Dismissing-then-recruiting: a unique mechanism for symbiont recruitment and lignocellulose degradation in gut of black soldier fly larvae

BACKGROUND: Black soldier fly larvae (Hermetia illucens L., BSFL) efficiently degrade lignocellulosic waste despite lacking endogenous lignocellulolytic enzymes, indicating a critical dependence on gut-associated microbiota. However, how BSFL are associated with the enrichment and spatial organization of lignocellulose-degrading symbionts within the gut remains poorly understood. RESULTS: We show that BSFL establish a spatially structured microbiome through gut compartment-specific immune regulation. Axenic larvae showed negligible lignocellulose degradation, whereas microbiota-associated larvae achieved ~ 33.3%, confirming microbial dependence. Antimicrobial peptides, including cecropin and defensin, were highly expressed in the anterior midgut, forming a selective barrier. In contrast, the posterior midgut showed reduced immune activity via peptidoglycan recognition proteins (PGRP-LB, PGRP-SC). Concurrently, host glycosylation-related genes (C1galt1, GlcAT-P, FUT8/11) were significantly upregulated in the posterior midgut (17-19 TPM), representing a 4-fivefold increase relative to the anterior region (p < 0.01). This region was correspondingly enriched in carbohydrate-active symbionts producing glycoside hydrolases, including galactosidases, fucosidases, and mannosidases, suggesting that upregulated glycan biosynthesis may provide sustained nutrient availability for microbial taxa with corresponding carbohydrate-utilizing capacities. Such compartmentalized immune-metabolic coordination is consistent with a potentially conserved strategy for modulating immune tolerance and fostering symbiont recruitment. CONCLUSIONS: Collectively, our findings define a compartmentalized "Dismissing-then-Recruiting" strategy for microbiome assembly in BSFL, which is associated with the structuring of functional symbiont communities for efficient lignocellulose bioconversion, thereby elucidating novel principles for sustainable waste management. Video Abstract.