Larval taste perception to fucose and its implications via an altered gut microbiota in the fall armyworm Spodoptera frugiperda

BACKGROUND: Chemosensory detection of sugars is crucial to the feeding and oviposition of herbivorous insects. The fall armyworm Spodoptera frugiperda is an invasive polyphagous insect in China, but its molecular and regulatory basis of sugar perception remains elusive. In this study, we investigated the molecular mechanism for sugar sensation in this species. RESULTS: The phylogenetic analysis found that sugar gustatory receptors (GRs) formed species-specific branches, and Group II sugar GRs are highly conserved, with the highest identity between SfruGR6 and HarmGR6. The oocyte expressing SfruGR6 responded to fucose and sucrose by using the Xenopus oocyte expression system. The larval sensilla styloconica have fucose-sensitive gustatory receptor neurons (GRNs), and the neural firing rates from medial sensilla styloconica towards fucose were higher than that in lateral sensilla styloconica. Fucose acts as a feeding stimulant, while sustained feeding of fucose caused the reduction of larval weight and the survival rate of female adults, but had no effect on the pupa weight and period. Ingestion of fucose alters the composition and abundance of gut microbiota in larvae, resulting in the abundance increase of Exceevirus Xc38, Escherichia coli, Klebsiella pneumoniae, and the decrease of Enterococcus casseliflavus, Microbacterium sp. Be9, Enterococcus faecium, and Enterococcus mundtii. CONCLUSION: These findings reveal that SfruGR6 is a sugar GR tuned to fucose and sucrose, and ingestion of fucose negatively affects growth and survival by regulating gut microbiota in S. frugiperda. This work not only enriches the knowledge of co-evolution between insects and plants, but also provides new insights into pest control strategies. © 2025 Society of Chemical Industry.