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The anaerobic end-products of helminths

Published online by Cambridge University Press:  06 April 2009

J. Barrett
J. Barrett
Affiliation:
Department of Zoology, University College of Wales, Aberystwyth
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Extract

Parasitic helminths belong to 3 separate phyla and there is always the danger of over-generalization. The various routes of anaerobic carbohydrate breakdown in parasitic helminth differ in their efficiencies and in their power output. The choice of end-product represents a compromise between these two conflicting forces. In addition, anaerobic pathways must satisfy the redox requirements of the tissues and provide a source of intermediates for synthetic reactions. Other considerations include the metabolic cost of excretion and the effect of end-products on protein structure and function. The different end-products may fulfil additional functions such as pH control, nitrogenous excretion, osmotic regulation, intracellular signalling and the suppression of host responses.

A complicating factor in parasitic helminths is the existence of strains with different biochemical characteristics, including marked variation in end-product formation. The various tissues of the same parasite can also produce different end-products and the pattern of end-product formation is influenced by a variety of extrinsic and intrinsic factors such as age, sex, length of incubation, pO2 and availability of substrates. The catabolic pathways of helminths thus show considerable functional adaptation.

There is, as yet, no satisfactory explanation as to why helminths do not make the maximum use of any oxygen available to them; and the contribution of oxidative processes to the overall energy balance of parasites probably varies from species to species.

The catabolic pathways of adult helminths are derived from the anaerobic pathways present in their free-living relatives. Two main trends are evident, homolactic fermentation and carbon dioxide fixation, the latter involving a partial reverse tricarboxylic acid cycle. In general, homolactic fermentation is found in blood and tissue parasites, carbon dioxide fixation in gut parasites. These two types of metabolism are, of course, in no way absolute, most homolactic fermentors fix carbon dioxide to a certain extent and many parasites which fix carbon dioxide also produce lactate. Parasitic helminths possess a wide range of different catabolic pathways, superimposed upon which is a high degree of functional plasticity.

Type
Trends and Perspectives
Information
Parasitology , Volume 88 , Issue 1 , February 1984 , pp. 179 - 198
Copyright
Copyright © Cambridge University Press 1984

