Antibacterial proteins in the midgut of Manduca sexta during metamorphosis

Abstract

Efforts to characterize insect antibacterial mechanisms have focused on defenses deployed via the hemolymph to eliminate bacteria in the body cavity. Little attention has been directed to defensive mechanisms targeted to the cuticular surfaces of the insect, or the alimentary canal, which are the primary sources of bacterial infection. While studying the synthesis of hemolymph antibacterial proteins in tobacco hornworm larvae, we discovered two antibacterial responses targeted to the midgut lumen: a “malaise syndrome” elicited concurrently with the synthesis of hemolymph antibacterial proteins following hemocoelic infection and a prophylactic mechanism apparently regulated by the endocrine signals that initiate metamorphosis. During metamorphosis, the lepidopteran midgut is restructured and the peritrophic membrane is lost, exposing the midgut epithelium to the natural bacterial flora of the gut lumen. During this period, differentiating pupal midgut epithelial cells synthesize and release into the lumen a cocktail of potent antibacterial proteins including lysozyme, bactericidal activity against Escherichia coli, hemolin, and phenoloxidase. Progress in the characterization of these proteins is reviewed and a potential similarity of the metamorphosis-associated, prophylactic response to the “malaise syndrome” is discussed.