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RESEARCH PRODUCT
Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism
Silvia GigliottiPaola VarricchioGianluca TettamantiFrancesco PennacchioIlaria Di LelioMorena CasartelliBarbara GiordanaSilvia CacciaNúria BanyulsDanilo ErcoliniAdriana MarinelliAntonietta La StoriaJuan FerréEleonora Franzettisubject
Crops Agricultural0301 basic medicineHemocytesSerratiaBacillus thuringiensisSpodopteraSerratiaMicrobiologyHemolysin Proteins03 medical and health sciencesBacterial ProteinsInsect-pathogen interactionImmunityBacillus thuringiensisAnimalsPest Control Biologicalbioinsecticide | insect-pathogen interactions | insect biocontrol | pore-forming toxins | immunitySpodoptera littoralisRNA Double-StrandedClostridiumImmunosuppression TherapyPore-forming toxinMultidisciplinaryBacillus thuringiensis ToxinsInsect biocontrolbiologyHost (biology)MicrobiotafungiImmunityMidgutBiological Sciencesbiology.organism_classificationImmunity InnateBioinsecticideEndotoxinsIntestines030104 developmental biologyGene Expression RegulationLarvaPore-forming toxinInsect ProteinsRNA InterferenceImmunocompetencedescription
Bacillus thuringiensis is a widely used bacterial entomopathogen producing insecticidal toxins, some of which are expressed in insect-resistant transgenic crops. Surprisingly, the killing mechanism of B. thuringiensis remains controversial. In particular, the importance of the septicemia induced by the host midgut microbiota is still debated as a result of the lack of experimental evidence obtained without drastic manipulation of the midgut and its content. Here this key issue is addressed by RNAi-mediated silencing of an immune gene in a lepidopteran host Spodoptera littoralis, leaving the midgut microbiota unaltered. The resulting cellular immunosuppression was characterized by a reduced nodulation response, which was associated with a significant enhancement of host larvae mortality triggered by B. thuringiensis and a Cry toxin. This was determined by an uncontrolled proliferation of midgut bacteria, after entering the body cavity through toxin-induced epithelial lesions. Consequently, the hemolymphatic microbiota dramatically changed upon treatment with Cry1Ca toxin, showing a remarkable predominance of Serratia and Clostridium species, which switched from asymptomatic gut symbionts to hemocoelic pathogens. These experimental results demonstrate the important contribution of host enteric flora in B. thuringiensis-killing activity and provide a sound foundation for developing new insect control strategies aimed at enhancing the impact of biocontrol agents by reducing the immunocompetence of the host.
year | journal | country | edition | language |
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2016-01-01 | Proceedings of the National Academy of Sciences |