Microsporidia) infecting mammals. J Eukaryot Microbiol 53:464–476PubMedCrossRefGoogle Scholar
  24. Visvesvara GS, Belloso M, Moura H, Da Silva AJ, Moura INS, Leitch GJ, Schwartz DA, Chevez-Barrios P, Wallace S, Pieniazek NJ, Goosey JD (1999) Isolation of Nosema algerae from the cornea of an immunocompetent patient. J Eukaryot Microbiol 46:10SPubMedCrossRefGoogle Scholar
  25. Visvesvara GS, Moura H, Leitch GJ, Schwartz DA, Xiao LX (2005) Public health importance of Brachiola algerae (Microsporidia)—an emerging pathogen of humans. Folia Parasit 52:83–94Google Scholar
  26. Weber R, Bryan RT, Schwartz DA, Owen RL (1994) Human microsporidial infections. Clin Microbiol Rev 7:426–461PubMedGoogle Scholar
  27. Weidner E, Canning EU, Hollister WF (1997) The plaque matrix (PQM) and tubules at the surface of intramuscular parasite, Trachipleistophora hominis. J Eukaryot Microbiol 44:359–365PubMedCrossRefGoogle Scholar
  28. Weidner E, Canning EU, Rutledge CR, Meek CL (1999) Mosquito (Diptera: Culicidae) host compatibility and vector competency for the human myositic parasite Trachipleistophora hominis (Phylum Microspora). J Med Entomol 36:522–525PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Jiří Vávra
    • 1
    • 3
    • 4
  • Martin Kamler
    • 5
  • David Modrý
    • 2
    • 5
  • Břetislav Koudela
    • 2
    • 5
  1. 1.Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech RepublicUniversity of South BohemiaČeské BudějoviceCzech Republic
  2. 2.Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech RepublicČeské BudějoviceCzech Republic
  3. 3.Department of Parasitology, Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic
  4. 4.Department of Parasitology, Faculty of ScienceCharles UniversityPragueCzech Republic
  5. 5.Department of Parasitology, Faculty of Veterinary MedicineUniversity of Veterinary and Pharmaceutical Sciences BrnoBrnoCzech Republic

Personalised recommendations