Genomic Basis and Immunosuppressive Mechanism of Xenorhabdus nematophila HNS01 Against the Rice Pest Chilo suppressalis

Xenorhabdus nematophila HNS01 engages in mutualistic symbiosis with nematodes of the genus Steinernema. This symbiotic complex exhibits potent insecticidal activity against Chilo suppressalis, a major biotic stress factor in rice production. To elucidate the insecticidal mechanism, we performed whole-genome sequencing and analysis of strain HNS01, and systematically evaluated its immunosuppressive effects on third-instar larvae of C. suppressalis. The genome of X. nematophila HNS01 comprises one chromosome and one plasmid, with a total size of 4,454,952 bp and a G+C content of 43.89%. Bioinformatic analysis revealed 19 secondary metabolite biosynthetic gene clusters, including those responsible for the biosynthesis of putrebactin/avaroferrin, xenematide, odilorhabdins, and xenocoumacin I/Ⅱ, as well as multiple putative protein-encoding genes that constitute the PirAB, Xpt, GroEL, and MCF toxins. Injection of strain HNS01 into third-instar larvae reduced total hemocyte counts to 7% of the initial level by 98 h, suppressed phenoloxidase and secreted phospholipase A₂ activities, and completely inhibited hemolymph melanization. Transcriptomic analysis of moribund larvae indicated that differentially expressed genes were significantly enriched in proteolysis, redox processes, cuticle structure, and fatty acid degradation pathways. Notably, genes encoding antimicrobial peptides (Cecropin, Attacin, Lebocin, and Gloverin) and serine protease inhibitors were upregulated, whereas genes encoding 5-aminoimidazole ribonucleotide carboxylase and carbon–nitrogen hydrolase were downregulated. These findings demonstrate that X. nematophila HNS01 disables host immunity through hemocyte depletion, interference with the eicosanoid pathway, and metabolic disruption, ultimately causing larval death. This study provides genomic and mechanistic insights that support X. nematophila HNS01 as a promising biocontrol agent for managing pest stress caused by C. suppressalis and improving rice stress resistance.