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

Abstract

Listeria monocytogenes ( Lm ) is a major human and animal foodborne pathogen. Here we show that hypervirulent Lm clones, particularly CC1, are strongly associated with dairy products, whereas hypovirulent clones, CC9 and CC121, are associated with meat products. Clone adaptation to distinct ecological niches and/or different food products contamination routes may account for this uneven distribution. Indeed, hypervirulent clones colonize better the intestinal lumen and invade more intestinal tissues than hypovirulent ones, reflecting their adaption to host environment. Conversely, hypovirulent clones are adapted to food processing environments, with a higher prevalence of stress resistance and benzalkonium chloride tolerance genes and a higher survival and biofilm formation capacity in presence of sub-lethal benzalkonium chloride concentrations. Lm virulence heterogeneity therefore reflects the diversity of the ecological niches in which it evolves. These results also have important public health implications and may help in reducing food contamination and improving food consumption recommendations to at-risk populations.

Modelling the survival of Listeria monocytogenes strains in soft lactic cheese following acid and salt stress exposures

“…Serotype 4b (lineage I) strains like ATCC19115 have a predilection for the human host but lack the ability to compete well in the food environment where lineage II strains dominate (Orsi et al ). Over and above the genetic lineage differences influencing stress adaptation, recent evidence shows that L. monocytogenes stress resistance heterogeneity exists among sublineages and clonal complexes (Maury et al, ).…”

Listeria monocytogenes, a model in infection biology

“…Interestingly, the clones which are the most prevalent in human patients are also the ones most frequently associated with listeriosis in dairy cattle, and also those most associated with contaminated dairy products. This suggests that Lm virulence in human may be linked to its ability to be associated with dairy cattle (Maury et al, ). In the same way that Pascale Cossart and colleagues have shown that comparative genomics between Lm and Li can lead to the identification of multiple Lm genes involved in its pathogenic potential (Glaser et al, ), comparative genomics of multiple Lm isolates from various sources is expected to be exceptionally powerful to identify clinically relevant microbial virulence attributes.…”

Dissemination and conservation of cadmium and arsenic resistance determinants in Listeria and other Gram‐positive bacteria

“…(Lee, Ward, Jima, Parsons, & Kathariou, ). It also shows strong propensity for the hypervirulent clone CC2 and a specific integration site but can also be encountered in diverse clones and integration sites (Lee et al, ; Maury et al, ; Pasquali et al, ). LGI2 is typically chromosomal (Kuenne et al, ; Lee et al, ), and only rarely plasmid‐borne (Hingston et al, ).…”

“…The distribution of LGI2 with cadA4C4 and LGI2‐1 with cadA5C5 also suggests possible associations with virulence, as these MGEs are primarily encountered in L. monocytogenes and have a propensity for the hypervirulent clones CC2 and CC1, respectively (Lee et al, ; Maury et al, ). CadA2C2 has been encountered in outbreak strains of both serotype 1/2a and 4b (Nelson et al, ).…”

“…(Lee, Ward, Jima, Parsons, & Kathariou, 2017). It also shows strong propensity for the hypervirulent clone CC2 and a specific integration site but can also be encountered in diverse clones and integration sites Maury et al, 2019;Pasquali et al, 2018).…”