Comparative phenotypic, genotypic and genomic analyses of Bacillus thuringiensis associated with foodborne outbreaks in France

Abstract

Bacillus thuringiensis (Bt) belongs to the Bacillus cereus (Bc) group, well known as an etiological agent of foodborne outbreaks (FBOs). Bt distinguishes itself from other Bc by its ability to synthesize insecticidal crystals. However, the search for these crystals is not routinely performed in food safety or clinical investigation, and the actual involvement of Bt in the occurrence of FBOs is not known. In the present study, we reveal that Bt was detected in the context of 49 FBOs declared in France between 2007 and 2017. In 19 of these FBOs, Bt was the only microorganism detected, making it the most likely causal agent. Searching for its putative origin of contamination, we noticed that more than 50% of Bt isolates were collected from dishes containing raw vegetables, in particular tomatoes (48%). Moreover, the genomic characterization of isolates showed that most FBO-associated Bt isolates exhibited a quantified genomic proximity to Bt strains, used as biopesticides, especially those from subspecies aizawai and kurstaki. Taken together, these results strengthen the hypothesis of an agricultural origin for the Bt contamination and call for further investigations on Bt pesticides.

Keeping up with the Bacillus cereus group: taxonomy through the genomics era and beyond

“…Additionally, the species name "B. thuringiensis" has been simultaneously used to refer to (i) any B. cereus s.l. isolate capable of producing insecticidal toxins (i.e., Bt toxins) (Bonis et al 2021;Ehling-Schulz, Lereclus, and Koehler 2019;Guinebreti ere et al 2008;Stenfors Arnesen, Fagerlund, and Granum 2008;Zheng et al 2017), or (ii) any isolate within the genomospecies boundary of the B. thuringiensis serovar Berliner str. ATCC 10792 T type strain genome (Baek et al 2019;Parks et al 2020).…”

“…Bt toxin-producing strains are denoted using biovar Thuringiensis, meaning that many commercial bioinsecticidal strains, which belong to panC Group IV, are classified as B. cereus s.s. biovar Thuringiensis within this framework (Supplemental Tables S1-S5). It is important to note that a species label of B. cereus s.s. does not imply that these strains are biosafety level 2 strains, although concerns have been raised about the safety of some commercially available Bt bioinsecticides (Bonis et al 2021;EFSA Panel on Biological Hazards 2016). This subject requires further research to evaluate whether bioinsecticidal strains are ecologically adapted to insect hosts to an extent that the adaptation would result in impaired ability to sporulate and express enterotoxins in the human gastrointestinal tract (Raymond 2017;Raymond and Federici 2017;Raymond et al 2010).…”

“…In addition to anthrax disease and emetic intoxication, B. cereus s.l. isolates can be, and have been, associated with diarrheal illness (Bonis et al 2021;Glasset et al 2016;Granum and Lund 2006;Schoeni and Wong 2005;Stenfors Arnesen, Fagerlund, and Granum 2008). Unlike "B. cereus" emetic intoxication, which results from the consumption of food containing pre-formed cereulide, B. cereus s.l.…”

“…Since 2008, panC has been used to characterize B. cereus s.l. isolates associated with illnesses, infections, and/or outbreaks (Bonis et al 2021;Carroll et al 2019;Glasset et al 2018;Glasset et al 2016;Johler et al 2018), strains isolated from food and food processing environments (Chaves et al 2017;Heini et al 2018;Johler et al 2018;Kindle et al 2019;Rossi et al 2017;Thorsen et al 2015;Zhuang et al 2019), and strains with important industrial applications (Johler et al 2018;Lazarte et al 2018), as well as to construct risk and exposure assessment frameworks for B. cereus s.l. (Guinebreti ere et al 2010;Rigaux et al 2013;Webb et al 2019) and to assign B. cereus s.l.…”

Profiling of Bacillus cereus on Canadian grain

“…These genes are important for the biopesticide activity of B . thuringiensis in commercially available products registered for use in Canada [ 50 ]. The absence of these genes in the samples from this study suggest that the isolates we recovered are not those from commercial products used in agriculture to control insect pests.…”