Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity

Maury, Mylène M.; Tsai, Yu Huan; Charlier, Caroline; Touchon, Marie; Chenal-Francisque, Viviane; Leclercq, Alexandre; Criscuolo, Alexis; Gaultier, Charlotte; Roussel, Sophie; Brisabois, Anne; Disson, Olivier; Rocha, Eduardo P. C.; Brisse, Sylvain; Lecuit, Marc

doi:10.1038/ng.3501

Cited by 563 publications

(1,003 citation statements)

References 44 publications

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“…The L. monocytogenes bile salt hydrolase was the first factor described to be involved in survival within the intestinal lumen (24). LLS was previously shown to be a hemolytic and cytotoxic factor (9) and has recently been associated with infectious potential in a molecular epidemiological and comparative genomic study of L. monocytogenes strains from different lineages (5).…”

Section: Discussionmentioning

confidence: 99%

“…As a consequence, L. monocytogenes lacking LLS is impaired in its capacity to compete with intestinal microbiota and does not survive as efficiently as WT bacteria in the intestinal lumen, a critical step for the establishment of listeriosis. Interestingly, the strains EGD-e and EGD, which lack LLS, rarely cause human disease (5). The mechanisms by which these strains can colonize the intestine need to be assessed in future experiments.…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, major listeriosis epidemics have been preferentially associated to L. monocytogenes clonal groups belonging to the evolutionary lineage I and, more specifically, to serotype 4b (4,5), but the molecular mechanisms that contribute to the higher virulence potential of these bacterial strains have not been identified yet.…”

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confidence: 99%

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Bacteriocin from epidemicListeriastrains alters the host intestinal microbiota to favor infection

Quereda

Dussurget

Nahori

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

151

163

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Listeria monocytogenes is responsible for gastroenteritis in healthy individuals and for a severe invasive disease in immunocompromised patients. Among the three identified L. monocytogenes evolutionary lineages, lineage I strains are overrepresented in epidemic listeriosis outbreaks, but the mechanisms underlying the higher virulence potential of strains of this lineage remain elusive. Here, we demonstrate that Listeriolysin S (LLS), a virulence factor only present in a subset of lineage I strains, is a bacteriocin highly expressed in the intestine of orally infected mice that alters the host intestinal microbiota and promotes intestinal colonization by L. monocytogenes, as well as deeper organ infection. To our knowledge, these results therefore identify LLS as the first bacteriocin described in L. monocytogenes and associate modulation of host microbiota by L. monocytogenes epidemic strains to increased virulence.T he gram-positive bacterium Listeria monocytogenes is a facultative intracellular pathogen that causes foodborne infections in humans and animals. Upon consumption of contaminated food, L. monocytogenes reaches the intestinal lumen, crosses the intestinal barrier, and disseminates within the host. The clinical manifestations of listeriosis vary from a mild, self-limiting gastroenteritis to severe intestinal and systemic infections, with a fatality rate estimated to 20-30% of infected individuals (1). Host gut microbiota plays a critical role in resistance against colonization by invading pathogens within the intestine (2). The mechanisms of L. monocytogenes to compete with the host microbiota to survive in the intestine remain unknown.During the last decades, the majority of Listeria studies in bacterial pathophysiology, cell biology, and immunology compared three pathogenic strains from lineage II: EGD, EGD-e, and 10403S (3). Interestingly, major listeriosis epidemics have been preferentially associated to L. monocytogenes clonal groups belonging to the evolutionary lineage I and, more specifically, to serotype 4b (4, 5), but the molecular mechanisms that contribute to the higher virulence potential of these bacterial strains have not been identified yet.Bacteriocins are bacterially synthesized proteinaceous substances that target and inhibit the growth of closely related bacteria, allowing competition in diverse ecological niches, including the digestive tract (6, 7). Production of these antimicrobial peptides is widespread among bacterial species, and such production is made possible by biosynthetic machineries present in the genome, plasmids, or conjugative transposons (7). A conserved biosynthetic gene cluster for the production of bacteriocins displaying thiazole and oxazole heterocycles was discovered in 2008 in six microbial phyla (8). These gene clusters encode a toxin precursor and all indispensable proteins for toxin maturation in a mode similar to that associated with the bacteriocin microcin B17 (8). This gene cluster in L .monocytogenes was only present in a subset of lineage I strains...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Bacteriocin from epidemicListeriastrains alters the host intestinal microbiota to favor infection

