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Genetic and immunological characterization of the microsporidian Septata intestinalis Cali, Kotler and Orenstein, 1993: reclassification to Encephalitozoon intestinalis

Published online by Cambridge University Press:  06 April 2009

R. A. Hartskeerl ,
T. Van Gool ,
A. R. J. Schuitema ,
E. S. Didier  and
W. J. Terpstra
R. A. Hartskeerl
Affiliation:
Department of Biomedical Research, Royal Tropical Institute (KIT), Meibergdreef 39, 1105 AZ Amsterdam, The Netherlands
T. Van Gool
Affiliation:
Department of Medical Microbiology, Academical Medical Center, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands
A. R. J. Schuitema
Affiliation:
Department of Biomedical Research, Royal Tropical Institute (KIT), Meibergdreef 39, 1105 AZ Amsterdam, The Netherlands
E. S. Didier
Affiliation:
Department of Microbiology, Tulane Regional Primate Research Centre, 18703 Three Rivers Road, Covington, LA 70433, USA
W. J. Terpstra
Affiliation:
Department of Biomedical Research, Royal Tropical Institute (KIT), Meibergdreef 39, 1105 AZ Amsterdam, The Netherlands
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Summary

Th relationships between the Encephalitozoon-like Septata intestinalis and other microsporidia that occur in humans, notably Encephalitozoon cuniculi and Encephalitozoon hellem, is insufficiently documented using morphological descriptions alone. To assess mutual relationships, we have examined other phenotypic as well as genetic aspects of S. intestinalis, obtained both from tissue culture and clinical specimens, in comparison with a number of other microsporidia. Phenotypic characterization was performed by analysis of the protein composition and antigenic structure of various microsporidian spores by SDS-PAGE and Western blotting. The genetic characterization consisted of the determination of the sequence of the S. intestinalis rrs gene encoding the small subunit ribosomal RNA (srRNA), restriction fragment length polymorphism (RFLP) analysis of amplified rrs genes and establishment of the degree of sequence identity between rrs genes of various microsporidian species. The unique sequence of rrs of S. intestinalis as well as the distinct RFLP and SDS-PAGE profiles indicate that S. intestinalis is clearly different from other human microsporidian species. However, its rrs gene shared about 90% sequence identity with rrs of both Encephalitozoon spp., E. cuniculi and E. hellem. This is remarkably higher than the about 70% identity observed between rrs of microsporidian species which belong to different genera and thus suggests that S. intestinalis should be regarded as a species of the genus Encephalitozoon. Western blots revealed a marked cross-reactivity between S. intestinalis and both species of Encephalitozoon which also stresses the close relationship between these organisms. It is concluded that S. intestinalis is so closely related to E. cuniculi, the type species of Encephalitozoon, that it should be reclassified as Encephalitozoon intestinalis.

Keywords

Microsporidia, EncephalitozoonSeptata intestinalispolymerase chain reactiondiagnosissmall subunit ribosomal RNAWestern blot immunodetection.
Type
Research Article
Information
Parasitology , Volume 110 , Issue 3 , April 1995 , pp. 277 - 285
Copyright
Copyright © Cambridge University Press 1995

