Listeria monocytogenes isolates from ready to eat plant produce are diverse and have virulence potential
Listeria monocytogenes is sporadically detected on a range of ready to eat fresh produce lines, such as spinach and rocket, and is a threat to public health. However, little is known about the diversity of L. monocytogenes present on fresh produce and their potential pathogenicity. In this work, fif...
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description | Listeria monocytogenes is sporadically detected on a range of ready to eat fresh produce lines, such as spinach and rocket, and is a threat to public health. However, little is known about the diversity of L. monocytogenes present on fresh produce and their potential pathogenicity. In this work, fifteen Listeria monocytogenes isolates from the UK fresh produce supply chain were characterised using whole genome sequencing (WGS). Additionally, isolates were characterised based on their ability to form biofilm. Whole genome sequencing data was used to determine the sequence type of isolates based on multi-locus sequence typing (MLST), construct a core single nucleotide polymorphism (SNP) phylogeny and determine the presence of virulence and resistance associated genes. MLST revealed 9 distinct sequence types (STs) spanning 2 lineages (I & II) with one isolate belonging to the ST6 subtype, strains from which have been recently implicated in two large, food-associated L. monocytogenes outbreaks in South Africa and across Europe. Although most of the 15 isolates were different, comparison of core genome SNPs showed 4 pairs of ‘indistinguishable’ strains ( |
doi_str_mv | 10.1016/j.ijfoodmicro.2019.03.013 |
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•The Lm population in the UK leafy produce supply chain is genetically diverse•Isolates are related to epidemic strains and possess the necessary genes for disease•Biofilm production differs amongst closely related isolates•WGS provides valuable information on isolates that is of interest to stakeholders</description><identifier>ISSN: 0168-1605</identifier><identifier>EISSN: 1879-3460</identifier><identifier>DOI: 10.1016/j.ijfoodmicro.2019.03.013</identifier><identifier>PMID: 30939364</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Biofilms ; Contamination ; Food ; Food contamination ; Food microbiology ; Food processing ; Food processing industry ; Food production ; Food safety ; Fresh produce ; Gene sequencing ; Genomes ; Health risks ; Listeria ; Listeria monocytogenes ; Microorganisms ; Multilocus sequence typing ; Nonsense mutation ; Nucleotide sequence ; Outbreaks ; Pathogenicity ; Pathogens ; Phylogeny ; Polymorphism ; Public health ; Single-nucleotide polymorphism ; Spinach ; Stop codon ; Supply chains ; Virulence ; Virulence factors ; Whole genome sequencing</subject><ispartof>International journal of food microbiology, 2019-06, Vol.299, p.23-32</ispartof><rights>2019 Elsevier B.V.</rights><rights>Copyright © 2019 Elsevier B.V. All rights reserved.</rights><rights>Copyright Elsevier BV Jun 16, 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c456t-4d2f0801d072a1b33f088e85bd6e14d8cdf7b6d94fb8e2d8f221f74ae57796d53</citedby><cites>FETCH-LOGICAL-c456t-4d2f0801d072a1b33f088e85bd6e14d8cdf7b6d94fb8e2d8f221f74ae57796d53</cites><orcidid>0000-0003-3886-9222</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.ijfoodmicro.2019.03.013$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30939364$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Smith, Alva</creatorcontrib><creatorcontrib>Hearn, Jack</creatorcontrib><creatorcontrib>Taylor, Clare</creatorcontrib><creatorcontrib>Wheelhouse, Nick</creatorcontrib><creatorcontrib>Kaczmarek, Maciej</creatorcontrib><creatorcontrib>Moorhouse, Edwin</creatorcontrib><creatorcontrib>Singleton, Ian</creatorcontrib><title>Listeria monocytogenes isolates from ready to eat plant produce are diverse and have virulence potential</title><title>International journal of food microbiology</title><addtitle>Int J Food Microbiol</addtitle><description>Listeria monocytogenes is sporadically detected on a range of ready to eat fresh produce lines, such as spinach and rocket, and is a threat to public health. However, little is known about the diversity of L. monocytogenes present on fresh produce and their potential pathogenicity. In this work, fifteen Listeria monocytogenes isolates from the UK fresh produce supply chain were characterised using whole genome sequencing (WGS). Additionally, isolates were characterised based on their ability to form biofilm. Whole genome sequencing data was used to determine the sequence type of isolates based on multi-locus sequence typing (MLST), construct a core single nucleotide polymorphism (SNP) phylogeny and determine the presence of virulence and resistance associated genes. MLST revealed 9 distinct sequence types (STs) spanning 2 lineages (I & II) with one isolate belonging to the ST6 subtype, strains from which have been recently implicated in two large, food-associated L. monocytogenes outbreaks in South Africa and across Europe. Although most of the 15 isolates were different, comparison of core genome SNPs showed 4 pairs of ‘indistinguishable’ strains (<5 SNPs difference). Virulence profiling revealed that some isolates completely lacked the Listeria pathogenicity island-3 (LIPI-3) amongst other virulence factors. Investigation of the inlA gene showed that no strains in this study contained a premature stop codon (PMSC), an indicator of attenuated virulence. Assessment of biofilm production showed that isolates found in the fresh produce supply chain differ in their ability to form biofilm. This trait is considered important for L. monocytogenes to persist in environments associated with food production and processing. Overall the work indicates that a genetically diverse range of L. monocytogenes strains is present in the UK fresh produce supply chain and the virulence profiles found suggests that at least some of the strains are capable of causing human illness. Interestingly, the presence of some genetically indistinguishable isolates within the 15 isolates examined suggests that cross-contamination in the fresh produce environment does occur. These findings have useful implications in terms of food safety and for informing microbial surveillance programmes in the UK fresh produce supply chain.
