Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

A mitochondrial remnant in the microsporidian Trachipleistophora hominis

Nature volume 418, pages 865–869 (2002)Cite this article

Abstract

Microsporidia are obligate intracellular parasites of several eukaryotes. They have a highly complex and unique infection apparatus but otherwise appear structurally simple1. Microsporidia are thought to lack typical eukaryotic organelles, such as mitochondria and peroxisomes. This has been interpreted as support for the hypothesis that these peculiar eukaryotes diverged before the mitochondrial endosymbiosis, which would make them one of the earliest offshoots in eukaryotic evolution2,3. But microsporidial nuclear genes that encode orthologues of typical mitochondrial heatshock Hsp70 proteins have been detected, which provides evidence for secondary loss of the organelle or endosymbiont4,5,6. In addition, gene trees and more sophisticated phylogenetic analyses have recovered microsporidia as the relatives of fungi, rather than as basal eukaryotes7,8,9. Here we show that a highly specific antibody raised against a Trachipleistophora hominis Hsp70 protein detects the presence, under light and electron microscopy, of numerous tiny (∼50 × 90 nm) organelles with double membranes in this human microsporidial parasite. The finding of relictual mitochondria in microsporidia provides further evidence of the reluctance of eukaryotes to lose the mitochondrial organelle, even when its canonical function of aerobic respiration has been apparently lost.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Characterization of a T. hominis gene encoding a mitochondrial Hsp70.
Figure 2: Analysis of the expression of the T. hominis Hsp70 in spores and infected and non-infected rabbit kidney (RK13) cells using a rabbit polyclonal antibody against T. hominis Hsp70.
Figure 3: Cellular localization of the T. hominis Hsp70 protein detected in situ using immunofluorescence and confocal microscopy.
Figure 4: Transmission electron microscopy of microsporidian structures.

Similar content being viewed by others

References

  1. Vávra, J. & Larsson, J. I. R. in The Microsporidia and Microsporidiosis (eds Wittner, M. & Weiss, L. M.) 7–84 (American Society for Microbiology, Washington DC, 1999)

    Book  Google Scholar 

  2. Cavalier-Smith, T. Eukaryotes with no mitochondria. Nature 326, 332–333 (1987)

    Article  ADS  CAS  Google Scholar 

  3. Vossbrinck, C. R., Maddox, J. V., Friedman, S., Debrunner-Vossbrinck, B. A. & Woese, C. R. Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326, 411–414 (1987)

    Article  ADS  CAS  Google Scholar 

  4. Peyretaillade, E. et al. Microsporidia, amitochondrial protists, possess a 70-kDa heat shock protein gene of mitochondrial evolutionary origin. Mol. Biol. Evol. 15, 683–689 (1998)

    Article  CAS  Google Scholar 

  5. Hirt, R. P., Healy, B., Vossbrinck, C. R., Canning, E. U. & Embley, T. M. A mitochondrial Hsp70 orthologue in Vairimorpha necatrix: molecular evidence that microsporidia once contained mitochondria. Curr. Biol. 7, 995–998 (1997)

    Article  CAS  Google Scholar 

  6. Germot, A., Philippe, H. & Le Guyader, H. Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae. Mol. Biochem. Parasitol. 87, 159–168 (1997)

    Article  CAS  Google Scholar 

  7. Keeling, P. J., Luker, M. A. & Palmer, J. D. Evidence from β-tubulin phylogeny that microsporidia evolved from within the fungi. Mol. Biol. Evol. 17, 23–31 (2000)

    Article  CAS  Google Scholar 

  8. Hirt, R. P. et al. Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc. Natl Acad. Sci. USA 96, 580–585 (1999)

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  10. Arisue, N., Sanchez, L. B., Weiss, L. M., Müller, M. & Hashimoto, T. Mitochondrial-type hsp70 genes of the amitochondriate protists, Giardia intestinalis, Entamoeba histolytica and two microsporidians. Parasitol. Int. 51, 9–16 (2002)

    Article  CAS  Google Scholar 

  11. Fast, N. M. & Keeling, P. J. α and β subunits of pyruvate dehydrogenase E1 from the microsporidian Nosema locustae: mitochondrion-derived carbon metabolism in microsporidia. Mol. Biochem. Parasitol. 117, 201–209 (2001)

    Article  CAS  Google Scholar 

  12. Katinka, M. D. et al. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414, 450–453 (2001)

    Article  ADS  CAS  Google Scholar 

  13. Pfanner, N. & Geissler, A. Versatility of the mitochondrial protein import machinery. Nature Rev. Mol. Cell. Biol. 2, 339–349 (2001)

