Inflammatory Effects of Edwardsiella ictaluri Lipopolysaccharide Modifications in Catfish Gut

Abstract

ABSTRACTBacterial lipopolysaccharides (LPS) are structural components of the outer membranes of Gram-negative bacteria and also are potent inducers of inflammation in mammals. Higher vertebrates are extremely sensitive to LPS, but lower vertebrates, like fish, are resistant to their systemic toxic effects. However, the effects of LPS on the fish intestinal mucosa remain unknown.Edwardsiella ictaluriis a primitive member of theEnterobacteriaceaefamily that causes enteric septicemia in channel catfish (Ictalurus punctatus).E. ictaluriinfects and colonizes deep lymphoid tissues upon oral or immersion infection. Both gut and olfactory organs are the primary sites of invasion. At the systemic level,E. ictaluripathogenesis is relatively well characterized, but our knowledge aboutE. ictaluriintestinal interaction is limited. Recently, we observed thatE. ictalurioligo-polysaccharide (O-PS) LPS mutants have differential effects on the intestinal epithelia of orally inoculated catfish. Here we evaluate the effects ofE. ictaluriO-PS LPS mutants by using a novel catfish intestinal loop model and compare it to the rabbit ileal loop model inoculated withSalmonella entericaserovar Typhimurium LPS. We found evident differences in rabbit ileal loop and catfish ileal loop responses toE. ictaluriandS. Typhimurium LPS. We determined that catfish respond toE. ictaluriLPS but not toS. Typhimurium LPS. We also determined thatE. ictaluriinhibits cytokine production and induces disruption of the intestinal fish epithelia in an O-PS-dependent fashion. TheE. ictaluriwild type and ΔwibTLPS mutant caused intestinal tissue damage and inhibited proinflammatory cytokine synthesis, in contrast toE. ictaluriΔgneand ΔugdLPS mutants. We concluded that theE. ictaluriO-PS subunits play a major role during pathogenesis, since they influence the recognition of the LPS by the intestinal mucosal immune system of the catfish. The LPS structure ofE. ictalurimutants is needed to understand the mechanism of interaction.