Skip to main content

Part of the book series: World Class Parasites ((WCPA,volume 9))

Abstract

Microsporidia are a group of obligate eukaryotic intracellular parasites first recognized over 100 years ago with the description of Nosema bombycis the parasite from silkworms that caused the disease pebrine in these economically important insects. Microsporidia infect almost all animal phyla. Among the more than 144 described genera, several have been demonstrated in human disease: Nosema, Vittaforma, Brachiola, Pleistophora, Encephalitozoon, Enterocytozoon, Septata (reclassified to Encephalitozoon) and Trachipleistophora. In addition, the genus Microsporidium has been used to designate microsporidia of uncertain taxonomic status. The recognition of microsporidia as opportunistic pathogens in humans has led to increased interest in the molecular biology of these pathogens. Recent work has focused on the determination of the nucleotide sequences for ribosomal RNA (rRNA) genes, which have been used as diagnostic tools for species identification as well as for the development of a molecular phylogeny of these organisms. Microsporidia have historically been considered to be “primitive” protozoa, however, molecular phylogenetic analysis has led to the recognition that these organisms are not “primitive” but degenerate and that they are related to the fungi and not to other protozoa. Such molecular phylogeny has also led to the recognition that the traditional phylogeny of these organisms based on structural observations may not reflect the “true” relationships among the various microsporidia species and genera. This chapter reviews the data on the taxonomy of the microsporidia and the relationship of these organisms to other eukaryotes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Arisue, N., L.B. Sanchez, L.M. Weiss, M. Muller, and T. Hashimoto. 2002. Mitochondrial-type 70 genes of the amitochondriate protists, Giardia intestinalis, Entamoeba histolytica and two microsporidians. Parasitology International 51: 9–16.

    Article  PubMed  CAS  Google Scholar 

  • Balbiani, G., 1882. Sur les microsporidies ou psorospermies des articules. Comptes rendus de l’Acadedmie des sciences 95: 1168–1171.

    Google Scholar 

  • Bui, E.T., P.J. Bradley, and P.J. Johnson. 1996. A common evolutionary origin for mitochondira and hydrogenosomes. Proceedings of the National Academy of Sciences USA 93: 9651–9656.

    Article  CAS  Google Scholar 

  • Bürglin, T.R. 2002. The homeobox genes of Encephalitozoon cuniculi (Microsporidia) reveal a putative mating-type locus. Developmental Genes and Evolution. 213: 50–52.

    Google Scholar 

  • Cavalier-Smith T. 1987. Eukaryotes with no mitochondria. Nature 326: 332–333.

    Article  PubMed  CAS  Google Scholar 

  • Chen, W, T. Kuo, and S. Wu. 1998. Development of a new microsporidian parasite, Intrapredatorus barri n.g., n.sp. (Microsporidia: Amblyosporidae) from the predacious mosquito Culex fruscanus Wiedemann (Diptera: Culicidae) Parasitology International 47: 183–193.

    Article  Google Scholar 

  • Clark, C.G., and A.J. Roger. 1995. Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proceedings of the National Academy of Sciences USA 92: 6518–6521.

    Article  CAS  Google Scholar 

  • Coyle, C.M., M. Kent, H.B. Tanowtiz, M. Wittner, and L.M. Weiss. 1998. TNP-470 is an effective anti-microsporidial agent. Journal of Infectious Disease 177: 515–518.

    Article  CAS  Google Scholar 

  • Dayhoff, M.O., R.V. Eck, and C.M. Park. 1972. A model of evolutionary change in proteins, P89–99. In M.O. Dayhoff (ed.) Atlas of Protein Sequence and Structure, vol. 5. National Biomedical Research Foundation, Washington D.C.

    Google Scholar 

  • Desportes, I. 1976. Ulatrastructure de Stempellia mutabilis leger et Hess, microsporidic parasite de l’ephernere Ephemera vulgatta. L. Protistologica 12: 121–150.

    Google Scholar 

  • Didier, E.S. 1997. Effects of albendazole, fumagillin and TNP-470 on microsporidial replication in vitro. Antimicrobial Agents and Chemotherapy 41:1541–1546.

    PubMed  CAS  Google Scholar 

  • DiMaria, P., L. Palic,. B.A. Debrunner-Vossbrinck, J. Lapp, and C.R. Vossbrinck. 1996. Characterization of the highly divergent U2 RNA homolog in the microsporidian Vairimorpha necatrix. Nucleic Acids Research 24: 515–522.

