Symbiotic bacteria mediate chemical-insecticide resistance but enhance the efficacy of a biological insecticide in diamondback moth.

Abstract

Insecticide resistance has been a major challenge for pest management worldwide. Here, we investigated how gut symbiotic bacteria in insects might affect resistance to chemical (organophosphate) and biological (Bacillus thuringiensis) insecticides in different ways to create opportunities for strategic pesticide rotations. Using the diamondback moth (Plutella xylostella) as the target pest, we demonstrated that long-term exposure to chlorpyrifos (an organophosphate insecticide) promotes the proliferation of the gut symbiont Enterococcus mundtii in P. xylostella populations, resulting in chlorpyrifos resistance in field populations across China that correlates closely with the abundance of this bacterium. Metabolic analysis revealed that E. mundtii can directly metabolize chlorpyrifos via a conserved cytochrome P450 enzyme in the genus Enterococcus. However, the accumulation of E. mundtii in the gut of chlorpyrifos-resistant populations may increase their susceptibility to Bacillus thuringiensis toxins, resulting in the increased efficacy of Bacillus thuringiensis in populations with high chemical insecticide resistance. The gut barrier disruption caused by Bacillus thuringiensis promotes invasion of E. mundtii from the gut into the hemolymph, leading to death by septicemia to enhance susceptibility. The study highlights an interaction between resistance to chemically synthesized and biological insecticides mediated by gut symbiotic bacteria and suggests a control strategy involving chemical/biological pesticide rotations that may apply to other cases of resistance to chemically synthesized insecticides.