Proteus vulgaris strain Ld01-originated mandelonitrile defends Leptinotarsa decemlineata larvae and adults against predation

Abstract Leptinotarsa decemlineata larvae and adults have evolved to apply aposematic signals to display their toxicity to natural enemies. Nevertheless, the chemical components of the volatile repellant remain to be identified. Here we show that the larvae and adults actively release hypertoxic hydrogen cyanide (HCN) from the degradation of nitriles, in contrast to the pupae. A bacterial symbiont Proteus vulgaris Ld01 is responsible for the production of a cyanoglucoside, amygdalin. The bacterium mainly lives in beetle guts and proliferates rapidly during ecdysis. Removal of larval bacteria significantly reduces HCN emission in the larvae and adults. Re-infection with the symbiont in or addition of mandelonitrile to the bacteria-deprived beetles restores the emission. Deprivation of bacteria decreases the defense of the larvae and adults against chick predation, which can be mitigated by re-colonization of P. vulgaris Ld01 or introduction of mandelonitrile. Together, these findings highlight the roles of intestinal P. vulgaris Ld01 in the production of an aromatic cyanoglucoside amygdalin in its host L. decemlineata. Degradation of amygdalin liberates an aposematic compound mandelonitrile to the hemolymph. Mandelonitrile and its metabolites are accumulated near the cuticle, where they are converted to HCN to defend the beetles against predation.