Microbiome–Epigenome Interplay Impacts Microbial Symbiosis and Stress Adaptations in the Brown Planthopper (Nilaparvata lugens)

Abstract

The gut microbiota and epigenetic processes both contribute to insect survival and adaptation; however, the relationship between these two systems remains largely unexplored. In this study, we used the brown planthopper (Nilaparvata lugens; BPH) to explore microbiome–epigenome interactions and evaluate its impact on BPH survivability under environmental stress. Disruption of the gut microbiome using antibiotics significantly altered the epigenetic profile of various stress-responsive genes in the BPH. Similarly, perturbations in the epigenome induced by 5-azacytidine resulted in an altered microbiome with diverse metabolic capacities, thus indicating the potential role of epigenetics in maintaining microbial symbiosis in BPH. Further, analysis of gene expression profiles revealed that 5-azacytidine treatment altered the mRNA levels of various genes involved in BPH immunity, suggesting that epigenetic mechanisms regulate and sustain microbial symbionts in insects by modulating their immune system. Altogether, these findings suggest an interplay between the epigenome and microbiome, that influences gene regulation and microbe-mediated regulation of shared metabolic pathways in BPH. Our results highlight new research avenues into the molecular mechanisms of symbiont-enabled herbivory and have implications for future studies on the relationship between gut microbiota and epigenetic mechanisms, the evolution of these processes and their effects on insect–plant interactions in changing environments.