    Article  PubMed  CAS  Google Scholar 

  • Dolflein, F. 1901. Die Protozoen als Parasiten und Krankheitserreger nach biologischen Gesichtspunkten dargestellt. Verlag von Gustav Fisher.

    Google Scholar 

  • Edlind, T.D., J. Li, G.S. Visvesvara, M.H. Vodkin, G.L. McLaughlin, and S.K. Katiyar. 1996. Phylogenetic analysis of beta-tubulin sequences from amitochondrial protozoa. Molecular Phylogenetics and Evolution 5: 357–367.

    Google Scholar 

  • —. 1998. Phylogenetics of protozoan tubulin with reference to the amitochondriate eukaryotes. In: Coombs, G.H., K. Vickerman, M.A. Sleigh and A. Warren. Eds. Evolutionary Relationships Among Protozoa. Chapman & Hall, London, pp. (91–108)

    Google Scholar 

  • Embley, T.M., L.J. Homer, and R.P. Hirt. 1997. Anaerobic eukaryote evolution: hydrogenosomes as biochemically modified mitochondria? TREE 12: 437–441.

    Google Scholar 

  • Fast, N.M., A.J. Roger, C.A. Richardson and W. F. Doolittle. 1998. U2 and U6 snRNA genes in the microsporidian. Nucleic Acids Research 26: 3202–3207.

    Article  PubMed  CAS  Google Scholar 

  • —, J.M. Logsdon, and W.F. Doolittle. 1999. Phylogenetic analysis of the TATA box binding protein (TBP) gene from Nosema locustae: Evidence for a Microsporidia-Fungi relationship and splicosomal intron loss. Molecular Biolology Evolution 6: 1415–1419.

    Google Scholar 

  • Fast, N. M., and P. J. Keeling. 2001. Alpha and beta subunits of pyruvate dehydrogenase E1 from the microsporidian Nosema locustae: mitochondrion-derived carbon metabolism in microsporidia. Molecular and Biochemical Parasitology. 117: 201–209.

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein, J. 1978. Cases in which parsimony or compatibility methods will be positively misleading. Systematic Zoology 27: 401–410.

    Article  Google Scholar 

  • —. 1988. Phylogenies from molecular sequences: inference and reliability. Annual Review of Genetics 22: 521–65.

    Article  PubMed  CAS  Google Scholar 

  • Flegel, TW and T.A. Paharawipas. 1995. A proposal for typical eukaryotic meiosis in microsporidians. Canadian Journal of Microbiology 41: 1–11.

    Article  CAS  Google Scholar 

  • Germot, A., H. Philippe, and H. LeGuyader. 1996. Presence of a mitochondrial-type 70-kDa heat shock protein in Trichomonas vaginalis suggest a very early mitochondrial endosymbiosis in eukaryotes. Proceedings of the National Academy of Sciences USA 93: 14614–14617.

    Article  CAS  Google Scholar 

  • —, —, and —. 1997. Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae. Molecular and Biochemical Parasitology 87:159–168.

    Google Scholar 

  • Hashimoto, T., and M. Hasegawa. 1996. Origin and early evolution of eukaryotes inferred from the amino acid sequences of translation elongation factors 1α/Tu and 2/G. Advances in Biophysics 32: 73–120.

    Article  PubMed  CAS  Google Scholar 

  • —, L.B. Sanches T. Shirakura, M. Muller, and M. Hasegawa. 1998. Secondary absence of mitochondria in Giardia lamblia and Trichomonas vaginalis revealed by valyl-tRNA synthetase phylogeny. Proceedings of the National Academy of Sciences USA 95: 6860–6865.

    Article  CAS  Google Scholar 

  • Hausemann S, C.P. Vivares, and S. Shuman. 2002. Characterization of the mRNA capping apparatus of the microsporidian parasite Encephalitozoon cuniculi. Journal of Biological Sciences 277: 96–102.

    Google Scholar 

  • Hirt, R.P., B. Healy, C.R. Vossbrinck, E.U. Canning, and T.M. Embley. 1997. A mitochondrial HSP70 orthologue in Vairimorpha necatrix: Molecular evidence that microsporidia once contained mitochondria. Current Biology 7: 995–998.

