Domesticated bacterial origin genes regulate homeostasis of the insect gut microbiome and empower adaptation.

Sap-sucking insects, represented by the globally distributed leafhoppers, have evolved a wide range of adaptive traits and play multiple ecological roles. However, their successful survival strategies in nature remain poorly understood. To explore the adaptive mechanisms of sap-sucking insects, we established a research system using three representative leafhopper species from the same family and found that they have acquired multiple cholesterol-dependent cytolysins (CDCs) derived from gram-positive bacterial genes. Furthermore, we demonstrated that these CDCs have been domesticated and co-evolved with leafhoppers, ultimately participating in various life activities of the host. Specifically, some CDCs exhibit high cytotoxicity, are specifically expressed in the egg serosa, and affect the feeding behaviors of leafhopper predators; others show non-cytotoxic activity, are specifically expressed in the gut, and may regulate leafhopper growth and development by potentially maintaining the homeostasis of the leafhopper gut microbiome. This study uncovers leafhoppers as a paradigm for understanding how organisms can borrow microbial innovations to address ecological challenges and thrive as agricultural pests. It provides a comprehensive perspective to bridge the genotypes of acquired genes with the phenotypes of adaptive traits and demonstrates how homologous genes from donor organisms undergo functional differentiation in recipient hosts, enabling them to exploit new ecological niches. By decoding these mechanisms, we not only gain fundamental insights into evolutionary processes but also develop powerful strategies for sustainable pest management.