Uninheritable but widespread bacterial symbiont mediates insecticide detoxification of an agricultural invasive pest Spodoptera frugiperda

Abstract

Identifying insecticide resistance-related insect bacterial symbiont is a vital compass for promoting symbiont-based insecticide resistance management and insecticide-free insect pest control. Known insecticide-resistance-related symbionts lack universality and genetic manipulation, as either not widespread or unculturable. Here, we discovered a widespread symbiont Enterococcus casseliflavus of a significant invasive insect pest, Spodoptera frugiperda. This symbiont enhances host insecticide resistance to chlorantraniliprole by amide bond breaking and dehalogenation-related insecticide degradation, suggesting its great potential for Lepidoptera pest insecticide resistance management. Complying with the increase in exposure risk of chlorantraniliprole, the E. casseliflavus of insects symbionts rather than mammals or environmental strains were notably enriched with putative chlorantraniliprole degradation genes. We also found that E. casseliflavus can transmit horizontally with high efficiency (100%) through cross-diet and cannibalism rather than vertical transmission from mother insect to offspring. Moreover, the widespread infection of E. casseliflavus in the field populations not only implies that an underlying symbiont-host co-evolution process driven by insecticide pressure might be underway, but also provides a novel therapeutic target of agricultural pests based on symbiont-targeted insect control (STIC).