Listeria monocytogenes source distribution analysis indicates regional heterogeneity and ecological niche preference among serotype 4b clones

Authors: LEE, SANGMI - North Carolina State University; CHEN, YI - Food And Drug Administration(FDA); Gorski, Lisa; Ward, Todd; OSBORNE, JASON - North Carolina State University; KATHARIOU, SOPHIA - North Carolina State University

Submitted to: mBio
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/8/2018
Publication Date: 4/17/2018
Citation: Lee, S., Chen, Y., Gorski, L.A., Ward, T.J., Osborne, J., Kathariou, S. 2018. Listeria monocytogenes source distribution analysis indicates regional heterogeneity and ecological niche preference among serotype 4b clones. mBio. 9(2):1-12. https://doi.org/10.1128/mBio.00396-18.
DOI: https://doi.org/10.1128/mBio.00396-18

Interpretive Summary: Human illness due to the foodborne pathogen Listeria monocytogenes is most frequently due to ingestion of strains of serotype 4b. Within serotype 4b are subtypes, based on the similarity of DNA sequences of specific genes in the genomes that are known as clonal complexes (CCs). CC1, CC2 and CC6 have been frequently implicated in sporadic listeriosis as well as numerous outbreaks of foodborne disease. Characterization of isolates of diverse serotype and sources, primarily from Europe, indicated that CC1, CC2, CC6 and especially the more recently identified clonal complex 4 (CC4) are significantly more likely to be encountered among isolates from human listeriosis than from food or environmental sources. While CC4 has been encountered in Europe, the extent to which this subtype of L. monocytogenes in found elsewhere is poorly characterized. In the current study, genotyping of 295 isolates of serotype 4b was done to assess the relative prevalence of different clonal groups in isolates from human listeriosis, mostly from N. America, vs. other sources. Surprisingly, CC1 and CC6 were similarly distributed between clinical and non-clinical isolates whereas CC2 was over-represented among food/environmental isolates, suggesting that frequent human exposure through contaminated foods contributes to the predominance of these CCs in human listeriosis. However, CC4, which has not yet been implicated in outbreaks of listeriosis in North America, was markedly over-represented among human clinical isolates, supporting the previously described human hypervirulence of this clone. The less abundant CC388 was also over-represented among human isolates. Isolates of CC 217, 382 and ST 639 were of human clinical origin and from watersheds but rare from food or food processing environments, raising the possibility that water, rather than food exposure, may contribute to human disease via these strains. Our findings indicate that serotype 4b clonal complexes might differ in their preferences of ecological niches and suggest the need to further elucidate the sources and vectors of these hypervirulent subtpyes.

Technical Abstract: Human illness due to the foodborne bacterial pathogen Listeria monocytogenes frequently involves certain widely disseminated clonal complexes (CCs), primarily of serotype 4b. CC1, CC2 and CC6, previously also designated epidemic clone (EC) I, Ia and II, respectively, have been frequently implicated in sporadic listeriosis as well as numerous outbreaks of foodborne disease. Characterization of isolates of diverse serotype and sources, primarily from Europe, indicated that CC1, CC2, CC6 and especially the more recently identified clonal complex 4 (CC4) are significantly more likely to be encountered among isolates from human listeriosis than from food or environmental sources. The extent to which such distributions of these CC4s are conserved among serotype 4b isolates in other regions poorly characterized. In the current study, genotyping of 295 isolates of serotype 4b was employed to assess the relative prevalence of different clonal groups in isolates from human listeriosis, mostly from N. America, vs. other sources. Surprisingly, CC1 and CC6 were similarly distributed between clinical and non-clinical isolates whereas CC2 was over-represented among food/environmental isolates, suggesting that frequent human exposure through contaminated foods contributes to the predominance of these CCs in human listeriosis. However, CC4, which has not yet been implicated in outbreaks of listeriosis in North America, was markedly over-represented among human clinical isolates, supporting the previously described human hypervirulence of this clone. The less abundant CC388 was also over-represented among human isolates. Of note, isolates of CC 217, 382 and ST 639 were of human clinical origin and from watersheds but rare from food or food processing environments, raising the possibility that water, rather than food exposure, may contribute to human disease via these strains. Our findings indicate that serotype 4b clonal complexes might differ in their preferences of ecological niches and suggest the need to further elucidate reservoirs and vehicles for clones over-represented in human listeriosis.