Novel, highly divergent clones in Listeria monocytogenes serotype 4b in North America: Sublineages 782 and 1039, members of the hypervirulent clonal complex 2
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Listeria monocytogenes is a Gram-positive bacterial foodborne pathogen responsible for the severe illness listeriosis. Of the 14 L. monocytogenes serotypes, serotype 4b is a major contributor to human listeriosis and encompasses all four leading hypervirulent clonal complexes (CCs), including the ancient, ubiquitous CC2. CC2 is globally dominated by sublineage (SL) 2, responsible for most human CC2-associated cases. Here we describe two other CC2 SLs, SLs 782 and 1039. These SLs are newly recognized, having been reported only since 2002, and to date are encountered exclusively in North America. Phylogenetic analysis revealed that they are strikingly divergent from each other as well as from SL2. SL782 and SL1039 have been implicated in human listeriosis and have also been repeatedly isolated from surface water and wildlife in North America, with several of these environmental strains exhibiting high genomic similarity (≤7 core genome allelic mismatches) to strains from human listeriosis. They share an unusual resistance profile towards a panel of Listeria wide-host-range-phages and exhibit several distinct lineage-specific traits. Specifically, SL782 universally lacks a gene otherwise unique to and conserved in serotype 4b and harbors the Listeria pathogenicity island LIPI-4, while SL1039 harbors LIPI-3 and is almost always resistant to tetracycline, harboring the novel Tn 916 -like transposon Tn 916 . 1039 . These and other traits may have driven clonal emergence of SL782 and SL1039, potentially via adaptations in natural ecosystems.
IMPORTANCE
Listeria monocytogenes causes the severe foodborne illness listeriosis and the hypervirulent clonal complex (CC) 2 is a major contributor to human disease. Most CC2 strains belong to the long-recognized, ubiquitous sublineage (SL) 2. Surprisingly, the two other leading SLs within CC2, SL782 and 1039, have been isolated exclusively from North America, and only subsequently to 2002. They differ remarkably from each other and other CC2 strains and exhibit unusual genomic and phenotypic traits. They have been repeatedly isolated from watersheds and wildlife, with such environmental isolates exhibiting high genomic similarity to those from human listeriosis. The findings are important in identifying novel, unexpected features in the composition and evolution of a major, hypervirulent L. monocytogenes CC. They will also serve as platforms for further studies to further elucidate the reservoirs, emergence, persistence, and dissemination of novel Listeria sublineages and their roles in the continuum between natural ecosystems and human disease.
