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Title: The arsenic resistance-associated Listeria genomic island LGI2 exhibits sequence and integration site diversity and a propensity for three Listeria monocytogenes clones with enhanced virulence

item LEE, SANGMI - North Carolina State University
item Ward, Todd
item KATHARIOU, SOPHIA - North Carolina State University

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/11/2017
Publication Date: 11/1/2017
Citation: Lee, S., Ward, T.J., Jima, D.D., Parsons, C., Kathariou, S. 2017. The arsenic resistance-associated Listeria genomic island LGI2 exhibits sequence and integration site diversity and a propensity for three Listeria monocytogenes clones with enhanced virulence. Applied and Environmental Microbiology. 83(21):83:e01189-17.

Interpretive Summary: Listeria monocytogenes is the only human pathogen in the genus Listeria that causes disease (listeriosis) transmitted via contaminated foods and manifested with severe symptoms and high mortality. Arsenic resistance was previously found to be strongly associated with certain groups of L. monocytogenes (serotype 4b) that are most commonly responsible for sporadic illness and major outbreaks of listeriosis. In this study, we characterized the distribution and diversity of arsenic resistance genes among 85 arsenic resistant L. monocytogenes strains, and determined that multiple independent acquisitions of arsenic resistance genes have occurred during the evolution of serotype 4b strains. The genes for arsenic resistance are accompanied by other genes with potentially significant biological functions in a mobile segment of DNA termed a genomic island that has been inserted into at least 8 different locations within the L. monocytogenes genome. These results indicate that the genomic island carrying arsenic resistance genes is capable of frequent movement between different Listeria strains and has the ability to transfer various accessory genes in addition to those that encode arsenic resistance. This study provides new information about the distribution of genes used by L. monocytogenes to persist in different environments and will be of direct interest to scientists involved in food safety research.

Technical Abstract: In the foodborne pathogen Listeria monocytogenes, arsenic resistance is encountered primarily in serotype 4b clones considered to have enhanced virulence and is associated with an arsenic resistance gene cluster within a 35-kb chromosomal region, Listeria genomic island 2 (LGI2). LGI2 was first identified in strain Scott A and includes genes putatively involved in arsenic and cadmium resistance, DNA integration, conjugation, and pathogenicity. However, the genomic localization and sequence content of LGI2 remain poorly characterized. Here we investigated 85 arsenic-resistant L. monocytogenes strains, mostly of serotype 4b. All but one of the 70 serotype 4b strains belonged to clonal complex 1 (CC1), CC2, and CC4, three major clones associated with enhanced virulence. PCR analysis suggested that 53 strains (62.4%) harbored an island highly similar to LGI2 of Scott A, frequently (42/53) in the same location as Scott A (LMOf2365_2257 homolog). Random-primed PCR and whole-genome sequencing revealed seven novel insertion sites, mostly internal to chromosomal coding sequences, among strains harboring LGI2 outside the LMOf2365_2257 homolog. Interestingly, many CC1 strains harbored a noticeably diversified LGI2 (LGI2-1) in a unique location (LMOf2365_0902 homolog) and with a novel additional gene. With few exceptions, the tested LGI2 genes were not detected in arsenic-resistant strains of serogroup 1/2, which instead often harbored a Tn554-associated arsenic resistance determinant not encountered in serotype 4b. These findings indicate that in L. monocytogenes, LGI2 has a propensity for certain serotype 4b clones, exhibits content diversity, and is highly promiscuous, suggesting an ability to mobilize various accessory genes into diverse chromosomal loci.