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References

REFERENCES

Barrett, J. (1978). Pyruvate and citrate metabolism in the muscle tissue of Ascaris lumbricoides. Zeitschrift für Parasitenkunde 55, 223–7.CrossRefGoogle ScholarPubMed
Barrett, J. (1981). Biochemistry of Parasitic Helminths. MacMillan: London.CrossRefGoogle Scholar
Barrett, J. & Beis, I. (1973). The redox state of the free nicotinarnide–adenine dinucleotide couple in the cytoplasm and mitochondria of muscle tissue from Ascaris lumbricoides (Nematoda). Comparative Biochemistry and Physiology 44A, 331–40.CrossRefGoogle ScholarPubMed
Bell, G. H., Emslie-Smith, D. & Paterson, C. R. (1976). Textbook of Physiology and Biochemistry, 9th Ed. Edinburgh: Churchill Livingstone.Google Scholar
Bowlus, R. D. & Somero, G. N. (1979). Solute compatibility with enzyme function and structure: rationales for the selection of osmotic agents and end-products of anaerobic metabolism in marine invertebrates. Journal of Experimental Zoology 208, 137–52.CrossRefGoogle ScholarPubMed
von Brand, T. (1966). Biochemistry of Parasites. New York: Academic Press.Google Scholar
Bryant, C. (1982). The biochemical origins of helminth parasitism. In Biology and Control of Endoparasites (ed. Symons, L. E. A., Donald, A. P. and Dineen, J. K.). New York: Academic Press.Google Scholar
Bryant, C. & Behm, C. A. (1976). Regulation of respiratory metabolism in Moniezia expansa under aerobic and anaerobic conditions. In Biochemistry of Parasites and Host–Parasite Relationships (ed. Bossche, H. Van den). Amsterdam: North-Holland.Google Scholar
Coles, G. C. & Simpkin, K. G. (1977). Metabolic gradient in Hymenolepis diminuta under aerobic conditions. International Journal for Parasitology 7, 127–8.CrossRefGoogle ScholarPubMed
Cornish, R. A. & Bryant, C. (1976). The metabolic integrity of Fasciola hepatica during in vitro maintenance. International Journal for Parasitology 6, 387–92.CrossRefGoogle ScholarPubMed
Davson, H. & Danielli, J. F. (1943). The Permeability of Natural Membranes. Cambridge: Cambridge University Press.Google Scholar
De Zwaan, A. (1977). Anaerobic energy metabolism in bivalve molluscs. Oceanography and Marine Biology an Annual Review 15, 103–87.Google Scholar
Fairbairn, D. (1970). Biochemical adaptation and loss of genetic capacity in helminth parasites. Biological Reviews 45, 29–72.CrossRefGoogle ScholarPubMed
Fields, J. H. A. & Quinn, J. F. (1981). Some theoretical considerations on cytosolic redox balance during anaerobiosis in marine invertebrates. Journal of Theoretical Biology 88, 35–45.CrossRefGoogle Scholar
Gnaiger, E. (1977). Thermodynamic considerations of invertebrate anoxibiosis. In Application of Calorimetry in Life Sciences (ed. Lamprecht, I. and Schaarschmidt, B.). Berlin: Walter de Gruyter.Google Scholar
Gruner, B. & Zebe, E. (1978). Studies on the anaerobic metabolism of earthworms. Comparative Biochemistry and Physiology 60B, 441–5.Google Scholar
Hazel, J. R. & Prosser, C. L. (1974). Molecular mechanisms of temperature compensation in poikilotherms. Physiological Reviews 54, 620–77.CrossRefGoogle ScholarPubMed
Hill, A. V. (1929). The diffusion of oxyen and lactic acid through tissues. Proceedings of the Royal Society, B 104, 39–96.Google Scholar
Kluytmans, J. H., Zandee, P. I., Zurburg, W. & Pieters, H. (1980). The influence of seasonal changes on energy metabolism in Mytilus edulis (L). III. Anaerobic energy metabolism. Comparative Biochemistry and Physiology 67B, 307–15.Google Scholar
KÖrting, W. & Barrett, J. (1977). Carbohydrate catabolism in the plerocercoids of Schistocephalus solidus (Cestoda: Pseudophyllidea). International Journal for Parasitology 7, 411–17.CrossRefGoogle Scholar
Krebs, H. A. (1972). The Pasteur effect and the relations between respiration and fermentation. In Essays in Biochemistry, vol. 8 (ed. Campbell, P. N. and Dickens, F.), pp. 1–34. New York: Academic Press.Google Scholar
Lahoud, H., Prichard, R. K., McManus, W. R. & Schofield, P. J. (1971). The dissimilation of leucine, isoleucine and valine to volatile fatty acids by adult Fasciola hepatica. International Journal for Parasitology 1, 223–33.CrossRefGoogle ScholarPubMed
Lloyd, G. M. & Barrett, J. (1983). Fasciola hepatica: aspects of carbohydrate metabolism in the adult parasite. Experimental Parasitology 56, 81–8.CrossRefGoogle Scholar
Mansour, T. E. (1959). Studies on the carbohydrate metabolism of the liver fluke Fasciola hepatica. Biochimica et biophysica acta 34, 456–64.CrossRefGoogle ScholarPubMed
