Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T11:38:18.940Z Has data issue: false hasContentIssue false
  • English
  • Français

Maltose utilization by extracellular hydrolysis followed by glucose transport in Trichomonas vaginalis

Published online by Cambridge University Press:  06 April 2009

B. H. Ter Kuile  and
M. Müller
B. H. Ter Kuile
Affiliation:
The Rockefeller University, 1230 York Avenue, New York, NY 10021, USA
M. Müller
Affiliation:
The Rockefeller University, 1230 York Avenue, New York, NY 10021, USA
Get access Rights & Permissions [Opens in a new window]

Extract

The amitochondriate parasitic protist Trichomonas vaginalis can utilize either glucose or maltose as carbon and energy source. The mechanisms of maltose utilization were explored with uptake experiments using radio-isotope labelled maltose in combination with the silicone-oil centrifugation technique and enzymatic assays measuring maltose hydrolysis. The uptake of maltose label became saturated after 2–3 h. The uptake of maltose as a function of the external maltose concentration was linear at low concentrations with no further increase at higher levels, kinetics characteristic of reactions obeying Michaelis–Menten kinetics preceded by a diffusion-limited step. Increased viscosity of the medium resulted in decreased maltose uptake, indicating an extracellular location of the diffusion-limited step. Most of the cellular α-glucosidase activity of T. vaginalis was detected on the cell surface, suggesting that maltose is hydrolysed to glucose outside the cell. Glucose interfered more with maltose uptake, and maltose less with glucose uptake, than would be expected if 1 mol of maltose were the equivalent of 2 mol of glucose. This pattern of interaction indicated that the interference occurs before the common metabolic pathway and even before the transport step, supporting the idea of extracellular maltose hydrolysis. We conclude that maltose is hydrolysed to glucose in the boundary layer of the cell, a process akin to membrane digestion in vertebrate enterocytes and on the teguments of helminths. The glucose formed is then transported by the glucose carrier of the organism.

