Gut microbiome convergence and functional adaptation underlie the evolution of predation in stink bugs (Heteroptera:...

True bugs (Heteroptera) have undergone repeated evolutionary shifts between phytophagous and carnivorous feeding strategies. Although gut microbiomes are recognized for aiding dietary adaptation, their function in mediating these transitions is still unclear, specifically, how microbial communities change during dietary evolution and influence the diversification of feeding traits.

Here, we selected a stink bug lineage of the subfamily Asopinae (Pentatomidae), representative of an independent feeding trait transition from phytophagy to carnivory. Their gut microbiomes were analyzed and compared to those of closely related phytophagous species within the Pentatomidae family, as well as predatory assassin bugs from the Reduviidae family, which represent the ancestral heteropteran feeding trait of predation. It was found that Asopinae lack the gammaproteobacterial symbionts and midgut crypts that are conserved in their phytophagous counterparts. Instead, their gut microbiomes converged on a community dominated by Enterococcus (Firmicutes) and select Proteobacteria (Serratia, Yokenella, Proteus), mirroring the microbiome of assassin bugs. This core community persisted despite prey variation, likely maintained through pentatomid ancestral eggshell-piercing behavior, enabling vertical transmission. Metagenomic analysis linked the Asopinae microbiome to functions potentially associated with predation adaptation, including the digestion of chitinous substrates likely sourced from prey's internal body. Through bacterial isolation, genomics, and functional assays, we demonstrated that Serratia mediates chitin degradation, which along with a potential coordination in diet digestion, may also have been involved in an antifungal effect. Meanwhile, an Enterococcus strain exhibits inhibition to multiple pathogens such that may provide protections to the host, potentially via a class III lanthipeptide.

Our findings reveal a coordinated restructuring of the gut microbiome during dietary shifts. The convergence of Asopinae and Reduviidae microbiomes underscores how microbial communities may have facilitated the ecological adaptation, likely by enabling hosts to exploit new dietary niches and providing defense against bacterial and fungal pathogens. Video Abstract.