Whole-Genome Sequencing-Based Characterization of 100 <named-content content-type="genus-species">Listeria monocytogenes</named-content> Isolates Collected from Food Processing Environments over a Four-Year Period

ABSTRACT Listeria monocytogenes 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, lead...

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Autores principales: Daniel Hurley, Laura Luque-Sastre, Craig T. Parker, Steven Huynh, Athmanya K. Eshwar, Scott V. Nguyen, Nicholas Andrews, Alexandra Moura, Edward M. Fox, Kieran Jordan, Angelika Lehner, Roger Stephan, Séamus Fanning
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:79737b259c974f9b900a8c9d96b212d02021-11-15T15:22:27ZWhole-Genome Sequencing-Based Characterization of 100 <named-content content-type="genus-species">Listeria monocytogenes</named-content> Isolates Collected from Food Processing Environments over a Four-Year Period10.1128/mSphere.00252-192379-5042https://doaj.org/article/79737b259c974f9b900a8c9d96b212d02019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00252-19https://doaj.org/toc/2379-5042ABSTRACT Listeria monocytogenes 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 L. monocytogenes isolates collected from three food processing environments. These WGS data from environmental and food isolates were analyzed to (i) assess the genomic diversity of L. monocytogenes, (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 in vivo pathogenicity of selected L. monocytogenes isolates carrying different virulence genotypes. The predominant L. monocytogenes 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 emrC followed by bcrABC, qacH-Tn6188, and qacC. The L. monocytogenes major virulence factor inlA was truncated in 31% of the isolates, and only one environmental isolate (L. monocytogenes CFS086) harbored all major virulence factors, including Listeria 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 L. monocytogenes isolates assayed. Higher embryo survival rates were observed following infection with unknown virulence potential (20%) and putatively hypovirulent (53 to 83%) L. monocytogenes isolates showing predicted pathogenic phenotypes inferred from virulence genotypes. IMPORTANCE This study extends current understanding of the genetic diversity among L. monocytogenes 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 L. monocytogenes 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 L. monocytogenes.Daniel HurleyLaura Luque-SastreCraig T. ParkerSteven HuynhAthmanya K. EshwarScott V. NguyenNicholas AndrewsAlexandra MouraEdward M. FoxKieran JordanAngelika LehnerRoger StephanSéamus FanningAmerican Society for MicrobiologyarticleListeria monocytogenesfoodborne pathogenspersistencevirulenceMicrobiologyQR1-502ENmSphere, Vol 4, Iss 4 (2019)
institution DOAJ
collection DOAJ
language EN
topic Listeria monocytogenes
foodborne pathogens
persistence
virulence
Microbiology
QR1-502
spellingShingle Listeria monocytogenes
foodborne pathogens
persistence
virulence
Microbiology
QR1-502
Daniel Hurley
Laura Luque-Sastre
Craig T. Parker
Steven Huynh
Athmanya K. Eshwar
Scott V. Nguyen
Nicholas Andrews
Alexandra Moura
Edward M. Fox
Kieran Jordan
Angelika Lehner
Roger Stephan
Séamus Fanning
Whole-Genome Sequencing-Based Characterization of 100 <named-content content-type="genus-species">Listeria monocytogenes</named-content> Isolates Collected from Food Processing Environments over a Four-Year Period
description ABSTRACT Listeria monocytogenes 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 L. monocytogenes isolates collected from three food processing environments. These WGS data from environmental and food isolates were analyzed to (i) assess the genomic diversity of L. monocytogenes, (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 in vivo pathogenicity of selected L. monocytogenes isolates carrying different virulence genotypes. The predominant L. monocytogenes 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 emrC followed by bcrABC, qacH-Tn6188, and qacC. The L. monocytogenes major virulence factor inlA was truncated in 31% of the isolates, and only one environmental isolate (L. monocytogenes CFS086) harbored all major virulence factors, including Listeria 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 L. monocytogenes isolates assayed. Higher embryo survival rates were observed following infection with unknown virulence potential (20%) and putatively hypovirulent (53 to 83%) L. monocytogenes isolates showing predicted pathogenic phenotypes inferred from virulence genotypes. IMPORTANCE This study extends current understanding of the genetic diversity among L. monocytogenes 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 L. monocytogenes 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 L. monocytogenes.
format article
author Daniel Hurley
Laura Luque-Sastre
Craig T. Parker
Steven Huynh
Athmanya K. Eshwar
Scott V. Nguyen
Nicholas Andrews
Alexandra Moura
Edward M. Fox
Kieran Jordan
Angelika Lehner
Roger Stephan
Séamus Fanning
author_facet Daniel Hurley
Laura Luque-Sastre
Craig T. Parker
Steven Huynh
Athmanya K. Eshwar
Scott V. Nguyen
Nicholas Andrews
Alexandra Moura
Edward M. Fox
Kieran Jordan
Angelika Lehner
Roger Stephan
Séamus Fanning
author_sort Daniel Hurley
title Whole-Genome Sequencing-Based Characterization of 100 <named-content content-type="genus-species">Listeria monocytogenes</named-content> Isolates Collected from Food Processing Environments over a Four-Year Period
title_short Whole-Genome Sequencing-Based Characterization of 100 <named-content content-type="genus-species">Listeria monocytogenes</named-content> Isolates Collected from Food Processing Environments over a Four-Year Period
title_full Whole-Genome Sequencing-Based Characterization of 100 <named-content content-type="genus-species">Listeria monocytogenes</named-content> Isolates Collected from Food Processing Environments over a Four-Year Period
title_fullStr Whole-Genome Sequencing-Based Characterization of 100 <named-content content-type="genus-species">Listeria monocytogenes</named-content> Isolates Collected from Food Processing Environments over a Four-Year Period
title_full_unstemmed Whole-Genome Sequencing-Based Characterization of 100 <named-content content-type="genus-species">Listeria monocytogenes</named-content> Isolates Collected from Food Processing Environments over a Four-Year Period
title_sort whole-genome sequencing-based characterization of 100 <named-content content-type="genus-species">listeria monocytogenes</named-content> isolates collected from food processing environments over a four-year period
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/79737b259c974f9b900a8c9d96b212d0
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