Role of the tegument and gut in nutrient uptake by parasitic platyhelminths

Abstract

The ease of procuring nutrient is probably the main selection pressure that drives and maintains the host–parasite relationship. The feeding activities of the ectoparasitic monogeneans exhibit similarities with the predatory turbellarians, with certain monopisthocotylean members feeding by means of a protrusible pharynx. These parasites degrade fish skin by secreting enzymes extracorporeally, but most of the digestion is carried out intracellularly in cells lining a well-differentiated gut. Some polyopisthocotylean monogeneans, however, living within the vascularized gill chamber, took advantage of the availability of a more highly nutritious, consistent, and renewable diet in the form of blood, and this represented a major step in the evolution of endoparasitism. Blood provides a rich source of carbohydrates for the production of energy and amino acids and fatty acids for the synthesis of parasite molecules and for egg production. The external surfaces of all parasitic flatworms depart from turbellarian character and are composed of a multifunctional syncytial tegument that is permeable to a variety of small organic solutes. Glucose and amino acid transporter molecules situated in the tegumental surface and basal membranes of trematodes and cestodes function in the uptake of these molecules and their distribution to the parasite tissues. Cestodes are bereft of any vestige of a gut, but their tegument has become elaborated into a highly efficient digestive–absorptive layer that competes with the vertebrate mucosa for nutrients. The patterns of energy metabolism in adult flatworm parasites are generally anaerobic and based on glycogen, with abbreviated metabolic pathways and the loss of biosynthetic capacities. In contrast to the tegument, the role of the gut is to digest host macromolecules and subsequently absorb the soluble products. However, the switch to blood as the major source of nutrient necessitated development of a means of overcoming the problems of blood clotting, attack by immune effector mechanisms, and the intracellular accumulations of haematin pigment. Digenean trematode, in contrast to monogeneans, digest blood extracellularly and their secretions include molecules capable of lysing erythrocytes and preventing blood clotting. Digestion of the ingested proteins is generally rapid, involving a range of cathepsin-like cysteine and aspartic proteases, which reduce the blood meal to absorbable peptides that are most likely further catabolized to amino acids by intracellular aminopeptidases. The parasites dispose of accumulated haematin by simply emptying the contents of their blind-ended gut.