1887

Abstract

Here it is shown that the flagellated protozoon , commonly regarded as an early branching eukaryote because of its lack of mitochondria, has membraneous structures that partition the cationic, membrane-potential-sensitive fluorophore rhodamine 123. This organism also reduces a tetrazolium fluorogen at discrete plasma-membrane-associated sites. That these functions occur in distinctive specialized membrane systems supports the growing evidence that may not be primitive, but is derived from an aerobic, mitochondria-containing flagellate.

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2002-05-01
2019-12-13
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References

  1. Akhmanova, A. A., Voncken, F., van Alen, T., van Hoeck, A., Boxma, B., Vogels, G., Veenhuis, M. & Hackstein, J. H. ( 1998; ). A hydrogenosome with a genome. Nature 396, 527-528.[CrossRef]
    [Google Scholar]
  2. Biagini, G. A., Suller, M. T. E., Finlay, B. J. & Lloyd, D. ( 1997a; ). Oxygen uptake and antioxidant responses of the free-living diplomonad Hexamita sp. J Eukaryot Microbiol 44, 447-453.[CrossRef]
    [Google Scholar]
  3. Biagini, G. A., Hayes, A. J., Suller, M. T. E., Winters, C. & Lloyd, D. ( 1997b; ). Hydrogenosomes of Metopus contortus physiologically resemble mitochondria. Microbiology 143, 1623-1629.[CrossRef]
    [Google Scholar]
  4. Biagini, G. A., Finlay, B. J. & Lloyd, D. ( 1997c; ). Evolution of the hydrogenosome. FEMS Microbiol Lett 155, 133-140.[CrossRef]
    [Google Scholar]
  5. Biagini, G. A., Vander Gizen, M., Hill, B., Winters, C. & Lloyd, D. ( 1997d; ). Ca2+ accumulation of Neocallimastix frontalis L2, a mitochondria-like physiological role. FEMS Microbiol Lett 149, 227-232.[CrossRef]
    [Google Scholar]
  6. Boothroyd, J. C., Wang, A., Campbell, D. A. & Wang, C. C. ( 1987; ). An unusually compact ribosomal DNA repeat in the protozoan Giardia lamblia. Nucleic Acids Res 15, 4065-4084.[CrossRef]
    [Google Scholar]
  7. Cavalier-Smith, T. ( 1987; ). The origin of eukaryotic and archaebacterial cells. Ann N Y Acad Sci 503, 17-54.[CrossRef]
    [Google Scholar]
  8. Chapman, A., Hann, A. C. & Linstead, D. ( 1985; ). Energy-dispersive X-ray microanalysis of membrane-associated inclusions in hydrogenosomes isolated from Trichomonas vaginalis. J Gen Microbiol 131, 2933-2939.
    [Google Scholar]
  9. Chen, L. B. ( 1988; ). Mitochondrial membrane potential in living cells. Ann Rev Cell Biol 4, 155-181.[CrossRef]
    [Google Scholar]
  10. Edlind, T. D. & Chakraborty, P. R. ( 1987; ). Unusual ribosomal RNA of the intestinal parasite Giardia lamblia. Nucleic Acids Res 15, 7889-7901.[CrossRef]
    [Google Scholar]
  11. Edwards, M. R., Gilroy, F. V., Jiminez, M. B. & O’Sullivan, W. J. ( 1989; ). Alanine is a major end product of metabolism of Giardia lamblia: a proton nuclear magnetic resonance study. Mol Biochem Parasitol 37, 19-26.[CrossRef]
    [Google Scholar]
  12. Ellis, J. E., Williams, R., Cole, D., Cammack, R. & Lloyd, D. ( 1993; ). Electron transport components of the parasitic protozoon Giardia lamblia. FEBS Letts 325, 196-200.[CrossRef]
    [Google Scholar]
  13. Embley, T. M. & Hirt, R. P. ( 1998; ). Early branching eukaryotes? Curr Opin Genet Dev 8, 624-629.[CrossRef]
    [Google Scholar]
