Altered Carbohydrate Levels and Gluconeogenic Enzyme Activity in Trichoplusia ni Parasitized by the Insect Parasite, Hyposoter exiguae

Abstract

The association of the insect parasite, Hyposoter exiguae, with its host, Trichoplusia ni, was characterized by increased host hemolymph sugar and fat body glycogen levels. Elevation of these carbohydrate reserves was accompanied by an increase in the maximal activity of fructose 1,6 bisphosphatase in the fat body. The latter result suggests that an increase in gluconeogenic flux through the fructose 6 phosphate-fructose 1,6 bisphosphate substrate cycle may occur in parasitized insects. Moreover, the maximum rate of cycling may be increased in parasitized tissue as suggested by alteration in the maximal activity of phosphofructokinase. The above effect on fructose 1,6 bisphosphatase could not be explained on the basis of alterations in adenylate nucleotide levels and positive substrate crossover was not observed. The results indicate that the normal metabolic regulation of carbohydrate synthesis may be upset in parasitized individuals. Altered tissue carbohydrate levels are commonly observed during parasitic infections involving invertebrate hosts and metazoan parasites. Although the specific nature of such changes is variable, depletion of carbohydrate reserves is commonly observed. Gordon et al. (1971) reported decreased fat body glycogen levels in Schistocerca gregaria infected by the nematode Mermis nigrescens, and Rutherford and Webster (1978) later observed depressed hemolymph trehalose concentrations. Lowered host blood sugar and glycogen reserves also characterized the associations of the schistosomes, Schistosoma mansoni and S. haematobium with their snail hosts, Biomphalaria alexandrina and Bulinus truncatus, respectively (Ishak et al., 1975). The metabolic basis for glycogen depletion in B. glabrata infected with S. mansoni was recently established by Schwartz and Carter (1982), who demonstrated elevated glycogen phosphorylase activity in infected hosts. In contrast to the above studies, Manohar and Venkateswaro Rao (1976) reported elevated blood sugar in the snail Lymnaea luteola following infection by the trematode, Prosthogonimus sp., and later concluded that gluconeogenesis was responsible (Manohar and Venkateswaro Rao, 1977a, 1977b). Changes in tissue carbohydrate levels also occur during the host associations of hymenopterous insect parasites. Dahlman (1975) reported that hemolymph trehalose concentrations deReceived 6 January 1984; revised 27 February 1984; accepted 27 February 1984. creased in Manduca sexta parasitized by Apanteles congregatus. Trehalose concentrations in Heliothis virescens parasitized by Microplitis croceipes, however, were markedly elevated (Dahlman and Vinson, 1975). Moreover, fat body glycogen levels were increased during the course of infection although total body glycogen decreased (Dahlman and Vinson, 1980). Those authors suggested that fat body glycogen was the source of the elevated hemolymph trehalose. Elevated host hemolymph trehalose and fat body glycogen concentrations were also reported in Trichoplusia ni (Hiibner) (Noctuidae) parasitized by Hyposoter exiguae (Viereck) (Ichneumonidae) (Thompson, 1982); preliminary assay of glycogen phosphorylase activity indicated very low levels in both control and parasitized individuals (Thompson, unpublished observations). Moreover, previous studies on nutritional physiology demonstrated that parasitized hosts have substantially lowered efficiencies of food conversion (Thompson, 1983). It is suggested, therefore, that increased gluconeogenesis may be responsible for the elevated carbohydrate reserves of parasitized Trichoplusia ni. The present investigation was carried out to test that hypothesis by examining the enzymes of the fructose 6 phosphate (F6P)-fructose 1,6 bisphosphate (FBP) substrate cycle. Specifically, the activities of phosphofructokinase (PFKase) and fructose 1,6 bisphosphatase (FBPase), 2 rate-controlling enzymes affecting the net flux through the glycolytic and gluconeogenic pathways, were determined in the fat body of parasitized fourth instar T. ni