DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Listeria monocytogenes in Stone Fruits Linked to a Multistate Outbreak: Enumeration of Cells and Whole-Genome Sequencing

Abstract

In 2014, the identification of stone fruits contaminated with led to the subsequent identification of a multistate outbreak. Simultaneous detection and enumeration of L. monocytogenes were performed on 105 fruits, each weighing 127 to 145 g, collected from 7 contaminated lots. The results showed that 53.3% of the fruits yielded L. monocytogenes (lower limit of detection, 5 CFU/fruit), and the levels ranged from 5 to 2,850 CFU/fruit, with a geometric mean of 11.3 CFU/fruit (0.1 CFU/g of fruit). Two serotypes, IVb-v1 and 1/2b, were identified by a combination of PCR- and antiserum-based serotyping among isolates from fruits and their packing environment; certain fruits contained a mixture of both serotypes. Single nucleotide polymorphism (SNP)-based whole-genome sequencing (WGS) analysis clustered isolates from two case-patients with the serotype IVb-v1 isolates and distinguished outbreak-associated isolates from pulsed-field gel electrophoresis (PFGE)-matched, but epidemiologically unrelated, clinical isolates. The outbreak-associated isolates differed by up to 42 SNPs. All but one serotype 1/2b isolate formed another WGS cluster and differed by up to 17 SNPs. Fully closed genomes of isolates from the stone fruits were used as references to maximize the resolution and to increase our confidence in prophage analysis. Putative prophages were conserved among isolates of eachmore » WGS cluster. All serotype IVb-v1 isolates belonged to singleton sequence type 382 (ST382); all but one serotype 1/2b isolate belonged to clonal complex 5.« less

Authors:
 [1];  [2];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [3];  [4];  [4];  [1];  [1];  [1];  [1];  [1] more »;  [2];  [1];  [1] « less
  1. U.S. Food and Drug Administration (FDA), College Park, MD (United States). Center for Food Safety and Applied Nutrition
  2. U.S. Food and Drug Administration (FDA), Laurel, MD (United States). Center for Food Safety and Applied Nutrition
  3. Newcastle Univ., Newcastle upon Tyne (United Kingdom)
  4. U.S. Food and Drug Administration (FDA), Alameda, CA (United States). Office of Regulatory Affairs
Publication Date:
Research Org.:
Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1626065
Grant/Contract Number:  
SC0014664
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 82; Journal Issue: 24; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biotechnology & Applied Microbiology; Microbiology