  14. Embley, T. M., Finlay, B. J., Dyal, P. L., Hirt, R. P., Wilkinson, M. & Williams, A. G. ( 1995; ). Multiple origins of anaerobic ciliates with hydrogenosomes within the radiation of aerobic ciliates. Proc R Soc Lond B Biol Sci 262, 87-93.[CrossRef]
    [Google Scholar]
  15. Embley, T. M., Horner, D. S. & Hirt, R. P. ( 1997; ). Anaerobic eukaryotic evolution: hydrogenosomes as biochemically-modified mitochondria? Trends Ecol Evol 12, 437-441.[CrossRef]
    [Google Scholar]
  16. Finlay, B. J. & Fenchel, T. ( 1989; ). Hydrogenosomes in some anaerobic protozoa resemble mitochondria. FEMS Microbiol Lett 65, 311-314.[CrossRef]
    [Google Scholar]
  17. Germot, A., Philippe, H. & Le Guyader, H. ( 1996; ). Presence of a mitochondrial-type 70-kDa heat shock protein in Trichomonas vaginalis suggests a very early mitochondrial endosymbiosis in eukaryotes. Proc Natl Acad Sci USA 93, 14614-14617.[CrossRef]
    [Google Scholar]
  18. Gupta, R. & Golding, G. B. ( 1996; ). The origin of the eukaryotic cell. Trends Biochem Sci 21, 166-171.[CrossRef]
    [Google Scholar]
  19. Harris, J. C. (2001). Giardia intestinalis, Trichomonas vaginalis and Tritrichomonas foetus: susceptibility to Allium sativum. PhD thesis, University of Wales (Cardiff).
  20. Hashimoto, T., Nakamura, Y., Kamaishi, T., Nakamura, F., Adachi, J., Okamoto, K. & Hasegawa, M. ( 1995; ). Phylogenetic place of mitochondrion-lacking protozoan, Giardia lamblia, inferred from amino acid sequences of elongation factor 2. Mol Biol Evol 12, 782-793.
    [Google Scholar]
  21. Hashimoto, T., Sanchez, L. B., Shirakura, T., Müller, M. & Hasegawa, M. ( 1998; ). Secondary absence of mitochondria in Giardia lamblia and Trichomonas vaginalis revealed by valyl-tRNA synthetase phylogeny. Proc Natl Acad Sci USA 95, 6860-6865.[CrossRef]
    [Google Scholar]
  22. Horner, D. S., Hirt, R. P., Kilvington, S., Lloyd, D. & Embley, T. M. ( 1996; ). Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proc R Soc Lond B Biol Sci 263, 1053-1059.[CrossRef]
    [Google Scholar]
  23. Humphreys, M., Ralphs, J. R., Durrant, L. & Lloyd, D. ( 1998; ). Confocal laser scanning microscopy of Trichomonads. Hydrogenosomes store calcium and show a membrane potential. Eur J Protistol 34, 356-362.[CrossRef]
    [Google Scholar]
  24. Keeling, P. J. ( 1998; ). A Kingdom’s progress: archezoa and the origin of eukaryotes. Bioessays 20, 87-95.[CrossRef]
    [Google Scholar]
  25. Keister, D. B. ( 1983; ). Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 77, 487-488.[CrossRef]
    [Google Scholar]
  26. Lloyd, D. (1974). The Mitochondria of Microorganisms, pp. 3–53. London: Academic Press.
  27. Lloyd, D., Williams, A. G., Yarlett, N. & Hillman, K. ( 1983; ). Similarities between rumen ciliates and Trichomonads: both possess hydrogenosomes. Protistologica 19, 465.
    [Google Scholar]
  28. Lloyd, D., Moran, C. A., Suller, M. T. E. & Dinsdale, M. G. ( 1996; ). Flow cytometric monitoring of rhodamine 123 and cyanine dye uptake by yeast during cider fermentation. J Inst Brew 102, 251-259.[CrossRef]
    [Google Scholar]
  29. Lloyd, D., Harris, J. C., Maroulis, S., Biagini, G. A., Wadley, R. B., Turner, M. P. & Edwards, M. R. ( 2000; ). The microaerophilic flagellate, Giardia intestinalis: oxygen and its reaction products collapse membrane potential and cause cytoxicity. Microbiology 146, 3109-3118.
