No shot in the dark: Myxozoans chemically detect fresh fish

Abstract

This work reports the discovery of an hitherto unknown chemical recognition trait enabling a parasitic life cycle in aquatic habitats. We believe this is the first record of a natural, host-derived chemical molecule identified as a recognition cue for the phylum Myxozoa. The actinospores of these parasites attach to fish hosts via polar filaments that are extruded upon mechanical stimulation after preceding recognition of a chemical trigger contained in surface mucus. Our goal was to identify this signal. We separated compounds from a purified active fraction derived from trout mucus by a novel HPLC method. By subsequent nuclear magnetic resonance analysis of distinct components and testing in bioassays we elicited stimulation of polar filament discharge and sporoplasm emission in actinospores of three myxozoan spp., Myxobolus cerebralis, Myxobolus pseudodispar and Henneguya nuesslini, by the free nucleosides inosine, 2′-deoxyinosine and guanosine. These nucleosides also activated sporoplasm emission. Nucleosides appear to be appropriate cues for rapid host recognition by the waterborne parasite stages since they are continuously released into surface mucus. The recognition mechanism is not specific for susceptible host species, at least in the myxozoan spp. examined. In addition, a novel function of nucleobase derivatives as semiochemicals was uncovered and a wider impact of this molecule class in parasite recognition systems and aquatic chemical ecology is predicted. The relevance for disease prevention and cell culturing remains to be explored.