Quereda

Dussurget

Nahori

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

151

163

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“…Listeriosis is of major importance in humans and in farmed ruminants3, in which it is associated with gastroenteritis, abortions, bacteremia, mastitis and central nervous system (CNS) infections (neurolisteriosis)4567. In humans, L. monocytogenes has the highest hospitalization and mortality rates amongst food-borne pathogens89.…”

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confidence: 99%

Listeria monocytogenes sequence type 1 is predominant in ruminant rhombencephalitis

Dreyer

Aguilar-Bultet

Rupp

et al. 2016

Sci Rep

Self Cite

131

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Listeria (L.) monocytogenes is an opportunistic pathogen causing life-threatening infections in diverse mammalian species including humans and ruminants. As little is known on the link between strains and clinicopathological phenotypes, we studied potential strain-associated virulence and organ tropism in L. monocytogenes isolates from well-defined ruminant cases of clinical infections and the farm environment. The phylogeny of isolates and their virulence-associated genes were analyzed by multilocus sequence typing (MLST) and sequence analysis of virulence-associated genes. Additionally, a panel of representative isolates was subjected to in vitro infection assays. Our data suggest the environmental exposure of ruminants to a broad range of strains and yet the strong association of sequence type (ST) 1 from clonal complex (CC) 1 with rhombencephalitis, suggesting increased neurotropism of ST1 in ruminants, which is possibly related to its hypervirulence. This study emphasizes the importance of considering clonal background of L. monocytogenes isolates in surveillance, epidemiological investigation and disease control.

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“…With the recent evolution of whole-genome sequencing technologies, high-resolution typing schemes have been developed for the characterization of L. monocytogenes strains (Ruppitsch et al, 2015a;Pightling et al, 2015;Kwong et al, 2016;Maury et al, 2016). The developed core genome (cg) MLST scheme based typing of L. monocytogenes represents an expansion of the classical seven gene MLST scheme (Salcedo et al, 2003) and is in all aspects superior for the tracking and source identification, as compared to the current gold standard methods PFGE and fAFLP (Schmid et al, 2014;Ruppitsch et al, 2015b).…”

Section: Introductionmentioning

confidence: 99%

Whole genome sequence-based serogrouping of Listeria monocytogenes isolates

Hyden

Pietzka

Lennkh

et al. 2016

Journal of Biotechnology

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Whole genome sequencing (WGS) is currently becoming the method of choice for characterization of Listeria monocytogenes isolates in national reference laboratories (NRLs). WGS is superior with regards to accuracy, resolution and analysis speed in comparison to several other methods including serotyping, PCR, pulsed field gel electrophoresis (PFGE), multilocus sequence typing (MLST), multilocus variable number tandem repeat analysis (MLVA), and multivirulence-locus sequence typing (MVLST), which have been used thus far for the characterization of bacterial isolates (and are still important tools in reference laboratories today) to control and prevent listeriosis, one of the major sources of foodborne diseases for humans. Backward compatibility of WGS to former methods can be maintained by extraction of the respective information from WGS data. Serotyping was the first subtyping method for L. monocytogenes capable of differentiating 12 serovars and national reference laboratories still perform serotyping and PCR-based serogrouping as a first level classification method for Listeria monocytogenes surveillance. Whole genome sequence based core genome MLST analysis of a L. monocytogenes collection comprising 172 isolates spanning all 12 serotypes was performed for serogroup determination. These isolates clustered according to their serotypes and it was possible to group them either into the IIa, IIc, IVb or IIb clusters, respectively, which were generated by minimum spanning tree (MST) and neighbor joining (NJ) tree data analysis, demonstrating the power of the new approach.

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Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity

Cited by 563 publications

References 44 publications

Bacteriocin from epidemicListeriastrains alters the host intestinal microbiota to favor infection

Bacteriocin from epidemicListeriastrains alters the host intestinal microbiota to favor infection

Listeria monocytogenes sequence type 1 is predominant in ruminant rhombencephalitis

Whole genome sequence-based serogrouping of Listeria monocytogenes isolates

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