    [Google Scholar]
  30. López-Garcia, P. & Moreira, D. ( 1999; ). Metabolic symbiosis at the origin of eukaryotes. Trends Biochem Sci 24, 88-93.[CrossRef]
    [Google Scholar]
  31. Madigan, M. T., Martinko, J. M. & Parker, J. (editors) (2000). Brock Biology of Microrganisms, 9th edn. Englewood Cliffs, NJ: Prentice Hall.
  32. Mai, Z., Ghosh, S., Frisardi, M., Rosenthal, B., Rogers, R. & Samuelson, J. ( 1999; ). Hsp60 is targeted to a cryptic mitochondrion-derived organelle (‘crypton’) in the microaerophilic protozoan parasite Entamoeba histolytica. Mol Cell Biol 19, 2198-2205.
    [Google Scholar]
  33. Martin, W. & Müller, M. ( 1998; ). The hydrogen hypothesis for the first eukaryote. Nature 392, 37-41.[CrossRef]
    [Google Scholar]
  34. Meyer, E. A. ( 1976; ). Giardia lamblia: isolation and axenic cultivation. Exp Parasitol 39, 101-105.[CrossRef]
    [Google Scholar]
  35. Müller, M. ( 1998; ). Enzymes and compartmentation of core energy metabolism of anaerobic protists – a special case in eukaryotic evolution? In Evolutionary Relationships among Protozoa , pp. 109-132. Edited by G. H. Coombs, K. Vickermann, M. A. Sleigh & A. Warren. London:Chapman Hall.
  36. Paget, T. A. & Lloyd, D. ( 1990; ). Trichomonas vaginalis requires traces of oxygen and high concentrations of carbon dioxide for optimum growth. Mol Biol Parasitol 41, 65-72.[CrossRef]
    [Google Scholar]
  37. Paget, T. A., Jarroll, E. L., Manning, P., Lindmark, D. G. & Lloyd, D. ( 1989; ). Respiration in the cysts and trophozoites of Giardia muris. J Gen Microbiol 135, 145-154.
    [Google Scholar]
  38. Phillipe, H., Lopez, P., Brinkmann, H., Budin, K., Germot, A., Laurent, J., Moretta, D., Müller, M. & Le Guyader, H. ( 2000; ). Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proc R Soc Lond B Biol Sci 267, 1213-1221.[CrossRef]
    [Google Scholar]
  39. Rodriguez, M. A., Garcia-Perez, R. M., Mendoza, L., Sanchez, T., Guillen, N. & Orozco, E. ( 1998; ). The pyruvate:ferredoxin oxidoreductase enzyme is located in the plasma membrane and in a cytoplasmic structure in Entamoeba. Microb Pathog 25, 1-10.[CrossRef]
    [Google Scholar]
  40. Roger, A. J., Clark, C. G. & Doolittle, W. F. ( 1996; ). A possible mitochondrial gene in the early-branching amitochondriate protist Trichomonas vaginalis. Proc Natl Acad Sci USA 93, 14618-14622.[CrossRef]
    [Google Scholar]
  41. Roger, A. J., Svard, S. G., Tovar, J., Clark, C. G., Smith, M. W., Gillin, F. D. & Sogin, M. L. ( 1998; ). A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that the diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc Natl Acad Sci USA 95, 229-234.[CrossRef]
    [Google Scholar]
  42. Sogin, M. L., Gunderson, J. H., Elwood, H. J., Alonso, R. A. & Peattie, D. A. ( 1989; ). Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243, 75-77.[CrossRef]
    [Google Scholar]
  43. Soltys, B. J. & Gupta, R. S. ( 1994; ). Presence and cellular distribution of a 60-kDa protein related to mitochondrial hsp60 in Giardia lamblia. J Protistol 80, 580-588.
    [Google Scholar]
  44. Tovar, J., Fischer, A. & Clark, C. G. ( 1999; ). The mitosome: a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol Microbiol 32, 1013-1021.[CrossRef]
    [Google Scholar]
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