Halide peroxidase in tissues that interact with bacteria in the host squidEuprymna scolopes

An enzyme with similarities to myeloperoxidase, the antimicrobial halide pe roxidase in mammalian neutrophils, occurs abundantly in the light organ tis sue of Euprymna scolopes, a squid that maintains a beneficial association w ith the luminous bacterium Vibrio fischeri. Using three independent assays typically applied to the analysis of halide peroxidase enzymes, we directly compared the activity of the squid enzyme with that of human myeloperoxida se. One of these methods, the diethanolamine assay, confirmed that the squi d peroxidase requires halide ions for its activity. The identification of a halide peroxidase in a cooperative bacterial association suggested that th is type of enzyme can function not only to control pathogens, but also to m odulate the interactions of host animals with their beneficial partners. To determine whether the squid peroxidase functions under both circumstances, we examined its distribution in a variety of host tissues, including those that typically interact with bacteria and those that do not. Tissues inter acting with bacteria included those that have specific cooperative associat ions with bacteria (i.e., the light organ and accessory nidamental gland) a nd those that have transient nonspecific interactions with bacteria (i.e., the gills, which clear the cephalopod circulatory system of invading microo rganisms). These bacteria-associated tissues were compared with the eye, di gestive gland, white body, and ink-producing tissues, which do not typicall y interact directly with bacteria. Peroxidase enzyme assays, immunocytochem ical localization, and DNA-RNA hybridizations showed that the halide-depend ent peroxidase is consistently expressed in high concentration in tissues t hat interact bacteria. Elevated levels of the peroxidase were also found in the ink-producing tissues, which are known to have enzymatic pathways asso ciated with antimicrobial activity. Taken together, these data suggest that the host uses a common biochemical response to the variety of types of ass ociations that it forms with microorganisms. J. Cell Biochem. 72:445-457, 1 999. (C) 1999 Wiley-Liss, Inc.