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References

REFERENCES

Boom, R., Sol, C. J. A., Salismans, M. M. M., Jansen, C. L., Wertheim-Van Dillen, P. M. E. & Van Der Noordaa, J. (1990). Rapid and simple method for purification of nucleic acids. Journal of Clinical Microbiology 28, 495–503.CrossRefGoogle ScholarPubMed
Cali, A. (1991). General microsporidian features and recent findings on AIDS isolates. Journal of Protozoology 38, 625–30.Google ScholarPubMed
Cali, A., Kotler, D. P. & Orenstein, J. M. (1993). Septata intestinalis, N. G., N. Sp., an intestinal microsporidian associated with chronic diarrhea and dissemination in AIDS patients. Journal of Eukaryotic Microbiology 40, 101–2.CrossRefGoogle Scholar
Canning, E. U., Field, A. S., Hing, M. C. & Marriott, D. J. (1994). Further observations on the ultrastructure of Septata intestinalis Cali, Kotler and Orenstein, 1993. European Journal of Protistology 40, 414–22.CrossRefGoogle Scholar
Davis, R. M., Font, R. L., Keisler, M. S., & Shadduck, J. A. (1990). Corneal microsporidiosis. A case report including ultrastructural observations. Ophthalmology 97, 953–7.CrossRefGoogle ScholarPubMed
Desportes, I., Lecharpentier, I., Galian, A., Bernard, F., Cochand-Priollet, B., Lavergne, A., Ravisse, P. & Modigliani, R. (1985). Occurrence of a new microsporidian: Enterocytozoon bieneusi, n.g., n.s., in the enterocytes of a human patients with AIDS. Journal of Protozoology 32, 250–4.CrossRefGoogle Scholar
Desser, S. S., Hong, H. & Yang, Y. J. (1992). Ultrastructure of the development of a species of Encephalitozoon cultured from the eye of an AIDS patient. Parasitology Research 78, 677–83.CrossRefGoogle ScholarPubMed
Devereux, J., Haeberli, P. & Smithies, O. (1984). A comprehensive set of sequence analysis programs for the Vax. Nucleic Acids Research 12, 387–95.CrossRefGoogle ScholarPubMed
De Wit, M. Y. L., Faber, W. R., Krieg, S. R., Douglas, J. T., Lucas, S. B., Montreewasuwat, N., Pattyn, S. R., Hussan, R., Ponninghaus, J. M., Hartskeerl, R. A. & Klatser, P. R. (1991). Application of a polymerase chain reaction for the detection of Mycobacterium leprae in skin tissues. Journal of Clinical Microbiology 29, 906–10.CrossRefGoogle ScholarPubMed
Didier, E. S., Didier, P. J., Friedberg, D. N., Stenson, S. M., Orenstein, J. M., Yee, R. W., Tio, F. O., Davis, R. M., Vossbrinck, C., Millichamp, N. & Shadduck, J. A. (1991 a). Isolation and characterization of a new human microsporidian, Encephalitozoon hellem (n. sp.) from three AIDS patients with keratoconjunctivitis. Journal of Infectious Diseases 163, 617–21.CrossRefGoogle Scholar
Didier, P. J., Orenstein, J. M., Didier, E. S. & Shadduck, J. A. (1991 b). Fine structure of a new human microsporidian, Encephalitozoon hellem, in culture. Journal of Protozoology 38, 502–7.CrossRefGoogle ScholarPubMed
Field, A. S., Hing, M. C., Millikin, S. T. & Marriot, D. J. (1993). Microsporidia in the small intestine of HIV-infected patients. Medical Journal of Australia 158, 390–4.CrossRefGoogle ScholarPubMed
Friedberg, D. N., Stenson, S. M., Orenstein, J. M., Tiero, P. & Charles, N. (1990). Microsporidial keratoconjunctivitis in the acquired immunodeficiency syndrome. Archives of Ophthalmology 108, 504–8.CrossRefGoogle ScholarPubMed
Harlow, E. & Lane, D. (1988). Antibodies: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.Google Scholar
Hartskeerl, R. A., Schuitema, A. R. J. & De Wachter, R. (1993 a). Secondary structure of the small subunit ribosomal RNA sequence of the microsporidium Encephalitozoon cuniculi. Nucleic Acids Research 21, 1489.CrossRefGoogle ScholarPubMed
