Tetracycline resistance in Listeria monocytogenes and L. innocua from wild black bears ( Ursus americanus ) in the United States is mediated by novel transposable elements

Author:

Brown Phillip1ORCID,Hernandez Kevin2,Parsons Cameron2,Chen Yi3,Gould Nicholas4,DePerno Christopher S.4,Niedermeyer Jeffrey2,Kathariou Sophia12

Affiliation:

1. Department of Plant and Microbial Biology, North Carolina State University , Raleigh, North Carolina, USA

2. Department of Food, Bioprocessing and Nutrition Sciences, North Carolina State University , Raleigh, North Carolina, USA

3. Division of Microbiology, Center for Food Safety and Applied Nutrition, Food and Drug Administration , College Park, Maryland, USA

4. Fisheries, Wildlife, and Conservation Biology, Department of Forestry and Environmental Resources, North Carolina State University , Raleigh, North Carolina, USA

Abstract

ABSTRACT Listeria monocytogenes is a facultative intracellular foodborne pathogen and the causative agent of the severe disease listeriosis. It is found ubiquitously in the environment and exhibits innate resistance to certain antimicrobials, but acquired antimicrobial resistance remains relatively uncommon. Given the potentially dire health outcomes associated with listeriosis, acquisition of antimicrobial resistance (AMR) by this pathogen is of considerable public health concern. AMR in L. monocytogenes has been surveyed frequently in strains of clinical and food origin, but much less commonly in wildlife. We analyzed 158 strains of L. monocytogenes and 27 of non-pathogenic Listeria spp. isolated from wild black bears ( Ursus americanus ) for resistance to a panel of antimicrobials. AMR was uncommon and noted mostly for tetracycline. Tetracycline resistance was more common in Listeria innocua than in L. monocytogenes . All tetracycline-resistant L. monocytogenes strains belonged to sequence type ST1039 and harbored the Tn 916 -like tet (M) transposon Tn 916.1039 in a conserved chromosomal location. In contrast, three different tetracycline resistance elements, i.e., the tet (M) elements Tn 5801.UAM and Tn 5801.551 and the tet (S) element Tn 6000.205 , were identified among tetracycline-resistant strains of L. innocua . The greater prevalence and diversity of tetracycline resistance elements among bear-derived non-pathogenic Listeria strains suggest the potential of the latter to serve as reservoirs for retention and diversification of AMR determinants in this wildlife host and warrant their further monitoring and study. IMPORTANCE Listeria monocytogenes causes severe foodborne illness and is the only human pathogen in the genus Listeria . Previous surveys of AMR in Listeria focused on clinical sources and food or food processing environments, with AMR in strains from wildlife and other natural ecosystems remaining under-explored. We analyzed 185 sequenced strains from wild black bears ( Ursus americanus ) from the United States, including 158 and 27 L . monocytogenes and L. innocua , respectively. Tetracycline resistance was the most prevalent resistance trait. In L . monocytogenes, it was encountered exclusively in serotype 4b strains with the novel Tn 916 -like element Tn 916.1039 . In contrast, three distinct, novel tetracycline resistance elements (Tn 5801.UAM , Tn5801.551 , and Tn 6000.205 ) were identified in L. innocua . Interestingly, Tn5801.551 was identical to elements in L. monocytogenes from a major foodborne outbreak in the United States in 2011. The findings suggest the importance of wildlife and non-pathogenic Listeria species as reservoir for resistance elements in Listeria .

Funder

U.S. Department of Agriculture

Alcinda Acorn Foundation

Faile Foundation

Publisher

American Society for Microbiology

Subject

Ecology,Applied Microbiology and Biotechnology,Food Science,Biotechnology

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