Multi-omics Reveals Uninheritable but Widespread Bacterial Symbiont Mediates Insecticide Detoxification of a New Agricultural Invasive Pest

Abstract

Abstract Background Host-symbiont co-evolution determines the fitness of holobiont under toxic stress and compensates for enhanced insecticide resistance well noted in many insects. However, the ecological causes and consequences of the symbionts involved in the global invasive success of agricultural pests remain unknown. Results Here, we discovered a widespread symbiont Enterococcus casseliflavus EMBL-3 of a significant invasive insect pest, Spodoptera frugiperda. Using multi-omics analysis, we indicated that EMBL-3 enhances host insecticide resistance to chlorantraniliprole by amide bond breaking and dehalogenation-related insecticide degradation. Complying with the increase in exposure risk of chlorantraniliprole, the E. casseliflavus isolates of insects’ symbionts but not those from mammals or environmental strains were notably enriched with putative chlorantraniliprole degradation genes. EMBL-3 widely infected (100%) field populations and can transmit horizontally with high efficiency through cross-diet and cannibalism. Conclusion This study revealed that EMBL-3 was an uninheritable but widespread symbiont in S. frugiperda that involved in host resistance by insecticide degradation. The results 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) for global crop protection.