Citation Formats

Chen, Yi, Burall, Laurel S., Luo, Yan, Timme, Ruth, Melka, David, Muruvanda, Tim, Payne, Justin, Wang, Charles, Kastanis, George, Maounounen-Laasri, Anna, De Jesus, Antonio J., Curry, Phillip E., Stones, Robert, K'Aluoch, Okumu, Liu, Eileen, Salter, Monique, Hammack, Thomas S., Evans, Peter S., Parish, Mickey, Allard, Marc W., Datta, Atin, Strain, Errol A., and Brown, Eric W. Listeria monocytogenes in Stone Fruits Linked to a Multistate Outbreak: Enumeration of Cells and Whole-Genome Sequencing. United States: N. p., 2016. Web. doi:10.1128/aem.01486-16.
Chen, Yi, Burall, Laurel S., Luo, Yan, Timme, Ruth, Melka, David, Muruvanda, Tim, Payne, Justin, Wang, Charles, Kastanis, George, Maounounen-Laasri, Anna, De Jesus, Antonio J., Curry, Phillip E., Stones, Robert, K'Aluoch, Okumu, Liu, Eileen, Salter, Monique, Hammack, Thomas S., Evans, Peter S., Parish, Mickey, Allard, Marc W., Datta, Atin, Strain, Errol A., & Brown, Eric W. Listeria monocytogenes in Stone Fruits Linked to a Multistate Outbreak: Enumeration of Cells and Whole-Genome Sequencing. United States. https://doi.org/10.1128/aem.01486-16
Chen, Yi, Burall, Laurel S., Luo, Yan, Timme, Ruth, Melka, David, Muruvanda, Tim, Payne, Justin, Wang, Charles, Kastanis, George, Maounounen-Laasri, Anna, De Jesus, Antonio J., Curry, Phillip E., Stones, Robert, K'Aluoch, Okumu, Liu, Eileen, Salter, Monique, Hammack, Thomas S., Evans, Peter S., Parish, Mickey, Allard, Marc W., Datta, Atin, Strain, Errol A., and Brown, Eric W. Mon . "Listeria monocytogenes in Stone Fruits Linked to a Multistate Outbreak: Enumeration of Cells and Whole-Genome Sequencing". United States. https://doi.org/10.1128/aem.01486-16. https://www.osti.gov/servlets/purl/1626065.
@article{osti_1626065,
title = {Listeria monocytogenes in Stone Fruits Linked to a Multistate Outbreak: Enumeration of Cells and Whole-Genome Sequencing},
author = {Chen, Yi and Burall, Laurel S. and Luo, Yan and Timme, Ruth and Melka, David and Muruvanda, Tim and Payne, Justin and Wang, Charles and Kastanis, George and Maounounen-Laasri, Anna and De Jesus, Antonio J. and Curry, Phillip E. and Stones, Robert and K'Aluoch, Okumu and Liu, Eileen and Salter, Monique and Hammack, Thomas S. and Evans, Peter S. and Parish, Mickey and Allard, Marc W. and Datta, Atin and Strain, Errol A. and Brown, Eric W.},
abstractNote = {In 2014, the identification of stone fruits contaminated with led to the subsequent identification of a multistate outbreak. Simultaneous detection and enumeration of L. monocytogenes were performed on 105 fruits, each weighing 127 to 145 g, collected from 7 contaminated lots. The results showed that 53.3% of the fruits yielded L. monocytogenes (lower limit of detection, 5 CFU/fruit), and the levels ranged from 5 to 2,850 CFU/fruit, with a geometric mean of 11.3 CFU/fruit (0.1 CFU/g of fruit). Two serotypes, IVb-v1 and 1/2b, were identified by a combination of PCR- and antiserum-based serotyping among isolates from fruits and their packing environment; certain fruits contained a mixture of both serotypes. Single nucleotide polymorphism (SNP)-based whole-genome sequencing (WGS) analysis clustered isolates from two case-patients with the serotype IVb-v1 isolates and distinguished outbreak-associated isolates from pulsed-field gel electrophoresis (PFGE)-matched, but epidemiologically unrelated, clinical isolates. The outbreak-associated isolates differed by up to 42 SNPs. All but one serotype 1/2b isolate formed another WGS cluster and differed by up to 17 SNPs. Fully closed genomes of isolates from the stone fruits were used as references to maximize the resolution and to increase our confidence in prophage analysis. Putative prophages were conserved among isolates of each WGS cluster. All serotype IVb-v1 isolates belonged to singleton sequence type 382 (ST382); all but one serotype 1/2b isolate belonged to clonal complex 5.},
doi = {10.1128/aem.01486-16},
journal = {Applied and Environmental Microbiology},
number = 24,
volume = 82,
place = {United States},
year = {Mon Nov 21 00:00:00 EST 2016},
month = {Mon Nov 21 00:00:00 EST 2016}
}

Works referenced in this record:

Prophages in Listeria monocytogenes Contain Single-Nucleotide Polymorphisms That Differentiate Outbreak Clones within Epidemic Clones
journal, February 2008

  • Chen, Y.; Knabel, S. J.
  • Journal of Clinical Microbiology, Vol. 46, Issue 4
  • DOI: 10.1128/JCM.01873-07

PulseNet standardized protocol for subtyping Listeria monocytogenes by macrorestriction and pulsed-field gel electrophoresis
journal, April 2001


REBASE—a database for DNA restriction and modification: enzymes, genes and genomes
journal, October 2009

  • Roberts, Richard J.; Vincze, Tamas; Posfai, Janos
  • Nucleic Acids Research, Vol. 38, Issue suppl_1
  • DOI: 10.1093/nar/gkp874

Fully Assembled Genome Sequence for Salmonella enterica subsp. enterica Serovar Javiana CFSAN001992
journal, February 2013


Ultrafast and memory-efficient alignment of short DNA sequences to the human genome
journal, January 2009


KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000

  • Kanehisa, Minoru; Goto, Susumu
  • Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
  • DOI: 10.1093/nar/28.1.27

Implementation of Nationwide Real-time Whole-genome Sequencing to Enhance Listeriosis Outbreak Detection and Investigation
journal, April 2016

  • Jackson, Brendan R.; Tarr, Cheryl; Strain, Errol
  • Clinical Infectious Diseases, Vol. 63, Issue 3
  • DOI: 10.1093/cid/ciw242

Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data
journal, May 2013

  • Chin, Chen-Shan; Alexander, David H.; Marks, Patrick
  • Nature Methods, Vol. 10, Issue 6
  • DOI: 10.1038/nmeth.2474

Multistate outbreak of listeriosis caused by imported cheese and evidence of cross-contamination of other cheeses, USA, 2012
journal, June 2015


Multi-Virulence-Locus Sequence Typing Clarifies Epidemiology of Recent Listeriosis Outbreaks in the United States
journal, October 2005


High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak
journal, January 2010


VarScan: variant detection in massively parallel sequencing of individual and pooled samples
journal, June 2009


Short-term genome evolution of Listeria monocytogenes in a non-controlled environment
journal, January 2008


Novel Epidemic Clones of Listeria monocytogenes , United States, 2011
journal, January 2013

  • Lomonaco, Sara; Verghese, Bindhu; Gerner-Smidt, Peter
  • Emerging Infectious Diseases, Vol. 19, Issue 1
  • DOI: 10.3201/eid1901.121167

A small outbreak of listeriosis potentially linked to the consumption of imitation crab meat
journal, August 2000


Statistics review 9: One-way analysis of variance
journal, January 2004

  • Bewick, Viv; Cheek, Liz; Ball, Jonathan
  • Critical Care, Vol. 8, Issue 2, p. 130
  • DOI: 10.1186/cc2836

Prevalence and Level of Listeria monocytogenes in Ice Cream Linked to a Listeriosis Outbreak in the United States
journal, November 2016


Two Outbreaks of Listeria monocytogenes Infection, Northern Spain
journal, December 2014

  • Pérez-Trallero, Emilio; Zigorraga, Carmen; Artieda, Junkal
  • Emerging Infectious Diseases, Vol. 20, Issue 12
  • DOI: 10.3201/eid2012.140993

The Pfam protein families database: towards a more sustainable future
journal, December 2015

  • Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y.
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1344

Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity
journal, February 2016

  • Maury, Mylène M.; Tsai, Yu-Huan; Charlier, Caroline
  • Nature Genetics, Vol. 48, Issue 3
  • DOI: 10.1038/ng.3501

CFSAN SNP Pipeline: an automated method for constructing SNP matrices from next-generation sequence data
journal, January 2015

  • Davis, Steve; Pettengill, James B.; Luo, Yan
  • PeerJ Computer Science, Vol. 1
  • DOI: 10.7717/peerj-cs.20

Whole genome sequencing as a tool to investigate a cluster of seven cases of listeriosis in Austria and Germany, 2011–2013
journal, May 2014

  • Schmid, D.; Allerberger, F.; Huhulescu, S.
  • Clinical Microbiology and Infection, Vol. 20, Issue 5
  • DOI: 10.1111/1469-0691.12638

MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004


Multistate Outbreak of Listeriosis Associated with Cantaloupe
journal, September 2013

  • McCollum, Jeffrey T.; Cronquist, Alicia B.; Silk, Benjamin J.
  • New England Journal of Medicine, Vol. 369, Issue 10
  • DOI: 10.1056/NEJMoa1215837

Core Genome Multilocus Sequence Typing for Identification of Globally Distributed Clonal Groups and Differentiation of Outbreak Strains of Listeria monocytogenes
journal, August 2016

  • Chen, Yi; Gonzalez-Escalona, Narjol; Hammack, Thomas S.
  • Applied and Environmental Microbiology, Vol. 82, Issue 20
  • DOI: 10.1128/AEM.01532-16

Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing
journal, November 2012

  • Fang, Gang; Munera, Diana; Friedman, David I.
  • Nature Biotechnology, Vol. 30, Issue 12
  • DOI: 10.1038/nbt.2432

