Persistence of Bacillus thuringiensis spores : Impacts on innate immune response of non-target organisms

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Abstract :

The Gram-positive sporulating bacterium Bacillus thuringiensis (Bt) is a worldwide used biopesticide to fight lepidopteran pests. Upon ingestion of Bt spores, target insects die in 3 days. The increasing environmental dispersion of Bt products raises the question about their potential risks on non-target animals. Indeed, Bt belongs to the phylogenetic group of B.cereus, the third cause of food poisoning in Europe and the second in France. Using Drosophila melanogaster, we have previously demonstrated that Bt vegetative cells are rapidly cleared from the intestine of non-target organisms. This rapid elimination is due to the activation of the local innate immune response in the anterior midgut (Benguettat et al., 2018). However, few studies suggest that Bt spores can persist in human and rodent guts (Oliviera-Filho et al., 2009, Wilcks et al., 2008). To understand why and how Bt/Bc spores persist in the gut of non-target organisms and the the innate immune response to the persistence of spores, we have used two powerful models: Drosophila melanogaster and mice. First, I showed that Bt/Bc spores can persist up to 10 days after acute contamination in the Drosophila gut and at least 48 hours in mouse intestine with severe diarrhea. These findings prompted me to further investigate the possible spore germination in the intestines. For this, I generated an innovative tool consisting in red fluorescent spores which once germinated fluoresce in green to mark vegetative bacteria. Using this tool, I showed that spores did not trigger any immune response in the anterior midgut while accumulating mainly in the posterior midgut where they could germinate. My data suggest that, in the posterior midgut, the innate immune response is inefficient to promptly eliminate germinated bacteria.  Finally, using in vitro culture of  mouse macrophages, I showed that Bt/Bc vegetative cells could activate the NLRP3 inflammasome pathway causing a high level of cells death. On the other side, spores were phagocytosed but did not activate the inflammasome pathway. Altogether, these data will help to understand why and how ingestion of Bt/Bc spores can trigger food poisoning. Moreover, my data suggest that Bt biopesticides could be responsible for unintended effects in non-target organisms.