Hostname: page-component-77c89778f8-cnmwb Total loading time: 0 Render date: 2024-07-16T23:17:18.988Z Has data issue: false hasContentIssue false

The transition from an aerobic to an anaerobic energy metabolism in transforming Schistosoma mansoni cercariae occurs exclusively in the head

Published online by Cambridge University Press:  06 April 2009

A. M. C. Horemans
Affiliation:
Laboratory of Veterinary Biochemistry, Utrecht University, P.O. Box 80176, 3508 TD Utrecht, The Netherlands
A. G. M. Tielens
Affiliation:
Laboratory of Veterinary Biochemistry, Utrecht University, P.O. Box 80176, 3508 TD Utrecht, The Netherlands
S. G. Van Den Bergh
Affiliation:
Laboratory of Veterinary Biochemistry, Utrecht University, P.O. Box 80176, 3508 TD Utrecht, The Netherlands

Summary

It has been shown that in intact cercariae of Schistosoma mansoni in water, both head and tail had an identical, aerobic energy metabolism. As long as the environment was water, glucose was mainly degraded to carbon dioxide by both head and tail whether or not these two were still connected to each other. Transfer of intact cercariae into a simple salt medium supplemented with glucose resulted in a very rapid transition towards a more anaerobic energy metabolism: the production of lactate and pyruvate increased, whereas the production of carbon dioxide remained more or less constant. A concomitant rise in temperature to 37°C was not essential for this biochemical transition, but made it more pronounced. Experiments on isolated cercarial bodies and tails in a transforming medium demonstrated that the tails oxidized glucose to carbon dioxide, whereas bodies produced mainly pyruvate and lactate. The results showed that the metabolic transition towards a more anaerobic energy metabolism occurred only in the head and not in the tail of the cercariae. Loss of the tail was shown not to be a pre-requisite for this transition, nor did it by itself trigger a metabolic switch in the resulting cercarial body.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

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

Bruce, J. I., Ruff, M. D. & Hasegawa, H. (1971). Schistosoma mansoni: endogenous and exogenous glucose and respiration of cercariae. Experimental Parasitology 29, 8693.CrossRefGoogle ScholarPubMed
Bruce, J. I., Weiss, E., Stirewalt, M. A. & Lincicome, D. R. (1969) Schistosoma mansoni: glycogen content and utilization of glucose, pyruvate, glutamate, and citric acid cycle intermediates by cercariae and schistosomules. Experimental Parasitology 26, 2940.CrossRefGoogle ScholarPubMed
Coles, G. C. (1972). Carbohydrate metabolism of larval Schistosoma mansoni. International Journal for Parasitology 2, 341–52.CrossRefGoogle ScholarPubMed
Coles, G. C. (1984). Recent advances in schistosome biochemistry. Parasitology 89, 603–37.CrossRefGoogle ScholarPubMed
Colley, D. G. & Wikel, S. K. (1974). Schistosoma mansoni: simplified method for the production of schistosomules. Experimental Parasitology 35, 4451.CrossRefGoogle ScholarPubMed
Cousin, C. E., Stirewalt, M. A., Dorsey, C. H. & Watson, L. P. (1986 a). Schistosoma mansoni: comparative development of schistosomules produced by artificial techniques. Journal of Parasitology 72, 606–9.CrossRefGoogle ScholarPubMed
Cousin, C. E., Stirewalt, M. A. & Dorsey, C. H. (1986 b). Schistosoma mansoni: transformation of cercariae to schistosomules in ELAC, saline and phosphate-buffered saline. Journal of Parasitology 72, 609–11.CrossRefGoogle ScholarPubMed
Eveland, L. K. & Morse, S. I. (1975). Schistosoma mansoni: in vitro conversion of cercariae to schistosomula. Parasitology 71, 327–35.CrossRefGoogle ScholarPubMed
Hockley, D. J. & McLaren, D. J. (1973). Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. International Journal for Parasitology 3, 1325.CrossRefGoogle ScholarPubMed
Lazdins, J. K., Stein, M. J., David, J. R. & Sher, A. (1982). Schistosoma mansoni: rapid isolation and purification of schistosomula of different developmental stages by centrifugation on discontinuous density gradients of Percoll. Experimental Parasitology 53, 3944.CrossRefGoogle ScholarPubMed
Pande, S. V. (1976). Liquid scintillation counting of aqueous samples using Triton-containing scintillants. Analytical Biochemistry 74, 2534.CrossRefGoogle ScholarPubMed
Salafsky, B., Fuscu, A. C., Whitley, K., Nowicki, D. & Ellenberger, B. (1988). Schistosoma mansoni: analysis of cercarial transformation methods. Experimental Parasitology 67, 116–27.CrossRefGoogle ScholarPubMed
Samuelson, J. C. & Stein, L. D. (1989). Schistosoma mansoni: increasing saline concentration signals cercariae to transform to schistosomula. Experimental Parasitology 69, 23–9.CrossRefGoogle Scholar
Stirewalt, M. A. (1974). Schistosoma mansoni: cercaria to schistosomule. Advances in Parasitology 12, 115–82.CrossRefGoogle ScholarPubMed
Thompson, D. P., Morrison, D. D., Pax, R. A. & Bennett, J. L. (1984). Changes in glucose metabolism and cyanide sensitivity in Schistosoma mansoni during development. Molecular and Biochemical Parasitology 13, 3951.CrossRefGoogle ScholarPubMed
Tielens, A. G. M. & Van Den Bergh, S. G. (1987). Glycogen metabolism in Schistosoma mansoni worms after their isolation from the host. Molecular and Biochemical Parasitology 24, 247–54.CrossRefGoogle ScholarPubMed
Tielens, A. G. M., Van Den Heuvel, J. M. & Van Den Bergh, S. G. (1990 a). Substrate cycling between glucose 6-phosphate and glycogen occurs in Schistosoma mansoni. Molecular and Biochemical Parasitology 39, 109–16.CrossRefGoogle ScholarPubMed
Tielens, A. G. M., Van Den Heuvel, J. M. & Van Den Bergh, S. G. (1990 b). Continuous synthesis of glycogen by individual worm pairs of Schistosoma mansoni inside the veins of the final host. Molecular and Biochemical Parasitology 39, 195202.CrossRefGoogle ScholarPubMed
Tielens, A. G. M., Van Der Meer, P. & Van Den Bergh, S. G. (1981). The aerobic energy metabolism of the juvenile Fasciola hepatica. Molecular and Biochemical Parasitology 3, 205–14.CrossRefGoogle ScholarPubMed
Van Oordt, B. E. P., Tielens, A. G. M. & Van Den Bergh, S. G. (1989). Aerobic to anaerobic transition in the carbohydrate metabolism of Schistosoma mansoni cercariae during transformation in vitro. Parasitology 98, 409–15.CrossRefGoogle ScholarPubMed
Von Kruger, W. M. A., Gazzinelli, G., Figueiredo, E. A. & Pellegrino, J. (1978). Oxygen uptake and lactate production by Schistosoma mansoni cercaria, cercarial body and tail, and schistosomule. Comparative Biochemistry and Physiology 60B, 41–6.Google ScholarPubMed
Wiest, P. M., Kossmann, R. J. & Tartakoff, A. M. (1989). Determinants of surface membrane maturation during the cercarial-schistosomula transformation of Schistosoma mansoni. American Journal of Tropical and Medical Hygiene 41, 70–7.CrossRefGoogle ScholarPubMed