Parasitology Research

, Volume 104, Issue 1, pp 35–42

Effects of host temperature and gastric and duodenal environments on microsporidia spore germination and infectivity of intestinal epithelial cells

Original Paper


Approximately 14 of the more than 1,000 species of microsporidia infect humans, only two of which, Enterocytozoon bieneusi and Encephalitozoon intestinalis, cause intestinal microsporidiosis. Clinical isolates of three microsporidia species, E. intestinalis, Encephalitozoon hellem, and the insect parasite, Anncaliia (Brachiola, Nosema) algerae were used in a spore germination assay, and enterocyte attachment and infection assays were performed to model the potential roles of gastric and duodenal environments and host temperature in determining why only one of these microsporidia species causes intestinal microsporidiosis. Enterocyte infection with A. algerae spores was 10% that of the Encephalitozoon species, a difference not attributable to differences in spore attachment to host cells. Prior spore treatment with pepsin in HCl, pancreatic enzymes, or ox bile did not inhibit germination or enterocyte infection by the three microsporidia species. While the Encephalitozoon species differentiated to mature spores within 3 days, the time taken for many enterocytes to turn over, A. algerae took 3–5 days to produce mature spores, near the upper limit for enterocyte turnover in vivo. Thus, host temperature may contribute to A. algerae not causing human intestinal microsporidiosis, but none of the factors tested account for the inability of E. hellem to cause such an infection.


