1887

Abstract

We present the LiSEQ ( Listeria SEQuencing) project, funded by the European Food Safety Agency (EFSA) to compare Listeria monocytogenes isolates collected in the European Union from ready-to-eat foods, compartments along the food chain (e.g. food-producing animals, food-processing environments) and humans. In this article, we report the molecular characterization of a selection of this data set employing whole-genome sequencing analysis. We present an overview of the strain diversity observed in different sampled sources, and characterize the isolates based on their virulence and resistance profile. We integrate into our analysis the global L. monocytogenes genome collection described by Moura and colleagues in 2016 to assess the representativeness of the LiSEQ collection in the context of known L. monocytogenes strain diversity.

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2019-02-18
2019-10-15
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References

  1. Allerberger F, Wagner M. Listeriosis: a resurgent foodborne infection. Clin Microbiol Infect 2010;16:16–23 [CrossRef][PubMed]
    [Google Scholar]
  2. Ricci A, Allende A, Bolton D, Chemaly M.EFSA Panel on Biological Hazards (BIOHAZ) et al. Listeria monocytogenes contamination of ready-to-eat foods and the risk for human health in the EU. EFSA J 2018;16:5134
    [Google Scholar]
  3. EFSA, ECDC The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J 2017;15:5077
    [Google Scholar]
  4. Holch A, Webb K, Lukjancenko O, Ussery D, Rosenthal BM et al. Genome sequencing identifies two nearly unchanged strains of persistent Listeria monocytogenes isolated at two different fish processing plants sampled 6 years apart. Appl Environ Microbiol 2013;79:2944–2951 [CrossRef][PubMed]
    [Google Scholar]
  5. Carpentier B, Cerf O. Review-Persistence of Listeria monocytogenes in food industry equipment and premises. Int J Food Microbiol 2011;145:1–8 [CrossRef][PubMed]
    [Google Scholar]
  6. Allerberger F, Bagó Z, Huhulescu S, Pietzka A. Listeriosis: the dark side of refrigeration and ensiling. In Sing A. (editor) Zoonoses – Infections Affecting Humans and Animals Dordrecht: Springer Netherlands; 2015; pp.249–286
    [Google Scholar]
  7. Moura A, Criscuolo A, Pouseele H, Maury MM, Leclercq A et al. Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes. Nat Microbiol 2016;2:16185 [CrossRef][PubMed]
    [Google Scholar]
  8. Camargo AC, Woodward JJ, Nero LA. The continuous challenge of characterizing the foodborne pathogen Listeria monocytogenes. Foodborne Pathog Dis 2016;13:405–416 [CrossRef][PubMed]
    [Google Scholar]
  9. Chen Y, Luo Y, Carleton H, Timme R, Melka D et al. Whole genome and core genome multilocus sequence typing and single nucleotide polymorphism analyses of Listeria monocytogenes associated with an outbreak linked to cheese, United States, 2013. Appl Environ Microbiol 2017;83:e00633-17 [CrossRef][PubMed]
    [Google Scholar]
  10. European Food Safety Authority Analysis of the baseline survey on the prevalence of Listeria monocytogenes in certain ready-to-eat foods in the EU, 2010–2011. Part A: Listeria monocytogenes prevalence estimates. EFSA J 2013;11:3241
    [Google Scholar]
  11. Orsi RH, den Bakker HC, Wiedmann M. Listeria monocytogenes lineages: genomics, evolution, ecology, and phenotypic characteristics. Int J Med Microbiol 2011;301:79–96 [CrossRef][PubMed]
    [Google Scholar]
  12. Burall LS, Grim CJ, Mammel MK, Datta AR. A comprehensive evaluation of the genetic relatedness of Listeria monocytogenes serotype 4b variant strains. Front Public Health 2017;5:241 [CrossRef][PubMed]
    [Google Scholar]
  13. Ragon M, Wirth T, Hollandt F, Lavenir R, Lecuit M et al. A new perspective on Listeria monocytogenes evolution. PLoS Pathog 2008;4:e1000146 [CrossRef][PubMed]
    [Google Scholar]
