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

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.

C-type lectin-mediated microbial homeostasis is critical for Helicoverpa armigera larval growth and development

“…For example, Enterococcus faecalis in Manduca sexta completes its commensal-to-pathogen switch after migration of bacteria from the gut to the hemocoel [ 20 ]. Plant-mediated translocation of bacteria from the gut to the hemolymph reduces larval growth and elevates mortality of the fall armyworm [ 19 ]. E .…”

“…For example, Enterococcus faecalis in Manduca sexta completes its commensal-to-pathogen switch after migration of bacteria from the gut to the hemocoel [20]. Plant-mediated translocation of bacteria from the gut to the hemolymph reduces larval growth and elevates mortality of the fall armyworm [19]. E. mundtii has demonstrated previously to be a pathogenic agent for the flacherie disease of the silkworm larvae, with symptoms involving retarded growth, flaccidity, and cessation of feeding [60].…”

“…The insect host bacterial community in the hemolymph may be influenced by the diet [ 18 ]. When a fall armyworm feeds on resistant maize, its gut microbes penetrate the intestinal barriers and invade the body cavity [ 19 ]. Some hemolymph bacteria are translocated from the gut through Bacillus thuringiensis toxin-induced epithelial lesions, changing the roles from resident symbionts in the gut to pathogens in the hemolymph [ 20 – 22 ].…”

Maize Endochitinase Expression in Response to Fall Armyworm Herbivory

“…The PM is a semipermeable lining in the intestine of many invertebrates that is primarily composed of chitin and glycoproteins (Hegedus et al 2009). PMs are normally produced during feeding and physically protect the midgut epithelium against food abrasion, digestive enzymes, toxins, and microorganisms (Hegedus et al 2009;Lehane 1997;Mason et al 2019). Since the insect PM is continuously exposed to ingested plant materials, compounds having the potential to damage PM would impair normal digestive processes and biological functions (Hegedus et al 2009; Zhu-Salzman et al 2008).…”

Host Species Determines the Composition of the Prokaryotic Microbiota in Phlebotomus Sandflies

“…In this context, a symbiotic Citrobacter carrying an organophosphate hydrolase conferred resistance in Bactocera dorsalis to organophosphate insecticides [ 19 ]. Conversely, insect symbiotic bacteria could be detrimental to their hosts by conferring pathogenesis (i.e., Spiroplasma and honeybees) [ 20 ] or by interacting with plant defense systems exacerbating their effect on insect pests [ 21 ].…”