Oral microbiome is related to lepidopteran herbivore performance by lignin degradation

Microorganisms associated with insects play crucial roles in mediating the host plant adaptation of their insect hosts. Although oral microbiota are the primary interface with ingested plant material, we still poorly understand their diversity, their function, and their ecological relationship with insect performance. Here, we investigated the diversity and function of the oral microbiota in two generalist lepidopteran pests (Spodoptera litura and Spodoptera frugiperda) feeding across three host plants (bok choy, peanut, and maize). Plant species significantly influenced the diversity and composition of oral microbiota in both S. litura and S. frugiperda. Oral microbial communities from insects feeding on bok choy exhibited significantly higher Sobs richness and Shannon diversity compared to those with peanut or maize plants. Community-level analysis revealed overlapping enriched oral taxa-including Brevibacterium, Staphylococcus, Microbacterium, Allorhizobium-Neorhizobium-Pararhizobium-Rhizobium, Brachybacterium, and Rhodococcus-that were enriched in both insect species when consuming bok choy. In contrast, they accumulated distinct bacterial taxa emerged when feeding on peanut and maize. Microbial ligninolysis capacity within the oral microbiota showed positive associations with leaf lignin content and herbivore performance. This functional trait primarily associated with Brevibacterium and Rhodococcus taxa. Accordingly, two isolated strains, Brevibacterium sedimins OS20 and Rhodococcus sp. OS5 demonstrated effective lignin degradation capacity, achieving 41.01% and 17.62% lignin loss in litter, respectively, after 60 days in microcosm experiments. Overall, host plants shape the diversity and composition of insect oral microbiota. Crucially, microbial ligninolysis capacity and leaf lignin content positively correlated with herbivore performance. This study provides novel insights into the function of oral microbiota in plant-insect interactions, potentially informing the complex multitrophic relationships underlying coevolutionary dynamics.