Hartskeerl, R. A., Schuitema, A. R. J., Van Gool, T. & Terpstra, W. J. (1993 b). Genetic evidence for the occurrence of extra-intestinal Enterocytozoon bieneusi infections. Nuclei Acids Research 21, 4150.CrossRefGoogle ScholarPubMed
Hazard, E. I. & Weiser, J. (1968). Spores of Thelohania in adult female Anopheles: development and transovarial transmission and redescription of T. legeri Hesse and T. obesa Kudop. Journal of Protozoology 15, 817–23.CrossRefGoogle Scholar
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227, 680–5.CrossRefGoogle ScholarPubMed
Olsen, G. J., Lane, D. J., Giovannoni, S. J., Pace, N. R. & Stahl, D. A. (1986). Microbial ecology and evolution: a ribosomal RNA approach. Annual Reviews of Microbiology 40, 337–65.CrossRefGoogle ScholarPubMed
Orenstein, J. M., Chiang, J., Steinberg, W., Smith, P., Rotterdam, H. & Kotler, D. P. (1990). Intestinal microsporidiosis as a cause of diarrhea in HIV-infected patients. A report of 20 cases. Human Pathology 21, 475–81.CrossRefGoogle ScholarPubMed
Orenstein, J. M., Dieterich, D. T. & Kotler, D. P. (1992). Systemic dissemination of newly recognized intestinal microsporidia species in AIDS. AIDS 6, 1143–50.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.Google Scholar
Shadduck, J. A. (1969). Nosema cuniculi: in vitro isolation. Science 166, 516–17.CrossRefGoogle ScholarPubMed
Shadduck, J. A., Meccoli, R. A., Davis, R. & Font, R. L. (1990). First isolation of a microsporidian from a human patient. Journal of Infectious Diseases 162, 773–6.CrossRefGoogle Scholar
Schuitema, A. R. J., Hartskeerl, R. A., Van Gool, T., Laxminarayan, R. & Terpstra, W. J. (1993). Application of the polymerase chain reaction for the diagnosis of microsporidiosis. AIDS 7 (Suppl. 3), S57–S61.Google Scholar
Takvorian, P. M. & Cali, A. (1983). Appendages associated with Glugea stephani, a microsporidian found in flounder. Journal of Protozoology 30, 251–6.CrossRefGoogle Scholar
Van Gool, T., Canning, E. U., Gilis, H., Van Den Bergh Weerman, M. A., Schattenkerk, J. K. M.Eeftinck & Dankert, J. (1994). Septota intestinalis frequently isolated from stool of AIDS patients with a new cultivation method. Parasitology 109, 281–9.CrossRefGoogle ScholarPubMed
Van Gool, T., Hollister, W., Schattenkerk, J.Eeftinck, Van Den Bergh Weerman, M. A., Terpstra, W. J., Van Ketel, R., Reiss, P. & Canning, E. U. (1990). Diagnosis of Enterocytozoon bieneusi in AIDS patients by recovery of spores from faeces. Lancet 336, 697–8.CrossRefGoogle ScholarPubMed
Visvesvara, G. S., Leitch, G. J., Moura, H., Wallace, S., Weber, R. & Bryan, R. T. (1991). Culture, electron microscopy, and immunoblot studies on a microsporidian parasite isolated from the urine of a patient with AIDS. Journal of Protozoology 38, 105S–11S.Google ScholarPubMed
Vossbrinck, C. R., Baker, M., Didier, E. S., Vossbrinck, B. D. & Shadduck, J. A. (1993). rDNA sequences of Encephalitozoon hellem and Encephalitozoon cuniculi: species identification and phylogenetic construction. Journal of Eukaryotic Microbiology 40, 354–62.CrossRefGoogle ScholarPubMed
Vossbrinck, C. R., Maddox, J. V., Friedman, S., Debrunner-Vossbrinck, B. A. & Woese, C. R. (1987). Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature, London 326, 411–14.CrossRefGoogle ScholarPubMed
Woese, C. R. (1987). Bacterial evolution. Microbiological Reviews 5, 221–71.CrossRefGoogle Scholar
Yee, R. W., Tio, F. O., Martinez, J. A., Held, K. S., Shadduck, J. A. & Didier, E. S. (1991). Resolution of microsporidial epithelial keratopathy in a patient with AIDS. Ophthalmology 98, 196–201.CrossRefGoogle Scholar