Abstract

Listeria monocytogenes is a pathogen mostly associated with the consumption of ready-to-eat foods and can cause severe disease and death. It can be introduced into food chains from raw materials, but often the contamination source is the food production environment, where certain clones can persist for years. In the meat chain, ST9 is one of the most commonly encountered L. monocytogenes sequence types, and for effective source tracking, the divergence and spread of ST9 must be understood. In this study, whole-genome sequencing (WGS) was used to characterize and track 252 L. monocytogenes ST9 isolates collected from four Norwegian meat processing plants between 2009 and 2017. The isolates formed distinct clusters relative to genomes found in public databases, and all but three isolates clustered into two major clonal populations. Different contamination patterns were revealed, e.g., evidence of contamination of two factories with a clone that diverged from its ancestor in the late 1990s through a common source of raw materials; breach of hygienic barriers within a factory, leading to repeated detection of two clones in the high-risk zone during a 4- to 6-year period; entry through the purchase and installation of second-hand equipment harboring a previously established clonal population; and spreading and diversification of two clones from two reservoirs within the same production room over a 9-year period. The present work provides data on the diversity of ST9, which is crucial for epidemiological investigations and highlights how WGS can be used for source tracking within food processing factories.IMPORTANCEListeria monocytogenes is a deadly foodborne pathogen that is widespread in the environment, and certain types can be established in food factories. The sequence type ST9 dominates in meat processing environments, and this work was undertaken to obtain data needed for the tracking of this subtype. By using whole-genome sequencing (WGS), we revealed the presence of cross-contamination routes between meat factories as well as within a single factory, including the spread from different reservoirs within the same room. It was also possible to estimate the time frame of persistence in the factory, as well as when and how new clones had entered. The present work contributes valuable information about the diversity of ST9 and exemplifies the potential power of WGS in food safety management, allowing the determination of relationships between strains both in an international context and locally between and within factories.

Highlights

  • Listeria monocytogenes is a pathogen mostly associated with the consumption of ready-to-eat foods and can cause severe disease and death

  • The goals of the present study were to (i) apply whole-genome multilocus sequence typing (MLST), core genome MLST, and single-nucleotide polymorphism (SNP) analyses to assess the genetic diversity of the ST9 strains; (ii) determine whether certain genetic clusters of ST9 were factory specific, to what extent they were present in the same factory during extended periods of time, and how they related to isolates from other sources; and (iii) explore whether whole-genome sequencing (WGS) analyses can be used to differentiate between contamination scenarios: hygienic breach between zones, dissemination of persistent listeria from a specific niche, or wide dissemination of a specific variant within a zone

  • Monocytogenes ST9 isolates from four Norwegian meat processing plants were subjected to whole-genome sequencing (WGS) analysis

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Summary

Introduction

Listeria monocytogenes is a pathogen mostly associated with the consumption of ready-to-eat foods and can cause severe disease and death It can be introduced into food chains from raw materials, but often the contamination source is the food production environment, where certain clones can persist for years. Listeria monocytogenes is a pathogenic bacterium causing the severe foodborne disease listeriosis, which is mostly linked to the consumption of ready-to-eat (RTE) food like fresh produce, soft cheeses, lightly processed fish products, and meat prod-. Many studies have reported that clones of L. monocytogenes may establish and persist for years in processing environments, including in factories in the meat industry [5,6,7,8,9,10,11,12,13,14,15]. In a previous study [26], we subtyped a total of 680 L. monocytogenes isolates from Norwegian meat and salmon processing plants and found that 70% of the isolates from the meat industry (obtained mainly from two extensively sampled factories) belonged to ST9

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