PHAST: A Fast Phage Search Tool
journal, June 2011

  • Zhou, Y.; Liang, Y.; Lynch, K. H.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr485

The Sequence Alignment/Map format and SAMtools
journal, June 2009


Whole-genome Sequencing Used to Investigate a Nationwide Outbreak of Listeriosis Caused by Ready-to-eat Delicatessen Meat, Denmark, 2014
journal, March 2016

  • Kvistholm Jensen, Anne; Nielsen, Eva Møller; Björkman, Jonas Torgny
  • Clinical Infectious Diseases, Vol. 63, Issue 1
  • DOI: 10.1093/cid/ciw192

The ubiquitous nature of L isteria monocytogenes clones: a large-scale Multilocus Sequence Typing study: MLST of L .  monocytogenes
journal, December 2013

  • Haase, Jana K.; Didelot, Xavier; Lecuit, Marc
  • Environmental Microbiology, Vol. 16, Issue 2
  • DOI: 10.1111/1462-2920.12342

Practical Value of Food Pathogen Traceability through Building a Whole-Genome Sequencing Network and Database
journal, March 2016

  • Allard, Marc W.; Strain, Errol; Melka, David
  • Journal of Clinical Microbiology, Vol. 54, Issue 8
  • DOI: 10.1128/JCM.00081-16

Surface proteins and the pathogenic potential of Listeria monocytogenes
journal, May 2002


Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data
journal, May 2013

  • Chin, Chen-Shan; Alexander, David H.; Marks, Patrick
  • Nature Methods, Vol. 10, Issue 6
  • DOI: 10.1038/nmeth.2474

Red versus green leaves: transcriptomic comparison of foliar senescence between two Prunus cerasifera genotypes
journal, February 2020


A small outbreak of listeriosis potentially linked to the consumption of imitation crab meat
journal, August 2000


VarScan: variant detection in massively parallel sequencing of individual and pooled samples
journal, June 2009


Whole-genome Sequencing Used to Investigate a Nationwide Outbreak of Listeriosis Caused by Ready-to-eat Delicatessen Meat, Denmark, 2014
journal, March 2016

  • Kvistholm Jensen, Anne; Nielsen, Eva Møller; Björkman, Jonas Torgny
  • Clinical Infectious Diseases, Vol. 63, Issue 1
  • DOI: 10.1093/cid/ciw192

Implementation of Nationwide Real-time Whole-genome Sequencing to Enhance Listeriosis Outbreak Detection and Investigation
journal, April 2016

  • Jackson, Brendan R.; Tarr, Cheryl; Strain, Errol
  • Clinical Infectious Diseases, Vol. 63, Issue 3
  • DOI: 10.1093/cid/ciw242

REBASE—a database for DNA restriction and modification: enzymes, genes and genomes
journal, November 2014

  • Roberts, Richard J.; Vincze, Tamas; Posfai, Janos
  • Nucleic Acids Research, Vol. 43, Issue D1, p. D298-D299
  • DOI: 10.1093/nar/gku1046

The ubiquitous nature of L isteria monocytogenes clones: a large-scale Multilocus Sequence Typing study: MLST of L .  monocytogenes
journal, December 2013

  • Haase, Jana K.; Didelot, Xavier; Lecuit, Marc
  • Environmental Microbiology, Vol. 16, Issue 2
  • DOI: 10.1111/1462-2920.12342

Whole genome sequencing as a tool to investigate a cluster of seven cases of listeriosis in Austria and Germany, 2011–2013
journal, May 2014

  • Schmid, D.; Allerberger, F.; Huhulescu, S.
  • Clinical Microbiology and Infection, Vol. 20, Issue 5
  • DOI: 10.1111/1469-0691.12638

Genome Sequencing Identifies Two Nearly Unchanged Strains of Persistent Listeria monocytogenes Isolated at Two Different Fish Processing Plants Sampled 6 Years Apart
journal, February 2013

  • Holch, Anne; Webb, Kristen; Lukjancenko, Oksana
  • Applied and Environmental Microbiology, Vol. 79, Issue 9
  • DOI: 10.1128/aem.03715-12

Draft Genome Sequence of Clostridium sp. Maddingley, Isolated from Coal-Seam Gas Formation Water
journal, February 2013