  1. Avery SW, Undeen AH (1987) The isolation of microsporidia and other pathogens from concentrated ditch water. J Am Mosq Control Assoc 3:54–58PubMedGoogle Scholar
  2. Cotte L, Rabodonirina M, Chapuis F, Bailly F, Bissuel F, Raynal C, Gelas P, Persat F, Piens M-A, Trepo C (1999) Waterborne outbreak of intestinal microsporidiosis in persons with and without human immunodeficiency virus infection. J Infect Dis 180:2003–2008PubMedCrossRefGoogle Scholar
  3. Couzinet S, Cejas E, Schittny J, Deplazes P, Weber R, Zimmerli S (2000) Phagocytic uptake of Encephalitozoon cuniculi by nonprofessional phagocytes. Infect Immun 68:6939–6945PubMedCrossRefGoogle Scholar
  4. 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 microsporidia Brachiola algerae, a mosquito pathogen. N Engl J Med 351:42–47PubMedCrossRefGoogle Scholar
  5. Didier ES (2005) Microsporidiosis: an emerging and opportunistic infection in humans and animals. Acta Trop 94:61–76PubMedCrossRefGoogle Scholar
  6. Didier ES, Orenstein JM, Aldras A, Bertucci D, Rogers LB, Janney FA (1995) Comparison of three staining methods for detecting microsporidia in fluids. J Clin Microbiol 33:3138–3145PubMedGoogle Scholar
  7. Dowd SE, Gerba CP, Pepper IL (1998) Confirmation of human-pathogenic microsporidia Enterocytozoon bieneusi, Encephalitozoon intestinalis, and Vittaforma corneae in water. Appl Environ Microbiol 64:3332–3335PubMedGoogle Scholar
  8. Franzen C (2004) Microsporidia: how can they invade other cells? Trends Parasitol 20:275–279PubMedCrossRefGoogle Scholar
  9. Franzen C, Hosl M, Salzberger B, Hartmann P (2005) Uptake of Encephalitozoon spp. and Vittaforma corneae (microsporidia) by different cells. J Parasitol 91:745–749PubMedCrossRefGoogle Scholar
  10. Franzen C, Nassanova ES, Scholmerich 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 53:26–35PubMedCrossRefGoogle Scholar
  11. 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 44:109–116PubMedCrossRefGoogle Scholar
  12. Graczyk TK, Conn DB, Lucy F, Minchin D, Tamang L, Moura LN, DaSilva AJ (2004) Human waterborne parasites in zebra mussels (Dreissena polymorpha) from the Shannon River drainage area, Ireland. Parasitol Res 93:385–391PubMedCrossRefGoogle Scholar
  13. Graczyk TK, Majewska AC, Schwab KJ (2008) The role of birds in dissemination of human waterborne enteropathogens. Trends Parasitol 24:55–59PubMedCrossRefGoogle Scholar
  14. 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 73:841–848PubMedCrossRefGoogle Scholar
  15. Jones BA, Gore GJ (1997) Physiology and pathophysiology of apoptosis in epithelial cells of the liver, pancreas and intestine. Am J Physiol 273:G1174–G1188PubMedGoogle Scholar
  16. Kotler DP, Orenstein JM (1998) Clinical syndromes associated with microsporidiosis. Adv Parasitol 40:321–341PubMedCrossRefGoogle Scholar
  17. Koudela B, Visvesvara GS, Moura H, Vavra J (2001) The human isolate of Brachiola algerae (Phylum Microsporidia): development in SCID mice and description of its fine structure features. Parasitology 123:153–162PubMedCrossRefGoogle Scholar
  18. 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
  19. Kwakye-Nuako G, Borkettey P, Mansah-Attipoe I, Asmah R, Ayeh-Kumi P (2007) Sachet drinking water in Accra: the potential threats of transmission of enteric pathogenic protozoan organisms. Ghana Med J 41:62–67PubMedGoogle Scholar
  20. Leitch GJ, He Q, Wallace S, Visvesvara GS (1993) Inhibition of the spore polar filament extrusion of the microsporidium, Encephalitozoon hellem, isolated from an AIDS patient. J Eukaryot Microbiol 40:711–717PubMedCrossRefGoogle Scholar
  21. Leitch GJ, Ward TL, Shaw AP, Newman G (2005) Apical spore phagocytosis is not a significant route of infection of differentiated enterocytes by Encephalitozoon intestinalis. Infect Immun 73:7697–7704PubMedCrossRefGoogle Scholar
  22. Lipkin M (1987) Proliferation and differentiation of normal and diseased gastrointestinal cells. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Raven, New York, NY, pp 255–284Google Scholar
  23. Lowman PM, Takvorian PM, Cali A (2000) The effects of elevated temperature 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
  24. Mathis A, Weber R, Deplazes P (2005) Zoonotic potential of the microsporidia. Clin Microbiol Rev 18:423–445PubMedCrossRefGoogle Scholar
  25. Moura H, da Silva AJ, Moura IN, Schwartz DA, Leitch GJ, Wallace S, Pieniazek NJ, Wirtz RA, Visvesvara GS (1999) Characterization of Nosema algerae isolates after continuous cultivation in mammalian cells at 37°C. J Eukaryot Microbiol 46:14S–16SPubMedGoogle Scholar
  26. Muller A, Bialek R, Kamper A, Fatkenheuer G, Salzberger B, Franzen C (2001) Detection of microsporidia in travelers with diarrhea. J Clin Microbiol 39:1630–1632PubMedCrossRefGoogle Scholar
  27. 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. Eukaryotic Cell 6:1354–1362PubMedCrossRefGoogle Scholar
  28. Trammer T, Dumbrowski F, Doehring M, Maier WA, Seitz HM (1997) Opportunistic properties of Nosema algerae (Microspora), a mosquito parasite, in immunocompromised mice. J Eukaryot Microbiol 44:258–262PubMedCrossRefGoogle Scholar
  29. Undeen AH (1975) Growth of Nosema algerae in pig kidney cell culture. J Protozool 22:107–110PubMedGoogle Scholar
  30. Undeen AH, Alger N (1976) Nosema algerae: infection of the white mouse by a mosquito parasite. Exp Parasitol 40:86–88PubMedCrossRefGoogle Scholar
  31. Visvesvara GS, Leitch GJ, Moura H, Wallace S, Weber R, Bryan RT (1991) Culture, electron microscopy, and immunoblot studies on a microsporidian isolated from the urine of a patient with AIDS. J Protozool 38:105S–111SPubMedGoogle Scholar
  32. Visvesvara GS, Moura H, Leitch GJ, Schwartz DA (1999) Culture and propagation of microsporidia. In: Whittner M, Weiss LM (eds) The microsporidia and microsporidiosis. ASM, Washington, DC, pp 363–392Google Scholar
  33. Visvesvara GS, Moura H, Leitch GJ, Schwartz DA, Xiao LX (2005) Public health importance of Brachiola algerae (Microsporidia)—an emerging pathogen of humans. Folia Parasitol (Praha) 52:83–94Google Scholar
  34. Wasson K, Barry PA (2003) Molecular characterization of Encephalitozoon intestinalis (Microsporidia) replication kinetics in a murine intestinal cell line. J Eukaryot Microbiol 50:169–174PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.The Whitney Laboratory for Marine BioscienceUniversity of FloridaSt. AugustineUSA

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