Plant defenses interact with insect enteric bacteria by initiating a leaky gut syndrome

Significance

Many plant defenses that deter insect herbivory target the attacker’s digestive system. We found that plant defenses against the fall armyworm created opportunities for resident gut microbes to penetrate protective gut barriers, invading the body cavity and exacerbating the negative impacts of plant defenses on the insect. These interactions triggered insect immune responses and collectively overwhelmed the insect’s ability to cope with multiple stressors. However, the effects varied between bacterial taxa, indicating that variation in the caterpillar microbiome can alter their phenotype. Our results reveal a previously unrecognized, and likely widespread, mechanism allowing the plant to use the insect’s gut microbiota against it in collaboration with the plant’s own defenses.

Abstract

Plants produce suites of defenses that can collectively deter and reduce herbivory. Many defenses target the insect digestive system, with some altering the protective peritrophic matrix (PM) and causing increased permeability. The PM is responsible for multiple digestive functions, including reducing infections from potential pathogenic microbes. In our study, we developed axenic and gnotobiotic methods for fall armyworm ( Spodoptera frugiperda) and tested how particular members present in the gut community influence interactions with plant defenses that can alter PM permeability. We observed interactions between gut bacteria with plant resistance. Axenic insects grew more but displayed lower immune-based responses compared with those possessing Enterococcus, Klebsiella, and Enterobacter isolates from field-collected larvae. While gut bacteria reduced performance of larvae fed on plants, none of the isolates produced mortality when injected directly into the hemocoel. Our results strongly suggest that plant physical and chemical defenses not only act directly upon the insect, but also have some interplay with the herbivore’s microbiome. Combined direct and indirect, microbe-mediated assaults by maize defenses on the fall armyworm on the insect digestive and immune system reduced growth and elevated mortality in these insects. These results imply that plant–insect interactions should be considered in the context of potential mediation by the insect gut microbiome.