•The Lm population in the UK leafy produce supply chain is genetically diverse•Isolates are related to epidemic strains and possess the necessary genes for disease•Biofilm production differs amongst closely related isolates•WGS provides valuable information on isolates that is of interest to stakeholders</description><subject>Biofilms</subject><subject>Contamination</subject><subject>Food</subject><subject>Food contamination</subject><subject>Food microbiology</subject><subject>Food processing</subject><subject>Food processing industry</subject><subject>Food production</subject><subject>Food safety</subject><subject>Fresh produce</subject><subject>Gene sequencing</subject><subject>Genomes</subject><subject>Health risks</subject><subject>Listeria</subject><subject>Listeria monocytogenes</subject><subject>Microorganisms</subject><subject>Multilocus sequence typing</subject><subject>Nonsense mutation</subject><subject>Nucleotide sequence</subject><subject>Outbreaks</subject><subject>Pathogenicity</subject><subject>Pathogens</subject><subject>Phylogeny</subject><subject>Polymorphism</subject><subject>Public health</subject><subject>Single-nucleotide polymorphism</subject><subject>Spinach</subject><subject>Stop codon</subject><subject>Supply chains</subject><subject>Virulence</subject><subject>Virulence factors</subject><subject>Whole genome sequencing</subject><issn>0168-1605</issn><issn>1879-3460</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNqNkU-PFCEQxYnRuLOrX8FgvHjpln8N9NFMVtdkEi96JnRTuHS6mxHoSebby2RWYzx5gSL8qurlPYTeUtJSQuWHqQ2Tj9EtYUyxZYT2LeEtofwZ2lGt-oYLSZ6jXWV1QyXpbtBtzhMhpOOcvEQ3nPS851Ls0OMh5AIpWLzENY7nEn_AChmHHGdbauFTXHAC6864RAy24ONs13qm6LYRsE2AXThByrVeHX60J8CnkLYZ1vp9jAXWEuz8Cr3wds7w-um-Q98_3X_bPzSHr5-_7D8emlF0sjTCMU80oY4oZunAeX1p0N3gJFDh9Oi8GqTrhR80MKc9Y9QrYaFTqpeu43fo_XVuFfhzg1zMEvIIcxUNccuGMcKklEypir77B53iltaqrlJMCaqFvgzsr1T1OucE3hxTWGw6G0rMJQ4zmb_iMJc4DOGmxlF73zxt2IYF3J_O3_5XYH8FoFpyCpBMHsPFOBcSjMW4GP5jzS-34KMV</recordid><startdate>20190616</startdate><enddate>20190616</enddate><creator>Smith, Alva</creator><creator>Hearn, Jack</creator><creator>Taylor, Clare</creator><creator>Wheelhouse, Nick</creator><creator>Kaczmarek, Maciej</creator><creator>Moorhouse, Edwin</creator><creator>Singleton, Ian</creator><general>Elsevier B.V</general><general>Elsevier BV</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QO</scope><scope>7QR</scope><scope>7T7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-3886-9222</orcidid></search><sort><creationdate>20190616</creationdate><title>Listeria monocytogenes isolates from ready to eat plant produce are diverse and have virulence potential</title><author>Smith, Alva ; Hearn, Jack ; Taylor, Clare ; Wheelhouse, Nick ; Kaczmarek, Maciej ; Moorhouse, Edwin ; Singleton, Ian</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c456t-4d2f0801d072a1b33f088e85bd6e14d8cdf7b6d94fb8e2d8f221f74ae57796d53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Biofilms</topic><topic>Contamination</topic><topic>Food</topic><topic>Food contamination</topic><topic>Food microbiology</topic><topic>Food processing</topic><topic>Food processing industry</topic><topic>Food production</topic><topic>Food safety</topic><topic>Fresh produce</topic><topic>Gene sequencing</topic><topic>Genomes</topic><topic>Health risks</topic><topic>Listeria</topic><topic>Listeria monocytogenes</topic><topic>Microorganisms</topic><topic>Multilocus sequence typing</topic><topic>Nonsense mutation</topic><topic>Nucleotide sequence</topic><topic>Outbreaks</topic><topic>Pathogenicity</topic><topic>Pathogens</topic><topic>Phylogeny</topic><topic>Polymorphism</topic><topic>Public health</topic><topic>Single-nucleotide polymorphism</topic><topic>Spinach</topic><topic>Stop codon</topic><topic>Supply chains</topic><topic>Virulence</topic><topic>Virulence factors</topic><topic>Whole genome sequencing</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Smith, Alva</creatorcontrib><creatorcontrib>Hearn, Jack</creatorcontrib><creatorcontrib>Taylor, Clare</creatorcontrib><creatorcontrib>Wheelhouse, Nick</creatorcontrib><creatorcontrib>Kaczmarek, Maciej</creatorcontrib><creatorcontrib>Moorhouse, Edwin</creatorcontrib><creatorcontrib>Singleton, Ian</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>International