    Article  PubMed  CAS  Google Scholar 

  • —, J.M. Logsdon, B. Healy, M.W. Dorey, W.F. Doolittle, and T.M. Embley. 1999. Microsporidida are related to Fungi: Evidence from the largest subunit of RNA polymerase II and other proteins. Proceedings of the National Academy of Sciences USA 96: 580–585.

    Article  CAS  Google Scholar 

  • Horner, D.S., R.P. Hirt, S. Kilvington, D. Lloyd, and T.M. Embley. 1996. Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proceedings Royal Society London B Biolologic Science 263: 1053–1059.

    Article  CAS  Google Scholar 

  • Huger, A. 1960. Electron microscope study on the cytology of a microsporidian spore by means of ultrathin sectioning. Journal of Insect Pathology 2: 84–105.

    Google Scholar 

  • Issi, I. V. 1986. Microsporidia as a phylum of parasitic protozoa. Academy of Science U.S.S.R. (Leningrad), 10: 6–136.

    Google Scholar 

  • Kamiashi, T., T. Hashimoto, Y. Nakamura, F. Nakamura, S. Murata, N. Okada, D. Okamoto, M. Shimizu and M. Hasegawa. 1996a. Protein phylogeny of translation elongation factor EF-1 alpha suggests microsporidians are extremely ancient eukaryotes. Journal of Molecular Evolution 42:257–263.

    Article  Google Scholar 

  • —, —, —, Y. Masuda, F. Nakamura, K. Okamoto, M. Shimizu, and M. Hasegawa. 1996b. Complete nucleotide sequence of the genes encoding translation elongation factors and 2 from a microsporidian parasite, Glugea plecoglossi: Implications for the deepest branching of eukaryotes. Journal of Biochemistry 120: 1095–1103.

    PubMed  Google Scholar 

  • Katinka, M. D., S. Duprat, E. Cornillot, G. Metenier, F. Thomarat, G. Prensier, V. Barbe, E. Peyretaillade, P. Brottier, P. Wincker, F. Delbac, H. El Alaoui, P. Peyret, W. Saurin, M. Gouy, J. Weissenback, and C.P. Vivares, 2001. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414: 450–453.

    Article  PubMed  CAS  Google Scholar 

  • Keeling P.J., and W. F. Doolittle, 1996. Alpha-Tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. Molecular Biology and Evolution 13: 1297–1305.

    PubMed  CAS  Google Scholar 

  • — and G.I. McFadden. 1998. Origins of microsporidia. Trends in Microbiology 6: 19–23.

    Article  PubMed  CAS  Google Scholar 

  • —, M. A. Luker, and J. D. Palmer. 2000. Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. Molecular Biology and Evolution 17: 23–31.

    PubMed  CAS  Google Scholar 

  • —, and N. M. Fast. 2002. Microsporidia: biology and evolution of highly reduced intracellular parasites. Annual Review of Microbiology 56: 93–116.

    Article  PubMed  CAS  Google Scholar 

  • —. 2003. Congruent evidence from α-tubulin and β- tubulin gene phylogenies for a sygomycete origin of microsporidia. Fungal Genetics and Biology 38: 298–309.

    Article  PubMed  CAS  Google Scholar 

  • Kent, M.L., L. Margolis, and J.O. Corliss. 1994. The demise of a class of protists: taxonomic and nomenclatural revisions proposed for the protist phylum Myxozoa Grassé, 1970. Canadian Journal of Zoology 72: 932–937.

    Google Scholar 

  • Krieg, A. 1955. Ueber Infektionskrankheiten bei Engerlingen von Melolontha sp. unter besonderer Berucksichtigung einer Mikrosporidien-Erkrankung. Zentralblatt fur Bakteriologie Parasitenkunde, Infektionskrankheiten und Hygiene. II Abt 108: 533–538.

    Google Scholar 

  • Kudo, R.R., and E.W. Daniels. 1963. An electron microscope study of the spore of a Microsporidian, Thelohania californica. Journal of Protozoology 10: 112–120.

    PubMed  CAS  Google Scholar 

  • Larsson, J. I. R. 1986. Ultrastructure, function, and classification of microsporidia. Progress in Protistology 1: 325–390.

    Google Scholar 

  • Larsson, J.I.R. 1988. Identification of microsporidian genera (Protozoa, Microspora)— a guide with comments on taxonomy. Archiv fur Protistenkunde 136: 1–37.