  • Rosewarne, Carly P.; Greenfield, Paul; Li, Dongmei
  • Genome Announcements, Vol. 1, Issue 1
  • DOI: 10.1128/genomea.00081-12

Draft Genome Sequence of Salmonella enterica subsp. enterica Serovar Give, Isolated from an Imported Chili Powder Product
journal, July 2015


Defining and Evaluating a Core Genome Multilocus Sequence Typing Scheme for Whole-Genome Sequence-Based Typing of Listeria monocytogenes
journal, July 2015

  • Ruppitsch, Werner; Pietzka, Ariane; Prior, Karola
  • Journal of Clinical Microbiology, Vol. 53, Issue 9
  • DOI: 10.1128/jcm.01193-15

Prospective Whole-Genome Sequencing Enhances National Surveillance of Listeria monocytogenes
journal, November 2015

  • Kwong, Jason C.; Mercoulia, Karolina; Tomita, Takehiro
  • Journal of Clinical Microbiology, Vol. 54, Issue 2
  • DOI: 10.1128/jcm.02344-15

MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004


Short-term genome evolution of Listeria monocytogenes in a non-controlled environment
journal, January 2008


Statistics review 9: One-way analysis of variance
journal, January 2004

  • Bewick, Viv; Cheek, Liz; Ball, Jonathan
  • Critical Care, Vol. 8, Issue 2, p. 130
  • DOI: 10.1186/cc2836

Novel Epidemic Clones of Listeria monocytogenes , United States, 2011
journal, January 2013

  • Lomonaco, Sara; Verghese, Bindhu; Gerner-Smidt, Peter
  • Emerging Infectious Diseases, Vol. 19, Issue 1
  • DOI: 10.3201/eid1901.121167

Two Outbreaks of Listeria monocytogenes Infection, Northern Spain
journal, December 2014

  • Pérez-Trallero, Emilio; Zigorraga, Carmen; Artieda, Junkal
  • Emerging Infectious Diseases, Vol. 20, Issue 12
  • DOI: 10.3201/eid2012.140993

Works referencing / citing this record:

Phylogenomic Pipeline Validation for Foodborne Pathogen Disease Surveillance
journal, February 2019

  • Timme, Ruth E.; Strain, Errol; Baugher, Joseph D.
  • Journal of Clinical Microbiology, Vol. 57, Issue 5
  • DOI: 10.1128/jcm.01816-18

Listeriosis Outbreak in South Africa: A Comparative Analysis with Previously Reported Cases Worldwide
journal, January 2020


Benchmark datasets for phylogenomic pipeline validation, applications for foodborne pathogen surveillance
posted_content, July 2017


An Assessment of Different Genomic Approaches for Inferring Phylogeny of Listeria monocytogenes
journal, November 2017

  • Henri, Clémentine; Leekitcharoenphon, Pimlapas; Carleton, Heather A.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.02351

Benchmark datasets for phylogenomic pipeline validation, applications for foodborne pathogen surveillance
journal, January 2017


Survival of a serotype 4b strain and a serotype 1/2a strain of Listeria monocytogenes, isolated from a stone fruit outbreak investigation, on whole stone fruit at 4 °C
journal, December 2020


An Assessment of Different Genomic Approaches for Inferring Phylogeny of Listeria monocytogenes
journal, November 2017

  • Henri, Clémentine; Leekitcharoenphon, Pimlapas; Carleton, Heather A.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.02351

Interpreting Whole-Genome Sequence Analyses of Foodborne Bacteria for Regulatory Applications and Outbreak Investigations
journal, July 2018


Listeriosis Outbreak in South Africa: A Comparative Analysis with Previously Reported Cases Worldwide
journal, January 2020


Growth potential of Listeria monocytogenes in six different RTE fruit products: impact of food matrix, storage temperature and shelf life
journal, October 2018

  • Ziegler, Matthias; Rüegg, Simon; Stephan, Roger
  • Italian Journal of Food Safety, Vol. 7, Issue 3
  • DOI: 10.4081/ijfs.2018.7581

Benchmark datasets for phylogenomic pipeline validation, applications for foodborne pathogen surveillance
posted_content, July 2017