Stepwise lignocellulose degradation in Apriona swainsoni: the role of gut microbiota.

BACKGROUND: Apriona swainsoni is a wood-boring pest whose larvae feed on recalcitrant plant xylem and occupy diverse niches. Gut microbiota play a vital role in assisting the host to degrade lignocellulose for nutrient acquisition. However, the compartment-specific mechanism of microbial lignocellulose degradation in different intestinal regions remains unclear. RESULTS: Using multi-omics analyses, we identified six cellulase genes three with corresponding protein expression), 21 hemicellulase genes (six with corresponding protein expression), and 40 lignin-degrading enzyme genes (12 with corresponding protein expression) encoded by the larval gut microbiota. PCoA revealed highly significant spatial divergence of lignocellulolytic proteins across discrete gut compartments (P = 0.001). Metabolomic data further validated a sequential, stepwise lignocellulose degradation cascade proceeding from foregut (FG) to midgut (MG), anterior hindgut (AHG), and posterior hindgut (PHG), where lignin undergoes thorough breakdown mainly in the AHG and PHG. Taxonomic annotation confirmed genera including Enterobacter (relative abundance, 2.35E-04), Gibbsiella (1.14E-04), Raoultella (1.00E-04) and Klebsiella (1.09E-05) dominate lignin degradation. Enzymatic assays demonstrated peak activities in Klebsiella oxytoca A3 for lignin peroxidase (3.75 ± 0.25 U/mL), manganese peroxidase (0.85 ± 0.09 U/mL), and neutral xylanase (1.47 ± 0.00 U/mL), while Raoultella terrigena A2 exhibited the maximum laccase activity (0.75 ± 0.06 nmol/min/L). CONCLUSION: This study reveals that larvae of A. swainsoni perform compartmentalized lignocellulose degradation by selectively enriching functional gut symbionts. Efficient lignin depolymerization acts as the core adaptive trait that allows this beetle to occupy unique wood-feeding niches. © 2026 Society of Chemical Industry.