    Google Scholar 

  • Leipe, D.D., J. H. Gunderson, T.A. Nerad, and M.L. Sogin. 1993. Small subunit ribosomal RNA of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Molecular and Biochemical Parasitology 59: 41–48

    Article  PubMed  CAS  Google Scholar 

  • Levine, N.D., J.O. Corliss, F.E. Cox, G. Deroux, J. Grain, B.M. Honigberg, G.F. Leedale, A.R. Loeblich 3d, J. Lom, D. Lynn, EG Merinfeld, F.C. Page, G. Poljansky, V. Sprague, J. Vavra, and F.G. Wallace. 1980. A newly revised classification of the protozoa. Journal of Protozoology 27: 37–58.

    PubMed  CAS  Google Scholar 

  • Lom, J., and J. Vavra. 1961. Niektore Wyniki Baden Nad Ultrastruktura Spor Posozyta Ryb Plistophora hyphessobrycornis (Microsporidia). Wiadomosci parazytologiczne 7: 828–832.

    PubMed  CAS  Google Scholar 

  • —, and —. 1962. A Proposal to the Classification within the Subphylum Cnidospora. Systematic Zoology 11: 172–175.

    Google Scholar 

  • Markiw, M.E., and K. Wolf. 1983. Mysoxoma cerebralis (Myxozoa: Myxosporea) etiologic agent of salmonid whirling disease requires tubificid worms (Annelida: Oligochaeta) in its life cycle. Journal of Protozoology 30: 561–564.

    Google Scholar 

  • Maxim, A.M., and W. Gilbert. 1977. A new method for sequencing DNA. Proceedings of the National Academy of Sciences 74: 560–564.

    Article  Google Scholar 

  • Peyretaillade, E., V. Broussolle, P. Peyret, G. Metenier, M. Gouy, and C.P. Vivares. 1998. Microsporidia, amitochondrial protists, possess a 70-kDa heat shock nprotein gene of mitochondrial evolutionary origin. Molecular Biology and Evolution 15: 683–689.

    PubMed  CAS  Google Scholar 

  • Philippe, H. A. Germot, and D. Moreira. 2000. The new phylogeny of eukaryotes. Current Opinions in Genetic Development 10: 596–601.

    Article  CAS  Google Scholar 

  • Roger, A.J., C.G. Clark, and W.F. Doolittle. 1996. A possible mitochondrial gene in the earlybranching amitochondriate protist Trichomonas vaginalis. Proceedings of the National Academy of Sciences USA 93: 14618–14622.

    Article  CAS  Google Scholar 

  • —, S.G. Svard, J. Tovar, C.G. Clark, M.W. Smith, F.D. Gillin, and M.L. Sogin. 1998. A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proceedings of the National Academy of Sciences USA 95: 229–234.

    Article  CAS  Google Scholar 

  • Sanger, F., and H. Tuppy. 1951. The amino-acid sequence in the phenylalanyl chain of insulin. 1. The identification of lower peptides from partial hydrolysates. Biochemistry 49: 463–481.

    CAS  Google Scholar 

  • — and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences 74: 5463–5467.

    Article  CAS  Google Scholar 

  • Siddall, M.E., D.S. Martin, D. Bridge, S.S. Desser, and D.K. Cone. 1995. The demise of a phylum of protists: Phylogeny of myxozoa and other parasitic cnidaria. Journal of Parasitology 81: 961–967.

    Article  PubMed  CAS  Google Scholar 

  • Sogin, M.L., J H. Cunderson, H.J. Elwood, R. A. Alonso, and D. A. Peattie. 1989. Phylogenetic meaning of the kingdom concept: an unusual RNA from Giardia lamblia. Science 243: 75–77.

    Article  PubMed  CAS  Google Scholar 

  • Soltys, B.J., and R.S. Gupta. 1994. Presence and cellular distribution of a 60-Kda protein related to mitochondrial HSP 60 in Giardia lamblia. Journal of Parasitology 80: 580–590.

    Article  PubMed  CAS  Google Scholar 

  • Sprague, V., and Vavra. 1977. “Systematics of the Microsporidia.“ In: ‘Comparative Pathobiology Vol. 2’. (L.A. Bulla and T.C. Cheng. eds.) pp. 1–30. Plenum Press, New York.

