Vibrio fischeri lipopolysaccharide induces developmental apoptosis, but not complete morphogenesis, of the Euprymna scolopes symbiotic light organ

During initiation of the association between the squid host Euprymna scolop es and its bacterial partner Vibrio fischeri, the bacteria induce dramatic morphogenesis of the host symbiotic organ, a portion of which involves the signaling of widespread apoptosis of the cells in a superficial ciliated ep ithelium on the colonized organ. In this study, we investigated the role in this process of lipopolysaccharide (LPS), a bacterial cell-surface molecul e implicated in the induction of animal cell apoptosis in other systems. Pu rified V. fischeri LPS, as well as the LPS of V. cholerae, Haemophilus infl uenzae, Escherichia coli, and Shigella flexneri, added in the concentration range of pg/ml to ng/ml, induced apoptosis in epithelial cells 10- to 100- fold above background levels. The absence of species specificity suggested that the conserved lipid A portion of the LPS was the responsible component of the LPS molecule. Lipid A from V. fischeri, E. coli, or S. flexneri ind uced apoptosis. In addition, strains of H. influenzae carrying a mutation i n the htrB gene, which is involved in the synthesis of virulent lipid A, sh owed a diminished ability to induce apoptosis of host cells. Confocal micro scopy using fluorescently labeled LPS indicated that the LPS behaves simila r to intact bacterial symbionts, interacting with host cells in the interna l crypt spaces and not directly with the superficial epithelium. Although L PS was able to induce apoptosis, it did not induce the full morphogenesis o f the ciliated surface, suggesting that multiple signals are necessary to m ediate the development of this animal-bacterial mutualism. (C) 2000 Academi c Press.