Hypervirulent Listeria monocytogenes clones’ adaption to mammalian gut accounts for their association with dairy products

Hypervirulent Listeria monocytogenes clones’ adaption to mammalian gut accounts for their association with dairy products

Listeria monocytogenes (Lm) is a major human and animal foodborne pathogen. Although all Lm strains are considered so far as equally virulent by regulatory authorities, we have previously shown, using epidemiological and experimental approaches, that this species is in fact very genetically and phenotypically diverse, with hypervirulent and hypovirulent Lm sub-populations, called clones (Maury, Tsai et al., Nat Genet 2016). It is therefore important, both scientifically and on a public health stand point, to determine if these clones evolve in distinct ecological niches and to identify the driving forces selecting for these differences in virulence.

Our last study published in Nature Communications investigated the distribution of these clones in different types of food products, and in particular tested for association of hypervirulent and hypovirulent clones with distinct food categories. To this aim, we analyzed all food (n = 3,333) and clinical (n = 3,308) non-redundant isolates prospectively collected for 12 consecutive years (from 2005 to 2016) in the context of the surveillance of listeriosis in France. This showed that highly distinct Lm populations are present in different types of food items. Indeed, hypervirulent clones, especially CC1, are associated to dairy products, whereas hypovirulent clones, mostly CC9 and CC121, are overrepresented in meat and seafood products.

In order to understand the bases of these differences, we performed in vivo and in vitro experiments, and showed that hypervirulent clones colonize better the intestinal lumen and invade more intestinal tissues than hypovirulent ones. This suggests that hypervirulent clones are better adapted for within-host survival, persistence, fecal shedding and likely inter-host transmission than other clones. In the particular case of dairy cattle, the higher gut colonization capacity of CC1 may lead to its prolonged fecal shedding, resulting in its high prevalence and persistence in dairy cattle farm environments and in milk-derived products.

In contrast, hypovirulent clones exhibit a higher prevalence of stress resistance and benzalkonium chloride tolerance genes, and a higher survival and biofilm formation capacity in presence of sub-lethal concentrations of this disinfectant, suggesting a better adaptation to the food production environment.  These data may help understand how Lm circulates between animals, food/feed, humans and the environment and eventually help better identify food contamination routes to reduce food contamination. These results also have important public health implications and may help improving food consumption recommendations to at-risk populations.

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