Gut microbiota variation drives differential performance in leaf beetles across host plants.

BACKGROUND: Host plant significantly influences herbivorous insect fitness, while plant-mediated gut microbiota are recognized as a key determinant of insect performance. However, to what extent the differential performance of herbivorous insects on various plants is attributed to plant properties versus plant-mediated gut microbiota remains less clear. RESULTS: Here, we initially observed that the leaf beetle Plagiodera versicolora preferred and exhibited superior performance on Salix babylonica compared with three other host plants. Intriguingly, eliminating larval gut microbiota abolished this preference-performance relationship, resulting in the loss of superior performance on S. babylonica. Further analysis of the larval gut microbiota revealed that Rosenbergiella nectarea was significantly enriched in S. babylonica-fed larvae and positively correlated with larval performance. Reintroduction of R. nectarea, but not two other gut commensal bacteria, restored the superior performance of germ-free (GF) larvae fed S. babylonica. Transcriptomic analysis linked this growth promotion to enhanced nutritional metabolism and developmental signaling. Integrated metabolomic and transcriptomic analyses further identified eight candidate genes underlying the observed effects. Notably, knockdown of either PvABCG1 or PvABCG5 recapitulated the microbiota-depleted phenotype, whereas reintroduction of R. nectarea into GF larvae only fully rescued PvABCG5 knockdown-induced growth retardation. Concurrently, R. nectarea supplementation increased the expression of key 20E synthesis genes (PvSPO, PvPHM, PvSHD), suggesting promotion of larval development may occur via a PvABCG5-mediated cholesterol-to-20E synthesis pathway. CONCLUSIONS: Collectively, our results suggest that host plant-induced differential performance in herbivorous insects largely depends on their gut microbiota, suggesting a crucial role of the gut microbiome in herbivore host preference and the "preference-performance" relationship. Video Abstract.