McManus, D. P. & Smyth, J. D. (1978). Differences in the chemical composition and carbohydrate metabolism of Echinococcus granulosus (horse and sheep strains) and E. multilocularis. Parasitology 77, 103–9.CrossRefGoogle ScholarPubMed
McManus, D. P. & Sterry, P. R. (1982). Ligula intestinalis: intermediary carbohydrate metabolism in plerocercoids and adults. Zeitschrift für Parasitenkunde 67, 73–85.CrossRefGoogle Scholar
Opperdoes, F. R. & Borst, P. (1977). Localization of nine glycolytic enzymes in a microbody-like organelle in Trypanosoma brucei: the glycosome. FEBS Letters 80, 360–4.CrossRefGoogle Scholar
Opperdoes, F. R., Borst, P. & Fonch, K. (1976). The potential use of inhibitors of glycerol-3-phosphate oxidase for chemotherapy of African trypanosomiasis. FEBS Letters 62, 169–72.CrossRefGoogle ScholarPubMed
Oudejans, R. C. H. M. & Van Der Horst, P. J. (1974). Aerobic–anaerobic biosynthesis of fatty acids and other lipids from glycolytic intermediates in the pulmonate land snail (Cepaea nemoralis (L.). Comparative Biochemistry and Physiology 47B, 139–47.Google ScholarPubMed
Ovington, K. S. & Bryant, C. (1981). The role of carbon dioxide in the formation of end products by Hymenolepis diminuta. International Journal for Parasitology 11, 221–8.CrossRefGoogle ScholarPubMed
Pappas, P. W. & Read, C. P. (1975). Membrane transport in helminth parasites: a review. Experimental Parasitology 37, 469–530.CrossRefGoogle ScholarPubMed
Podesta, R. B. & Mettrick, D. F. (1974). Pathophysiology of cestode infections: effect of Hymenolepis diminuta on oxygen tensions, pH and gastrointestinal function. International Journal for Parasitology 4, 277–92.CrossRefGoogle ScholarPubMed
Podesta, R. B., Mustafa, T., Moon, T. W., Hulbert, W. C. & Mettrick, D. F. (1976). Anaerobes in an aerobic environment: role of CO2 in energy metabolism of Hymenolepis diminuta. In Biochemistry of Parasites and Host–Parasite Relationships (ed. Bossche, H. Van den). Amsterdam: North-Holland.Google Scholar
Rahman, M. S., Mettrick, D. F. & Cornish, R. A. (1982). Comparative studies of carbohydrate metabolism in two strains of the rat tapeworm Hymenolepis diminuta. Molecular and Biochemical Parasitology (Suppl.) 143. Abstracts 5th International Congress of Parasitology, Toronto.Google Scholar
Read, C. P. (1961). The carbohydrate metabolism of worms. In Comparative Physiology of Carbohydrate Metabolism in Heterothermic Animals (ed.Martin, A. W.). University of Washington Press, Seattle.Google Scholar
Reuter, J. (1968). Studies on plerocercoids of Diphyllobothriunz dendriticum. II. The dependence of lactic and succinic acid excretion on the gas phase. Acta Academiae Aboensis, Ser B. 27, 1–7.Google Scholar
Ridley, R. K., Slonka, G. F. & Leland, S. E. (1977). Utilization of propionic acid by the L4 and adult stages of Cooperia punctala (Nematoda: Trichostrongylidae) grown in vitro. Journal of Parasitology 63, 348–56.CrossRefGoogle ScholarPubMed
Ruben, J. A. & Bennett, A. F. (1980). Antiquity of the vertebrate pattern of activity metabolism and its possible relation to vertebrate origins. Nature, London 286, 886–8.CrossRefGoogle ScholarPubMed
RyboŠ, M., LeŠtan, P. & DubinskÝ, P. (1974). Study of the excretory products of Ascaridia galli. Biologica Bratislava B29, 129–32.Google Scholar
Saz, H. J. & Lescure, O. L. (1966). Interrelationships between the carbohydrate and lipid metabolism of Ascaris lumbricoides egg and adult stages. Comparative Biochemistry and Physiology 18, 845–57.CrossRefGoogle ScholarPubMed
Schöttler, U. & Schroff, G. (1976). Untersuchungen zum anaeroben Glykogenabbau bei Tubifex tubifex M. Journal of Comparative Physiology, B 108, 243–54.CrossRefGoogle Scholar
Visser, N., Opperdoes, F. R. & Borst, P. (1981). Subcellular compartmentation of glycolytic intermediates in Trypanosoma brucei. European Journal of Biochemistry 118, 521–6.CrossRefGoogle ScholarPubMed
Ward, P. F. V. (1982). Aspects of helminth metabolism. Paraaitology 84, 177–94.CrossRefGoogle ScholarPubMed
Ward, P. F. V. & Huskisson, N. S. (1978). The energy metabolism of adult Haemonchus contortus, in vitro. Parasitology 77, 255–71.CrossRefGoogle ScholarPubMed
Warren, L. G., Lushbaugh, W. B. & Roy, M. J. (1970). Energy metabolism of Ancylostoma caninum. Journal of Parasitology 56, 360–1. (Suppl.)Google Scholar
Yancey, P. H., Clark, M. E., Hand, S. C., Bowlus, R. D. & Somero, G. N. (1982). Living with water stress: evolution of osmolyte systems. Science 217, 1214–22.CrossRefGoogle ScholarPubMed
Zurburg, W. & De Zwaan, A. (1981). The role of amino acids in anaerobiosis and osmoregulation in bivalves. Journal of Experimental Zoology 215, 315–25.CrossRefGoogle Scholar