  14. Rychli K, Müller A, Zaiser A, Schoder D, Allerberger F et al. Genome sequencing of Listeria monocytogenes "Quargel" listeriosis outbreak strains reveals two different strains with distinct in vitro virulence potential. PLoS One 2014;9:e89964 [CrossRef][PubMed]
    [Google Scholar]
  15. Kwong JC, Mercoulia K, Tomita T, Easton M, Li HY et al. Prospective whole-genome sequencing enhances national surveillance of Listeria monocytogenes. J Clin Microbiol 2016;54:333–342 [CrossRef][PubMed]
    [Google Scholar]
  16. Jackson BR, Tarr C, Strain E, Jackson KA, Conrad A et al. Implementation of nationwide real-time whole-genome sequencing to enhance listeriosis outbreak detection and investigation. Clin Infect Dis 2016;63:380–386 [CrossRef][PubMed]
    [Google Scholar]
  17. Kvistholm Jensen A, Nielsen EM, Björkman JT, Jensen T, Müller L et al. Whole-genome sequencing used to investigate a nationwide outbreak of listeriosis caused by ready-to-eat delicatessen meat, Denmark, 2014. Clin Infect Dis 2016;63:64–70 [CrossRef][PubMed]
    [Google Scholar]
  18. Moura A, Tourdjman M, Leclercq A, Hamelin E, Laurent E et al. Real-time whole-genome sequencing for surveillance of Listeria monocytogenes, France. Emerg Infect Dis 2017;23:1462–1470 [CrossRef][PubMed]
    [Google Scholar]
  19. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014;30:2114–2120 [CrossRef][PubMed]
    [Google Scholar]
  20. Tewolde R, Dallman T, Schaefer U, Sheppard CL, Ashton P et al. MOST: a modified MLST typing tool based on short read sequencing. PeerJ 2016;4:e2308 [CrossRef][PubMed]
    [Google Scholar]
  21. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012;19:455–477 [CrossRef][PubMed]
    [Google Scholar]
  22. Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 2014;15:524 [CrossRef][PubMed]
    [Google Scholar]
  23. Charpentier E, Courvalin P. Antibiotic resistance in Listeria spp. Antimicrob Agents Chemother 1999;43:2103–2108 [CrossRef][PubMed]
    [Google Scholar]
  24. Lungu B, O'Bryan CA, Muthaiyan A, Milillo SR, Johnson MG et al. Listeria monocytogenes: antibiotic resistance in food production. Foodborne Pathog Dis 2011;8:569–578 [CrossRef][PubMed]
    [Google Scholar]
  25. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012;9:357–359 [CrossRef][PubMed]
    [Google Scholar]
  26. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J1000 Genome Project Data Processing Subgroup et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009;25:2078–2079 [CrossRef][PubMed]
    [Google Scholar]
  27. Camejo A, Carvalho F, Reis O, Leitão E, Sousa S et al. The arsenal of virulence factors deployed by Listeria monocytogenes to promote its cell infection cycle. Virulence 2011;2:379–394 [CrossRef][PubMed]
    [Google Scholar]
  28. Maury MM, Tsai YH, Charlier C, Touchon M, Chenal-Francisque V et al. Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity. Nat Genet 2016;48:308–313 [CrossRef][PubMed]
    [Google Scholar]
  29. Cabanes D, Sousa S, Cebriá A, Lecuit M, García-del Portillo F et al. Gp96 is a receptor for a novel Listeria monocytogenes virulence factor, Vip, a surface protein. Embo J 2005;24:2827–2838 [CrossRef][PubMed]
    [Google Scholar]
  30. Chen J, Luo X, Jiang L, Jin P, Wei W et al. Molecular characteristics and virulence potential of Listeria monocytogenes isolates from Chinese food systems. Food Microbiol 2009;26:103–111 [CrossRef][PubMed]
    [Google Scholar]
  31. Gómez D, Azón E, Marco N, Carramiñana JJ, Rota C et al. Antimicrobial resistance of Listeria monocytogenes and Listeria innocua from meat products and meat-processing environment. Food Microbiol 2014;42:61–65 [CrossRef][PubMed]
    [Google Scholar]
  32. Ryan S, Begley M, Hill C, Gahan CG. A five-gene stress survival islet (SSI-1) that contributes to the growth of Listeria monocytogenes in suboptimal conditions. J Appl Microbiol 2010;109:984–995 [CrossRef][PubMed]