Keywords

maltose metabolismα-glucosidasemembrane digestionparasitic protist
Type
Research Article
Information
Parasitology , Volume 110 , Issue 1 , January 1995 , pp. 37 - 44
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Benito, B. & Lacunas, R. (1992). The low-affinity component of Saccharomyces cerevisiae maltose transport is an artifact. Journal of Bacteriology 174, 3065–9.CrossRefGoogle ScholarPubMed
Bergmeyer, H. U. (1974). Enzymes as biochemical reagents: hexokinase. In Methods of Enzymatic Analysis (ed. Bergmeyer, H. U.), p. 473. New York: Academic Press.Google Scholar
Carruthers, A. (1990). Facilitated diffusion of glucose. Physiological Reviews 70, 1135–76.CrossRefGoogle ScholarPubMed
Diamond, L. S. (1957). The establishment of various trichomonads of animals and man in axenic cultures. Journal of Parasitology 43, 488–90.CrossRefGoogle ScholarPubMed
Doran, D. J. (1957). Studies on trichomonads. I. The metabolism of Tritrichomonas foetus and trichomonads from the nasal cavity and cecum of swine. Journal of Protozoology 4, 182–90.CrossRefGoogle Scholar
Gottlieb, M. (1989). The surface membrane 3′-nucleotidase/nuclease of trypanosomatid protozoa. Parasitology Today 5, 257–60.CrossRefGoogle ScholarPubMed
Hill, R. & Whittingham, C. P. (1955). Photosynthesis. London: Methuen.Google Scholar
Kiy, T. & Tiedtke, A. (1991). Lysosomal enzymes produced by immobilized Tetrahymena thermophila. Applied Microbiology and Biotechnology 35, 14–18.CrossRefGoogle ScholarPubMed
Linstead, D. & Cranshaw, M. A. (1983). The pathway of arginine catabolism in the parasitic flagellate Trichomonas vaginalis. Molecular and Biochemical Parasitology 8, 241–52.CrossRefGoogle ScholarPubMed
Markos, A., Miretsky, A. & Müller, M. (1993). A glyceraldehyde 3-phosphate dehydrogenase with eubacterial features in the amitochondriate eukaryote, Trichomonas vaginalis. Journal of Molecular Evolution 37, 631–43.CrossRefGoogle ScholarPubMed
Mertens, E. & Müller, M. (1990). Glucokinase and fructokinase of Trichomonas vaginalis and Tritrichomonas foetus. Journal of Protozoology 37, 384–8.CrossRefGoogle ScholarPubMed
Müller, M. (1972). Secretion of acid hydrolases and its intracellular source in Tetrahymena pyriformis. Journal of Cell Biology 52, 478–87.CrossRefGoogle ScholarPubMed
Müller, M. (1989). Biochemistry of Trichomonas vaginalis. In Trichomonads Parasitic in Humans (ed. Honigberg, B. M.), pp. 53–83. New York: Springer.Google Scholar
Read, C. P. (1957). Comparative studies on the physiology of trichomonad protozoa. Journal of Parasitology 43, 385–94.CrossRefGoogle ScholarPubMed
Sanchez-Moreno, M., Lasztity, D., Coppens, I. & Opperdoes, F. R. (1992). Characterization of carbohydrate metabolism and demonstration of glycosomes in Phytomonas sp. isolated from Euphorbia characias. Molecular and Biochemical Parasitology 54, 185–200.CrossRefGoogle ScholarPubMed
Schwartz, M. (1987). The maltose regulon. In Escherichia coli and Salmonella typhimurium Cellular and Molecular Biology (ed. Neidharde, F. C.), pp. 1482–1502. Washington, DC: American Society for Microbiology.Google Scholar
Semenza, G. (1987). Glycosidases. In Mammalian Ectoenzymes (ed. Kenny, A. J. & Turner, A. J.), pp. 265–87. Amsterdam: Elsevier Science Publishers.Google Scholar
Serrano, R. (1977). Energy requirements for maltose transport in yeast. European Journal of Biochemistry 80, 97–102.CrossRefGoogle ScholarPubMed
Stanley, K. K., Newby, A. C. & Luzio, J. P. (1982). What do ectoenzymes do? Trends in Biochemical Science 7, 145–7.CrossRefGoogle Scholar
Ter, Kuile B. H. (1993). Glucose and proline transport in kinetoplastids. Parasitology Today 9, 206–10.Google Scholar
Ter, Kuile B. H. (1994). Adaptation of the carbon metabolism of Trichomonas vaginalis to the nature and availability of the carbon source. Microbiology 140, 2503–10.Google Scholar
Ter, Kuile B. H. & Müller, M. (1993). Interaction between facilitated diffusion of glucose across the plasma membrane and its metabolism in Trichomonas vaginalis. FEMS Microbiology Letters 110, 27–32.Google Scholar
Ter, Kuile B. H. & Opperdoes, F. R. (1992). Comparative physiology of two protozoan parasites, Leishmania donovani and Trypanosoma brucei, grown in chemostats. Journal of Bacteriology 174, 2929–34.Google Scholar
Thomson, A. B. R. & Dietschy, J. M. (1984). The role of the unstirred water layer in intestinal permeation. In Pharmacology of Intestinal Permeation II (ed. Csaky, T. Z.), pp. 165–269. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Trussel, R. E. & Johnson, G. (1941). Physiology of pure culture of Trichomonas vaginalis: III. Fermentation of carbohydrates and related compounds. Proceedings of the Society for Experimental Biology and Medicine 47, 176–8.CrossRefGoogle Scholar
Ugolev, A. M. (1965). Membrane (contact) digestion. Physiological Reviews 45, 555–95.CrossRefGoogle ScholarPubMed
Ugolev, A. M., Iezuitova, N. N. & Smirnova, L. F. (1984). Role of digestive enzymes in the permeability of the enterocyte. In Pharmacology of Intestinal Permeation II (ed. Csaky, T. Z.), pp. 31–117. Berlin: Springer-Verlag.CrossRefGoogle Scholar