Whole-Genome Sequencing Reveals Multiple Subpopulations of Dominant and Persistent Lineage I Isolates of <i>Listeria monocytogenes</i> in Two Meat Processing Facilities during 2011–2015
<i>Listeria monocytogenes</i> 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 <i>L. monocytogenes</i> is well-described...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-05-01
|
| Series: | Microorganisms |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2076-2607/10/5/1070 |
| _version_ | 1797497613118865408 |
|---|---|
| author | Elton Burnett Zuzana Kucerova Molly Freeman Sophia Kathariou Jessica Chen Monica Smikle |
| author_facet | Elton Burnett Zuzana Kucerova Molly Freeman Sophia Kathariou Jessica Chen Monica Smikle |
| author_sort | Elton Burnett |
| collection | DOAJ |
| description | <i>Listeria monocytogenes</i> 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 <i>L. monocytogenes</i> 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 <i>L. monocytogenes</i> 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 <i>inlA</i> and the <i>LIPI-3</i> cluster were detected in multiple isolates, along with the stress survival islet cluster-1 (SSI-1), and benzalkonium (<i>bcrABC</i>) and cadmium (<i>cad1, cad2, cad4</i>) 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 <i>L. monocytogenes</i>, and/or constant re-entry of the pathogens into the facilities from common sources. These findings highlight the ability of lineage I isolates of <i>L. monocytogenes</i> 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. |
| first_indexed | 2024-03-10T03:21:44Z |
| format | Article |
| id | doaj.art-0cf56a0536514b4ebb5b9c2395c1c5e2 |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-10T03:21:44Z |
| publishDate | 2022-05-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-0cf56a0536514b4ebb5b9c2395c1c5e22023-11-23T12:17:24ZengMDPI AGMicroorganisms2076-26072022-05-01105107010.3390/microorganisms10051070Whole-Genome Sequencing Reveals Multiple Subpopulations of Dominant and Persistent Lineage I Isolates of <i>Listeria monocytogenes</i> in Two Meat Processing Facilities during 2011–2015Elton Burnett0Zuzana Kucerova1Molly Freeman2Sophia Kathariou3Jessica Chen4Monica Smikle5Institute of Parasitology, McGill University, 2111 Lakeshore Road, Montreal, QC H9X 3V9, CanadaCenters for Disease Control and Prevention (CDC), 1600 Clifton Road, Atlanta, GA 30329, USACenters for Disease Control and Prevention (CDC), 1600 Clifton Road, Atlanta, GA 30329, USADepartment of Food, Bioprocessing and Nutrition Sciences, North Carolina State University, Raleigh, NC 27695, USACenters for Disease Control and Prevention (CDC), 1600 Clifton Road, Atlanta, GA 30329, USADepartment of Microbiology, University of the West Indies, Mona, Kingston 7, Jamaica<i>Listeria monocytogenes</i> 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 <i>L. monocytogenes</i> 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 <i>L. monocytogenes</i> 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 <i>inlA</i> and the <i>LIPI-3</i> cluster were detected in multiple isolates, along with the stress survival islet cluster-1 (SSI-1), and benzalkonium (<i>bcrABC</i>) and cadmium (<i>cad1, cad2, cad4</i>) 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 <i>L. monocytogenes</i>, and/or constant re-entry of the pathogens into the facilities from common sources. These findings highlight the ability of lineage I isolates of <i>L. monocytogenes</i> 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.https://www.mdpi.com/2076-2607/10/5/1070<i>Listeria monocytogenes</i>lineage IMLSTclonal complexPFGE |
| spellingShingle | Elton Burnett Zuzana Kucerova Molly Freeman Sophia Kathariou Jessica Chen Monica Smikle Whole-Genome Sequencing Reveals Multiple Subpopulations of Dominant and Persistent Lineage I Isolates of <i>Listeria monocytogenes</i> in Two Meat Processing Facilities during 2011–2015 Microorganisms <i>Listeria monocytogenes</i> lineage I MLST clonal complex PFGE |
| title | Whole-Genome Sequencing Reveals Multiple Subpopulations of Dominant and Persistent Lineage I Isolates of <i>Listeria monocytogenes</i> in Two Meat Processing Facilities during 2011–2015 |
| title_full | Whole-Genome Sequencing Reveals Multiple Subpopulations of Dominant and Persistent Lineage I Isolates of <i>Listeria monocytogenes</i> in Two Meat Processing Facilities during 2011–2015 |
| title_fullStr | Whole-Genome Sequencing Reveals Multiple Subpopulations of Dominant and Persistent Lineage I Isolates of <i>Listeria monocytogenes</i> in Two Meat Processing Facilities during 2011–2015 |
| title_full_unstemmed | Whole-Genome Sequencing Reveals Multiple Subpopulations of Dominant and Persistent Lineage I Isolates of <i>Listeria monocytogenes</i> in Two Meat Processing Facilities during 2011–2015 |
| title_short | Whole-Genome Sequencing Reveals Multiple Subpopulations of Dominant and Persistent Lineage I Isolates of <i>Listeria monocytogenes</i> in Two Meat Processing Facilities during 2011–2015 |
| title_sort | whole genome sequencing reveals multiple subpopulations of dominant and persistent lineage i isolates of i listeria monocytogenes i in two meat processing facilities during 2011 2015 |
| topic | <i>Listeria monocytogenes</i> lineage I MLST clonal complex PFGE |
| url | https://www.mdpi.com/2076-2607/10/5/1070 |
| work_keys_str_mv | AT eltonburnett wholegenomesequencingrevealsmultiplesubpopulationsofdominantandpersistentlineageiisolatesofilisteriamonocytogenesiintwomeatprocessingfacilitiesduring20112015 AT zuzanakucerova wholegenomesequencingrevealsmultiplesubpopulationsofdominantandpersistentlineageiisolatesofilisteriamonocytogenesiintwomeatprocessingfacilitiesduring20112015 AT mollyfreeman wholegenomesequencingrevealsmultiplesubpopulationsofdominantandpersistentlineageiisolatesofilisteriamonocytogenesiintwomeatprocessingfacilitiesduring20112015 AT sophiakathariou wholegenomesequencingrevealsmultiplesubpopulationsofdominantandpersistentlineageiisolatesofilisteriamonocytogenesiintwomeatprocessingfacilitiesduring20112015 AT jessicachen wholegenomesequencingrevealsmultiplesubpopulationsofdominantandpersistentlineageiisolatesofilisteriamonocytogenesiintwomeatprocessingfacilitiesduring20112015 AT monicasmikle wholegenomesequencingrevealsmultiplesubpopulationsofdominantandpersistentlineageiisolatesofilisteriamonocytogenesiintwomeatprocessingfacilitiesduring20112015 |