    [Google Scholar]
  33. Carvalho F, Atilano ML, Pombinho R, Covas G, Gallo RL et al. L-Rhamnosylation of Listeria monocytogenes Wall Teichoic Acids Promotes Resistance to Antimicrobial Peptides by Delaying Interaction with the Membrane. PLoS Pathog 2015;11:e1004919 [CrossRef][PubMed]
    [Google Scholar]
  34. Promadej N, Fiedler F, Cossart P, Dramsi S, Kathariou S. Cell wall teichoic acid glycosylation in Listeria monocytogenes serotype 4b requires gtcA, a novel, serogroup-specific gene. J Bacteriol 1999;181:418–425[PubMed]
    [Google Scholar]
  35. Cabanes D, Dussurget O, Dehoux P, Cossart P. Auto, a surface associated autolysin of Listeria monocytogenes required for entry into eukaryotic cells and virulence. Mol Microbiol 2004;51:1601–1614 [CrossRef][PubMed]
    [Google Scholar]
  36. Ebner R, Stephan R, Althaus D, Brisse S, Maury M et al. Phenotypic and genotypic characteristics of Listeria monocytogenes strains isolated during 2011–2014 from different food matrices in Switzerland. Food Control 2015;57:321–326 [CrossRef]
    [Google Scholar]
  37. Félix B, Feurer C, Maillet A, Guillier L, Boscher E et al. Population genetic structure of Listeria monocytogenes strains isolated from the pig and pork production chain in France. Front Microbiol 2018;9:684 [CrossRef][PubMed]
    [Google Scholar]
  38. Henri C, Leekitcharoenphon P, Carleton HA, Radomski N, Kaas RS et al. An assessment of different genomic approaches for inferring phylogeny of Listeria monocytogenes. Front Microbiol 2017;8:2351 [CrossRef][PubMed]
    [Google Scholar]
  39. Bertrand S, Huys G, Yde M, D'Haene K, Tardy F et al. Detection and characterization of tet(M) in tetracycline-resistant Listeria strains from human and food-processing origins in Belgium and France. J Med Microbiol 2005;54:1151–1156 [CrossRef][PubMed]
    [Google Scholar]
  40. Morvan A, Moubareck C, Leclercq A, Hervé-Bazin M, Bremont S et al. Antimicrobial resistance of Listeria monocytogenes strains isolated from humans in France. Antimicrob Agents Chemother 2010;54:2728–2731 [CrossRef][PubMed]
    [Google Scholar]
  41. Granier SA, Moubareck C, Colaneri C, Lemire A, Roussel S et al. Antimicrobial resistance of Listeria monocytogenes isolates from food and the environment in France over a 10-year period. Appl Environ Microbiol 2011;77:2788–2790 [CrossRef][PubMed]
    [Google Scholar]
  42. Jamali H, Paydar M, Ismail S, Looi CY, Wong WF et al. Prevalence, antimicrobial susceptibility and virulotyping of Listeria species and Listeria monocytogenes isolated from open-air fish markets. BMC Microbiol 2015;15:144 [CrossRef][PubMed]
    [Google Scholar]
  43. den Besten HMW, Amézquita A, Bover-Cid S, Dagnas S, Ellouze M et al. Next generation of microbiological risk assessment: potential of omics data for exposure assessment. Int J Food Microbiol 2018;287:18–27 [CrossRef][PubMed]
    [Google Scholar]
  44. Rantsiou K, Kathariou S, Winkler A, Skandamis P, Saint-Cyr MJ et al. Next generation microbiological risk assessment: opportunities of whole genome sequencing (WGS) for foodborne pathogen surveillance, source tracking and risk assessment. Int J Food Microbiol 2018;287:3–9 [CrossRef][PubMed]
    [Google Scholar]
  45. Franz E, Gras LM, Dallman T. Significance of whole genome sequencing for surveillance, source attribution and microbial risk assessment of foodborne pathogens. Curr Opin Food Sci 2016;8:74–79 [CrossRef]
    [Google Scholar]
  46. Pielaat A, Boer MP, Wijnands LM, van Hoek AH, Bouw E et al. First step in using molecular data for microbial food safety risk assessment; hazard identification of Escherichia coli O157:H7 by coupling genomic data with in vitro adherence to human epithelial cells. Int J Food Microbiol 2015;213:130–138 [CrossRef][PubMed]
    [Google Scholar]
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