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Whole-genome sequencing-based characterization of 100 Listeria monocytogenes isolates collected from food processing environments over a four-year period


Hurley, Daniel; Luque-Sastre, Laura; Parker, Craig T; Huynh, Steven; Eshwar, Athmanya K; Nguyen, Scott V; Andrews, Nicholas; Moura, Alexandra; Fox, Edward M; Jordan, Kieran; Lehner, Angelika; Stephan, Roger; Fanning, Séamus (2019). Whole-genome sequencing-based characterization of 100 Listeria monocytogenes isolates collected from food processing environments over a four-year period. mSphere, 4(4):e00252-19.

Abstract

<jats:named-content content-type="genus-species">Listeria monocytogenes</jats:named-content> is frequently found in foods and processing facilities, where it can persist, creating concerns for the food industry. Its ability to survive under a wide range of environmental conditions enhances the potential for cross-contamination of the final food products, leading to possible outbreaks of listeriosis. In this study, whole-genome sequencing (WGS) was applied as a tool to characterize and track 100 <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> isolates collected from three food processing environments. These WGS data from environmental and food isolates were analyzed to (i) assess the genomic diversity of <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content>, (ii) identify possible source(s) of contamination, cross-contamination routes, and persistence, (iii) detect absence/presence of antimicrobial resistance-encoding genes, (iv) assess virulence genotypes, and (v) explore <jats:italic>in vivo</jats:italic> pathogenicity of selected <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> isolates carrying different virulence genotypes. The predominant <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> sublineages (SLs) identified were SL101 (21%), SL9 (17%), SL121 (12%), and SL5 (12%). Benzalkonium chloride (BC) tolerance-encoding genes were found in 62% of these isolates, a value that increased to 73% among putative persistent subgroups. The most prevalent gene was <jats:italic>emrC</jats:italic> followed by <jats:italic>bcrABC</jats:italic>, <jats:italic>qacH</jats:italic>-Tn<jats:italic>6188</jats:italic>, and <jats:italic>qacC.</jats:italic> The <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> major virulence factor <jats:italic>inlA</jats:italic> was truncated in 31% of the isolates, and only one environmental isolate (<jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> CFS086) harbored all major virulence factors, including <jats:italic>Listeria</jats:italic> pathogenicity island 4 (LIPI-4), which has been shown to confer hypervirulence. A zebrafish embryo infection model showed a low (3%) embryo survival rate for all putatively hypervirulent <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> isolates assayed. Higher embryo survival rates were observed following infection with unknown virulence potential (20%) and putatively hypovirulent (53 to 83%) <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> isolates showing predicted pathogenic phenotypes inferred from virulence genotypes.
<jats:bold>IMPORTANCE</jats:bold> This study extends current understanding of the genetic diversity among <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> from various food products and food processing environments. Application of WGS-based strategies facilitated tracking of this pathogen of importance to human health along the production chain while providing insights into the pathogenic potential for some of the <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> isolates recovered. These analyses enabled the grouping of selected isolates into three putative virulence categories according to their genotypes along with informing selection for phenotypic assessment of their pathogenicity using the zebrafish embryo infection model. It has also facilitated the identification of those isolates with genes conferring tolerance to commercially used biocides. Findings from this study highlight the potential for the application of WGS as a proactive tool to support food safety controls as applied to <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content>.

Abstract

<jats:named-content content-type="genus-species">Listeria monocytogenes</jats:named-content> is frequently found in foods and processing facilities, where it can persist, creating concerns for the food industry. Its ability to survive under a wide range of environmental conditions enhances the potential for cross-contamination of the final food products, leading to possible outbreaks of listeriosis. In this study, whole-genome sequencing (WGS) was applied as a tool to characterize and track 100 <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> isolates collected from three food processing environments. These WGS data from environmental and food isolates were analyzed to (i) assess the genomic diversity of <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content>, (ii) identify possible source(s) of contamination, cross-contamination routes, and persistence, (iii) detect absence/presence of antimicrobial resistance-encoding genes, (iv) assess virulence genotypes, and (v) explore <jats:italic>in vivo</jats:italic> pathogenicity of selected <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> isolates carrying different virulence genotypes. The predominant <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> sublineages (SLs) identified were SL101 (21%), SL9 (17%), SL121 (12%), and SL5 (12%). Benzalkonium chloride (BC) tolerance-encoding genes were found in 62% of these isolates, a value that increased to 73% among putative persistent subgroups. The most prevalent gene was <jats:italic>emrC</jats:italic> followed by <jats:italic>bcrABC</jats:italic>, <jats:italic>qacH</jats:italic>-Tn<jats:italic>6188</jats:italic>, and <jats:italic>qacC.</jats:italic> The <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> major virulence factor <jats:italic>inlA</jats:italic> was truncated in 31% of the isolates, and only one environmental isolate (<jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> CFS086) harbored all major virulence factors, including <jats:italic>Listeria</jats:italic> pathogenicity island 4 (LIPI-4), which has been shown to confer hypervirulence. A zebrafish embryo infection model showed a low (3%) embryo survival rate for all putatively hypervirulent <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> isolates assayed. Higher embryo survival rates were observed following infection with unknown virulence potential (20%) and putatively hypovirulent (53 to 83%) <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> isolates showing predicted pathogenic phenotypes inferred from virulence genotypes.
<jats:bold>IMPORTANCE</jats:bold> This study extends current understanding of the genetic diversity among <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> from various food products and food processing environments. Application of WGS-based strategies facilitated tracking of this pathogen of importance to human health along the production chain while providing insights into the pathogenic potential for some of the <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content> isolates recovered. These analyses enabled the grouping of selected isolates into three putative virulence categories according to their genotypes along with informing selection for phenotypic assessment of their pathogenicity using the zebrafish embryo infection model. It has also facilitated the identification of those isolates with genes conferring tolerance to commercially used biocides. Findings from this study highlight the potential for the application of WGS as a proactive tool to support food safety controls as applied to <jats:named-content content-type="genus-species">L. monocytogenes</jats:named-content>.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:05 Vetsuisse Faculty > Institute of Food Safety and Hygiene
Dewey Decimal Classification:570 Life sciences; biology
610 Medicine & health
Uncontrolled Keywords:Listeria monocytogenes; foodborne pathogens; persistence; virulence
Language:English
Date:7 August 2019
Deposited On:14 Feb 2020 15:46
Last Modified:15 Feb 2020 19:06
Publisher:American Society for Microbiology
ISSN:2379-5042
OA Status:Gold
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1128/msphere.00252-19
PubMed ID:31391275

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