journal of food microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Smith, Alva</au><au>Hearn, Jack</au><au>Taylor, Clare</au><au>Wheelhouse, Nick</au><au>Kaczmarek, Maciej</au><au>Moorhouse, Edwin</au><au>Singleton, Ian</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Listeria monocytogenes isolates from ready to eat plant produce are diverse and have virulence potential</atitle><jtitle>International journal of food microbiology</jtitle><addtitle>Int J Food Microbiol</addtitle><date>2019-06-16</date><risdate>2019</risdate><volume>299</volume><spage>23</spage><epage>32</epage><pages>23-32</pages><issn>0168-1605</issn><eissn>1879-3460</eissn><abstract>Listeria monocytogenes is sporadically detected on a range of ready to eat fresh produce lines, such as spinach and rocket, and is a threat to public health. However, little is known about the diversity of L. monocytogenes present on fresh produce and their potential pathogenicity. In this work, fifteen Listeria monocytogenes isolates from the UK fresh produce supply chain were characterised using whole genome sequencing (WGS). Additionally, isolates were characterised based on their ability to form biofilm. Whole genome sequencing data was used to determine the sequence type of isolates based on multi-locus sequence typing (MLST), construct a core single nucleotide polymorphism (SNP) phylogeny and determine the presence of virulence and resistance associated genes. MLST revealed 9 distinct sequence types (STs) spanning 2 lineages (I & II) with one isolate belonging to the ST6 subtype, strains from which have been recently implicated in two large, food-associated L. monocytogenes outbreaks in South Africa and across Europe. Although most of the 15 isolates were different, comparison of core genome SNPs showed 4 pairs of ‘indistinguishable’ strains (<5 SNPs difference). Virulence profiling revealed that some isolates completely lacked the Listeria pathogenicity island-3 (LIPI-3) amongst other virulence factors. Investigation of the inlA gene showed that no strains in this study contained a premature stop codon (PMSC), an indicator of attenuated virulence. Assessment of biofilm production showed that isolates found in the fresh produce supply chain differ in their ability to form biofilm. This trait is considered important for L. monocytogenes to persist in environments associated with food production and processing. Overall the work indicates that a genetically diverse range of L. monocytogenes strains is present in the UK fresh produce supply chain and the virulence profiles found suggests that at least some of the strains are capable of causing human illness. Interestingly, the presence of some genetically indistinguishable isolates within the 15 isolates examined suggests that cross-contamination in the fresh produce environment does occur. These findings have useful implications in terms of food safety and for informing microbial surveillance programmes in the UK fresh produce supply chain.
•The Lm population in the UK leafy produce supply chain is genetically diverse•Isolates are related to epidemic strains and possess the necessary genes for disease•Biofilm production differs amongst closely related isolates•WGS provides valuable information on isolates that is of interest to stakeholders</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>30939364</pmid><doi>10.1016/j.ijfoodmicro.2019.03.013</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0003-3886-9222</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Biofilms Contamination Food Food contamination Food microbiology Food processing Food processing industry Food production Food safety Fresh produce Gene sequencing Genomes Health risks Listeria Listeria monocytogenes Microorganisms Multilocus sequence typing Nonsense mutation Nucleotide sequence Outbreaks Pathogenicity Pathogens Phylogeny Polymorphism Public health Single-nucleotide polymorphism Spinach Stop codon Supply chains Virulence Virulence factors Whole genome sequencing |
title | Listeria monocytogenes isolates from ready to eat plant produce are diverse and have virulence potential |
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