Whole-Genome Sequencing Reveals Multiple Subpopulations of Dominant and Persistent Lineage I Isolates of Listeria monocytogenes in Two Meat Processing Facilities during 2011–2015

Abstract

Listeria monocytogenes is a foodborne pathogen with a highly clonal population structure comprising multiple phylogenetic sub-groups that can persist within food processing environments and contaminate food. The epidemiology of L. monocytogenes is well-described in some developed countries; however, little is known about the prevalence and population structure of this pathogen in food and food processing environments located in less developed regions. The aim of this study was to determine the genetic characteristics and clonal relatedness of L. monocytogenes that were isolated from two Jamaican meat processing facilities. Of the 37 isolates collected between 2011 and 2015, only a single lineage II isolate was recovered (serotype 1/2c), and the remaining were lineage I isolates representing serotypes 4b, 1/2b, 3b, and two untypeable isolates. Pulsed-field gel electrophoresis (PFGE) delineated isolates into seven pulsotypes, and whole-genome sequencing (WGS) categorized most isolates within one of three clonal complexes (CC): CC2 (N = 12), CC5 (N = 11), and CC288 (N = 11). Isolates representing CC1 (N = 2) and CC9 (N = 1) were also recovered. Virulence-associated genes such as inlA and the LIPI-3 cluster were detected in multiple isolates, along with the stress survival islet cluster-1 (SSI-1), and benzalkonium (bcrABC) and cadmium (cad1, cad2, cad4) resistance cassettes. Multiple isolates that belong to the same CC and matching PFGE patterns were isolated from food and the environment from both facilities across multiple years, suggesting the presence of persistent strains of L. monocytogenes, and/or constant re-entry of the pathogens into the facilities from common sources. These findings highlight the ability of lineage I isolates of L. monocytogenes to colonize, persist, and predominate within two meat-producing environments, and underscores the need for robust surveillance strategies to monitor and mitigate against these important foodborne pathogens.

The Slaughterhouse as Hotspot of CC1 and CC6 Listeria monocytogenes Strains with Hypervirulent Profiles in an Integrated Poultry Chain of Italy

“…Other authors also reported similar results [ 21 , 27 , 52 , 53 ] with hypervirulent clones such as CC1, CC2 and CC6 persisting for long time. These findings could indicate that the fitness of a strain is relative to the environment with which it is interacting.…”

Whole Genome Sequencing as the Ultimate Genomic Subtyping Tool for the Identification and Control of Listeria monocytogenes in the RTE Food Chain

“…Furthermore, using WGS, Demaître et al (2021) concluded that the persistence of Listeria contamination on the slaughter line was due to the presence of hypovirulent lineage II CC9 strain in the carcass splitter for longer than one year. However, Burnett et al (2022) found hypervirulent I strains of L monocytogenes in two meat processing facilities during 2011-2015. These strains originated from raw and environmental samples, representing serotypes 4b, 1/2b and 3b and belonged to clonal complexes: CC1, CC2, CC5 and CC288.…”

Persistence of microbiological hazards in food and feed production and processing environments

“…(A) Genetic lineage I CC associated with environmental persistence; (B) Genetic lineage II CC associated with environmental persistence. Note : Based on (Brown et al., 2021; Burnett et al., 2022; Centorotola et al., 2021; Chase et al., 2017; Chen et al., 2017; Chen et al., 2022; Chen, Burall, et al., 2016; Cherifi et al., 2018; Chiara et al., 2014; Conficoni et al., 2016; Corcoran et al., 2013; Daeschel et al., 2022; De Cesare et al., 2017; Demaitre et al., 2021; Demaître et al., 2021; Elson et al., 2019; Fagerlund et al., 2016; Fagerlund et al., 2020; Fei et al., 2015; Gan et al., 2021; Gelbicova et al., 2018; Gelbícová et al., 2019; Guidi et al., 2021; Guidi et al., 2022; Harrand et al., 2020; Holch et al., 2013; Hurley et al., 2019; Jensen et al., 2016; Kaszoni‐Rückerl et al., 2020; Knudsen et al., 2017; Kovacevic et al., 2016; Lachmann et al., 2021; Lachmann et al., 2022; Lake et al., 2021; Lassen et al., 2016; Lee et al., 2019; Liu et al., 2022; Louha et al., 2020; Lu et al., 2019; Luth et al., 2020; Madden et al., 2018; Maggio et al., 2021; Maurella et al., 2018; McLauchlin et al., 2020; Melero, Manso, et al., 2019; Melero, Stessl, et al., 2019; Mohan et al., 2021; Moretro et al., 2017; Muhterem‐Uyar et al., 2018; Negrete et al., 2022; Nilsson et al., 2012; Nowak et al., 2017; Nowak et al., 2021; Nüesch‐Inderbinen et al., …”