Ingestion of Bacillus cereus spores dampens the immune response to favor bacterial persistence

Salma Hachfi, Alexandra Brun-Barale, Arnaud Fichant, Patrick Munro, Marie-Paule Nawrot-Esposito, Gregory Michel, Raymond Ruimy, Raphaël Rousset, Mathilde Bonis, Laurent Boyer () and Armel Gallet ()
Additional contact information
Salma Hachfi: INRAE, ISA
Alexandra Brun-Barale: INRAE, ISA
Arnaud Fichant: INRAE, ISA
Patrick Munro: C3M
Marie-Paule Nawrot-Esposito: INRAE, ISA
Gregory Michel: C3M
Raymond Ruimy: C3M
Raphaël Rousset: INRAE, ISA
Mathilde Bonis: Université Paris-Est
Laurent Boyer: C3M
Armel Gallet: INRAE, ISA

Nature Communications, 2024, vol. 15, issue 1, 1-19

Abstract: Abstract Strains of the Bacillus cereus (Bc) group are sporulating bacteria commonly associated with foodborne outbreaks. Spores are dormant cells highly resistant to extreme conditions. Nevertheless, the pathological processes associated with the ingestion of either vegetative cells or spores remain poorly understood. Here, we demonstrate that while ingestion of vegetative bacteria leads to their rapid elimination from the intestine of Drosophila melanogaster, a single ingestion of spores leads to the persistence of bacteria for at least 10 days. We show that spores do not germinate in the anterior part of the intestine which bears the innate immune defenses. Consequently, spores reach the posterior intestine where they germinate and activate both the Imd and Toll immune pathways. Unexpectedly, this leads to the induction of amidases, which are negative regulators of the immune response, but not to antimicrobial peptides. Thereby, the local germination of spores in the posterior intestine dampens the immune signaling that in turn fosters the persistence of Bc bacteria. This study provides evidence for how Bc spores hijack the intestinal immune defenses allowing the localized birth of vegetative bacteria responsible for the digestive symptoms associated with foodborne illness outbreaks.

Date: 2024
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DOI: 10.1038/s41467-024-51689-9

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