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
2024-04-25
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References

  1. Akhmanova A. A., Voncken F., Boxma B., Vogels G., Veenhuis M., Hackstein J. H., van Alen T., van Hoeck A. 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 Hexamit a 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);
    [Google Scholar]
  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., Hasegawa M., Müller 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;
    [Google Scholar]
  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;
    [Google Scholar]
  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 Coombs G. H. Vickermann K., Sleigh M. A., Warren A. London: Chapman Hall;
    [Google Scholar]
  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. 251–10 [CrossRef]
  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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