Root inoculation with soil-borne microorganisms alters gut bacterial communities and performance of the leaf-chewer Spodoptera exigua

Soil-borne microorganisms can impact leaf-chewing insect fitness by modifying plant nutrition and defence. Whether the altered insect performance is linked to changes in microbial partners of caterpillars remains unclear. We investigated the effects of root inoculation with soil bacteria or fungi on the gut bacterial community and biomass of the folivore Spodoptera exigua. We also explored the potential correlation between both parameters. We performed herbivory bioassay using leaves of tomato plants (Solanum lycopersicum), measured caterpillar weight gain and characterized the gut bacterial communities via 16S rRNA gene metabarcoding. All soil microbes modified the gut bacterial communities, but the extent of these changes depended on the inoculated species. Rhizophagus irregularis and Bacillus amyloliquefaciens had opposite effects on S. exigua weight. While plant inoculation with the fungus influenced gut bacterial diversity, B. amyloliquefaciens also affected the community composition. A reduced abundance of two S. exigua enterococcal symbionts correlated with decreased insect biomass. Our results show that soil microorganisms can induce plant-mediated changes in the gut bacterial community of foliar-feeding caterpillars. We propose that the impact of these alterations on insect performance might rely on specific adaptations within the gut bacteria, rather than solely on the occurrence of changes.