    Google Scholar 

  • —, J.J. Becnel and E.I. Hazard. 1992. Taxonomy of the phylum microspora. Critical Review of Microbiology 18: 285–395.

    Article  Google Scholar 

  • —, and —. 1998. Note on the Name-Author-Date combination of the taxon Microsporidies. Balbiani, 1882, When Ranked as a Phylum. Journal of Invertebrate Pathology 71: 91–4.

    Google Scholar 

  • Swofford, D.L, P. J. Waddell, J. P. Huelsenbeck, P. G. Foster, P.O. Lewis, and J. S. Rogers. 2001. Bias in phylogenetic estimation and its relevance to the choice between parsimony and likelihood methods. Journal of Systematic Biology 50: 525–39.

    Article  CAS  Google Scholar 

  • Tuzet, O., J. Maurand, A. Fize, R. Michel, and B. Fenwich. 1971. Proposition d’un nouveau cadre systematique por les genres de Microsporidies. Comptes rendus de l’Acadedmie des sciences (Paris) 272: 1268–1271.

    Google Scholar 

  • Williams B.A.P., R.P. Hirt, J.M. Lucocq, and T.M. Embley. 2002. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418: 865–869.

    Article  PubMed  CAS  Google Scholar 

  • Weill, R. 1938 L’interpretation des Cnidosporides et la valeur taxonomique de leur cnidome. Leur cycle comparé è la phase larvaire des Narcomeduses Cuninides. Travaux de la Station Zoologique de Wimereaux. 13: 727–744.

    Google Scholar 

  • Weiser, J. 1959. Nosema laphygmae n. sp. and the internal structure of the microsporidian spore. Journal of Insect Pathology 1: 52–59.

    Google Scholar 

  • —. 1977. Contribution to the classification of microsporidia. Vestnick Ceskoslovenske Spolecnost Zoologica. 41: 308–320.

    Google Scholar 

  • Woese, C.R., and Fox, G.E. 1977. Phylogenetic structure of the prokaryotic domain: The primary kingdoms. Proceedings of the National Academy of Sciences USA 74: 5088–5090.

    Article  CAS  Google Scholar 

  • Van de Peer Y, A. Ben Ali, and A. Meyer. 2000. Microsporidia: accumulating molecular evidence that a group of amitochondriate and suspectedly primitive eukaryoties are just curious fungi. Gene 246: 1–8.

    Article  PubMed  Google Scholar 

  • Vossbrinck, C.R., and C.R. Woese. 1986. Eukaryotic ribosomes that lack a 5.8s RNA. Nature 320: 287–288.

    Article  PubMed  CAS  Google Scholar 

  • —, J.V. Maddox, S. Friedman, B.A. Debrunner-Vossbrinck, and C.R. Woese. 1987. Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326: 411–414

    Article  PubMed  CAS  Google Scholar 

  • Vivares, C., C. Biderre, F. Duffieux, E. Peyretaillade, P. Peyret, G. Metenier, and M. Pages. 1996. Chromosomal localization of five genes in Encephalitozoon cuniculi (microsporidia). Journal of Eukaryotic Microbiology. 43: 97S

    Article  PubMed  CAS  Google Scholar 

  • —, M. Gouy, F. Thomarat, and G. Metenier. 2002. Functional and evolutionary analysis of a eukaryotic parasitic genome. Current Opinions in Microbiology 5: 499–505.

    Article  CAS  Google Scholar 

  • Yang D., Y. Oyaizu, H. Oyaizu, G.J. Olsen, and C.R. Woese. 1985. Mitochondrial origins. Proceedings of the National Academy of Sciences U.S.A. 82: 4443–4447.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2004 Kluwer Academic Publishers

About this chapter

Cite this chapter

Vossbrinck, C.R., Andreadis, T.G., Weiss, L.M. (2004). Phylogenetics: Taxonomy and the microsporidia as derived fungi. In: Lindsay, D.S., Weiss, L.M. (eds) Opportunistic Infections: Toxoplasma, Sarcocystis, and Microsporidia. World Class Parasites, vol 9. Springer, Boston, MA. https://doi.org/10.1007/978-1-4020-7846-0_11

Download citation

  • DOI: https://doi.org/10.1007/978-1-4020-7846-0_11

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4020-7814-9

  • Online ISBN: 978-1-4020-7846-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics