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The population structure and genetic diversity of Listeria monocytogenes ST9 strains based on genomic analysis.

ABSTRACT: Listeria monocytogenes is a ubiquitous foodborne pathogen causing both invasive and non-invasive listeriosis. Sequence type (ST) 9 strains is common in food and food processing environments. In this study, the whole-genome sequences (WGS) of 207 ST9 isolates from different sources, geographical locations (14 countries), and isolated years were analyzed. The ST9 isolates were divided into three clusters after phylogenetic analysis; 67.63% of ST9 isolates contained putative plasmids with different sizes and genomic structure, the putative prophages inserted in the chromosome at ten hotspots, and seven types of premature stop codon (PMSC) mutations in inlA were found in 81.86% of the ST9 isolates. In addition, 78.26% of ST9 isolates harbored Tn554-like elements carrying arsenic resistance genes. All the ST9 isolates conservatively contained environment-resistance genes on the chromosome. This analysis of population structures and features of ST9 isolates was aimed to help develop effective strategies to control this prevalent pathogen in the food chain.

SUBMITTER: Song Z

PROVIDER: S-EPMC9680904 | biostudies-literature | 2022

REPOSITORIES: biostudies-literature

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The population structure and genetic diversity of <i>Listeria monocytogenes</i> ST9 strains based on genomic analysis.

Song Zexuan Z Ji Shunshi S Wang Yan Y Luo Lijuan L Wang Yiqian Y Mao Pan P Li Lingling L Jiang Huaying H Ye Changyun C

Frontiers in microbiology 20221108

<i>Listeria monocytogenes</i> is a ubiquitous foodborne pathogen causing both invasive and non-invasive listeriosis. Sequence type (ST) 9 strains is common in food and food processing environments. In this study, the whole-genome sequences (WGS) of 207 ST9 isolates from different sources, geographical locations (14 countries), and isolated years were analyzed. The ST9 isolates were divided into three clusters after phylogenetic analysis; 67.63% of ST9 isolates contained putative plasmids with di ...[more]

PMID: 36425025

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Project description:UnlabelledListeria monocytogenes is a ubiquitous bacterium that may cause the foodborne illness listeriosis. Only a small amount of data about the population genetic structure of strains isolated from food is available. This study aimed to provide an accurate view of the L. monocytogenes food strain population in France. From 1999 to 2014, 1,894 L. monocytogenes strains were isolated from food at the French National Reference Laboratory for L. monocytogenes and classified according to the five risk food matrices defined by the European Food Safety Authority (EFSA). A total of 396 strains were selected on the basis of different pulsed-field gel electrophoresis (PFGE) clusters, serotypes, and strain origins and typed by multilocus sequence typing (MLST), and the MLST results were supplemented with MLST data available from Institut Pasteur, representing human and additional food strains from France. The distribution of sequence types (STs) was compared between food and clinical strains on a panel of 675 strains. High congruence between PFGE and MLST was found. Out of 73 PFGE clusters, the two most prevalent corresponded to ST9 and ST121. Using original statistical analysis, we demonstrated that (i) there was not a clear association between ST9 and ST121 and the food matrices, (ii) serotype IIc, ST8, and ST4 were associated with meat products, and (iii) ST13 was associated with dairy products. Of the two major STs, ST121 was the ST that included the fewest clinical strains, which might indicate lower virulence. This observation may be directly relevant for refining risk analysis models for the better management of food safety.ImportanceThis study showed a very useful backward compatibility between PFGE and MLST for surveillance. The results enabled better understanding of the population structure of L. monocytogenes strains isolated from food and management of the health risks associated with L. monocytogenes food strains. Moreover, this work provided an accurate view of L. monocytogenes strain populations associated with specific food matrices. We clearly showed that some STs were associated with food matrices, such as meat, meat products, and dairy products. We opened the way to source attribution modeling in order to quantify the relative importance of the main food matrices.

Project description:Listeria monocytogenes is an ubiquitous pathogenic bacterium, transmissible to humans through the consumption of contaminated food. The pork production sector has been hit hard by a series of L. monocytogenes-related food poisoning outbreaks in France. An overview of the diversity of strains circulating at all levels of the pork production chain, from pig farming (PF) to finished food products (FFP), is needed to identify the contamination routes and improve food safety. Until now, no typing data has been available on strains isolated across the entire pig and pork production chain. Here, we analyzed the population genetic structure of 687 L. monocytogenes strains isolated over the last 20 years in virtually all the French départements from three compartments of this production sector: PF, the food processing environment (FPE), and FFP. The genetic structure was described based on Multilocus sequence typing (MLST) clonal complexes (CCs). The CCs were obtained by mapping the PFGE profiles of the strains. The distribution of CCs was compared firstly between the three compartments and then with CCs obtained from 1106 strains isolated from other food production sectors in France. The predominant CCs of pig and pork strains were not equally distributed among the three compartments: the CC37, CC59, and CC77 strains, rarely found in FPE and FFP, were prevalent in PF. The two most prevalent CCs in the FPE and FFP compartments, CC9 and CC121, were rarely or never detected in PF. No CC was exclusively associated with the pork sector. Three CCs (CC5, CC6, and CC2) were considered ubiquitous, because they were observed in comparable proportions in all food production sectors. The two most prevalent CCs in all sectors were CC9 and CC121, but their distribution was disparate. CC9 was associated with meat products and food products combining several food categories, whereas CC121 was not associated with any given sector. Based on these results, CC121 is likely able to colonize a larger diversity of food products than CC9. Both CCs being associated with the food production suggests, that certain processing steps, such as slaughtering or stabilization treatments, favor their settlement and the recontamination of the food produced.

Project description:BackgroundListeria monocytogenes is the causative agent of listeriosis, a serious disease affecting both animals and humans. Here, multilocus sequence typing (MLST) was used to characterize the genetic diversity of Listeria monocytogenes strains isolated from the natural environment and animal clinical cases in Europe. The prevalence of clonal complexes (CCs) obtained was compared according to (i) the origin of isolation - clinical cases vs. natural environment - and (ii) the clinical form of animal listeriosis - rhombencephalitis vs. abortion. To this aim, two datasets were constructed. The clinical dataset consisted of 350 animal clinical isolates originating from France and Slovenia and supplemented with isolates from Switzerland and Great Britain. The natural environment dataset consisted of 253 isolates from the natural environment originating from Slovenia and supplemented with isolates from nine other European countries.ResultsFor the clinical cases, CC1, CC4-CC217 and CC412 were the most prevalent in rhombencephalitis and CC1, CC37 and CC4-CC217 in abortion. The hypervirulent CC1 and CC4-CC217 prevailed in both datasets. These results indicated that livestock is constantly exposed to hypervirulent CCs. CC1 was significantly associated with a clinical origin, whereas CC9, CC29 and CC14 were associated with the natural environment. CC1 was predominant among rhombencephalitis cases both in cattle and small ruminants, and its prevalence did not differ significantly between these two groups. A novel association of CC37 and CC6 with abortion cases was revealed.ConclusionsHere, we show that CC1 and CC4-CC217 are prevalent in isolates of environmental and animal clinical origin, suggesting that ruminants are frequently exposed to hypervirulent CCs. The presence of CC4 in two mastitis cases calls for further attention due to direct threat to the consumer. We showed several associations between CCs and the origin of isolation or clinical form of listeriosis, e.g. CC37 and CC6 with abortion. This study improves our understanding of the population structure of L. monocytogenes isolates from the natural environment and animal clinical cases. Moreover, it provides a basis for future studies aiming to determine the underlying mechanisms of phenotypic traits of interest.

Project description: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.

Project description:BACKGROUND:In a beef cattle facility an outbreak of abortions occurred over a 36-day period and included samples from two aborted (non-viable) fetuses and 21 post-abortion clinical cases. There are numerous etiologies, including clinical listeriosis. At the species level, Listeria monocytogenes is ubiquitous in cattle production environments, including soil, feed, and occasionally water sources, and is a common enteric resident of cattle and other mammals. There are four genetically distinct lineages of L. monocytogenes (I-IV), with most lineage III and IV isolates obtained from ruminants. Definitive diagnosis of L. monocytogenes as a causative agent in disease outbreaks relies upon case identification, appropriate sample collection, and laboratory confirmation. Furthermore, clearly establishing a relationship between a pathogen source and clinical disease is difficult. RESULTS:Of the two fetal and 21 clinical case submissions, 19 were positive for L. monocytogenes. Subsequent culture for L. monocytogenes from water and silage sources identified both as potential origins of infection. Using whole-genome sequencing and phylogenetic analyses, clinical, water and silage L. monocytogenes strains grouped into two of four lineages. All water and silage strains, plus 11 clinical strains placed in lineage III, with identical or nearly identical genomic sequences. The remaining eight clinical strains placed in lineage I, with seven having nearly identical sequences and one distinctly different. CONCLUSION:Three genetically distinct strains within two lineages of L. monocytogenes caused the abortion outbreak. The etiology of abortion in 11 cases was directly linked to water and silage contamination from a lineage III L. monocytogenes strain. The source of infection for the remaining abortion cases with two different strains from lineage I is unknown. This is the first report of L. monocytogenes genomics being used as part of an outbreak investigation of cattle abortion.

Dataset Information

The population structure and genetic diversity of Listeria monocytogenes ST9 strains based on genomic analysis.

Publications

The population structure and genetic diversity of <i>Listeria monocytogenes</i> ST9 strains based on genomic analysis.

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