Symbiont-Induced HSP83 Establishes Two-Tiered Control of Antifungal Immunity in an Invasive Beetle-Fungus Complex

Hosts must distinguish mutualistic symbionts from antagonists while avoiding harmful immune overactivation, yet the mechanisms maintaining this balance remain unclear. This challenge is acute during biological invasions, where exposure to novel microbial communities can outpace host genetic adaptation. Dendroctonus valens (RTB) associates with its mutualistic fungus Leptographium procerum (Lp), forming an invasive beetle-fungus complex during attacks on Chinese pines. Lp fails to trigger antimicrobial peptide expression but induces the heat shock protein 83 (HSP83). The native antagonist Ophiostoma minus (Om) activates immunity through pattern recognition receptors, including PGRP-SA, PGRP-SC2, βGRP3, and βGRP5. HSP83 modulates these responses through two-tiered negative regulation. First, it associates with PGRP-SA, βGRP3, and βGRP5 to attenuate Om detection. Second, it interacts with NF-κB-like factor Dorsal to limit antimicrobial peptide production. This symbiont-induced regulation enables selective defense, supporting RTB survival during combined Lp and Om exposure while limiting excessive Toll-dependent PRR/AMP activation and easing immune-metabolic trade-offs. These findings define a symbiont-assisted, mutation-independent mechanism of host adjustment during biological invasions, in which microbial partners provide immediate immune benefits and influence host success in novel environments.