    Article  CAS  Google Scholar 

  14. Winzeler, E. A. et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901–906 (1999)

    Article  CAS  Google Scholar 

  15. Bukau, B. & Horwich, A. L. The Hsp70 and Hsp60 chaperone machines. Cell 92, 351–366 (1998)

    Article  CAS  Google Scholar 

  16. Lill, R. & Kispal, G. Maturation of cellular Fe-S proteins: an essential function of mitochondria. Trends Biochem. Sci. 25, 352–356 (2000)

    Article  CAS  Google Scholar 

  17. Hollister, W. S. et al. 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, 143–154 (1996)

    Article  Google Scholar 

  18. Huynen, M. A., Snel, B., Bork, P. & Gibson, T. J. The phylogenetic distribution of frataxin indicates a role in iron-sulfur cluster protein assembly. Hum. Mol. Genet. 10, 2463–2468 (2001)

    Article  CAS  Google Scholar 

  19. Akhmanova, A. et al. A hydrogenosome with a genome. Nature 396, 527–528 (1998)

    Article  ADS  CAS  Google Scholar 

  20. van Der Giezen, M. et al. Conserved properties of hydrogenosomal and mitochondrial ADP/ATP carriers: a common origin for both organelles. EMBO J. 21, 572–579 (2002)

    Article  CAS  Google Scholar 

  21. Dyall, S. D. & Johnson, P. J. Origins of hydrogenosomes and mitochondria: evolution and organelle biogenesis. Curr. Opin. Microbiol. 3, 404–411 (2000)

    Article  CAS  Google Scholar 

  22. Tovar, J., Fischer, A. & Clark, C. G. The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol. Microbiol. 32, 1013–1021 (1999)

    Article  CAS  Google Scholar 

  23. Mai, Z. et al. Hsp60 is targeted to a cryptic mitochondrion-derived organelle (‘crypton’) in the microaerophilic protozoan parasite Entamoeba histolytica. Mol. Cell. Biol. 19, 2198–2205 (1999)

    Article  CAS  Google Scholar 

  24. Canning, E. U. in Handbook of Protoctista (eds Margulis, L., Corliss, J. O., Melkonian, M. & Chapman, D. J.) 53–72 (Jones and Bartlett, Boston, 1990)

    Google Scholar 

  25. Roger, A. J. et al. A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc. Natl Acad. Sci. USA 95, 229–234 (1998)

    Article  ADS  CAS  Google Scholar 

  26. Cheney, S. A., Lafranchi-Tristem, N. J. & Canning, E. U. Serological differentiation of microsporidia with special reference to Trachipleistophora hominis. Parasite 8, 91–97 (2001)

    Article  CAS  Google Scholar 

  27. Lockhart, P. J., Steel, M. A., Hendy, M. D. & Penny, D. Recovering evolutionary trees under a more realistic model of sequence evolution. Mol. Biol. Evol. 11, 605–612 (1994)

    CAS  PubMed  Google Scholar 

  28. Wilbanks, S. in Guidebook to the Molecular Chaperones and Protein-Folding Catalysts (ed. Gething, M.-J. H.) 13–18 (Oxford Univ. Press, New York, 1997)

    Google Scholar 

  29. Buchberger, A. & Bukau, B. in Guidebook to the Molecular Chaperones and Protein-Folding Catalysts (ed. Gething, M.-J. H.) 22–25 (Oxford Univ. Press, New York, 1997)

    Google Scholar 

Download references

Acknowledgements

We thank E. Canning for the T. hominis culture system and advice on growing microsporidia; M. Duchen and A. Ball for help with confocal microscopy; C. Thomson for help with electron microscopy; and C. Danpure and G. Birdsey for comments on the manuscript and help with heterologous transfection experiments. J.M.L. was supported by a Wellcome Trust Research Leave Fellowship and Tenovus Scotland. B.A.P.W. was supported by a Wellcome Trust Biodiversity studentship, R.P.H. was supported by a Wellcome Trust University award.

Author information

Authors and Affiliations

  1. Department of Zoology, The Natural History Museum, Cromwell Road, SW7 5BD, London, UK

    Bryony A. P. Williams, Robert P. Hirt & T. Martin Embley

  2. School of Life Sciences, WTB/MSI complex, University of Dundee, DD1 5EH, Dundee, UK

    John M. Lucocq

Authors
  1. Bryony A. P. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert P. Hirt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John M. Lucocq
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. Martin Embley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. Martin Embley.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Williams, B., Hirt, R., Lucocq, J. et al. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418, 865–869 (2002). https://doi.org/10.1038/nature00949

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature00949

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing