Genome analysis of Listeria monocytogenes sequence type 8 strains persisting in salmon and poultry processing environments and comparison with related strains

PLoS ONE

Volumn 11, Issue 3, 2016, Pages

  Fagerlund, Annette ^a   Langsrud, Solveig ^a   Schirmer, Bjørn C T ^a,b   Møretrø, Trond ^a   Heir, Even ^a  

^a NOFIMA   (Norway)

^b NORWEGIAN VETERINARY INSTITUTE   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; CONTROLLED STUDY; DISEASE TRANSMISSION; FOOD INDUSTRY; FOOD INTAKE; FOOD PROCESSING; GENE LOCUS; GENETIC ASSOCIATION; GENOME ANALYSIS; LISTERIA MONOCYTOGENES; LISTERIA MONOCYTOGENES SEQUENCE TYPE 8; LISTERIOSIS; NONHUMAN; POULTRY; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; BIOLOGY; CLASSIFICATION; DNA SEQUENCE; FOOD CONTROL; FOOD HANDLING; FOOD SAFETY; GENETICS; MICROBIOLOGY; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; PLASMID; PROCEDURES; PROPHAGE; SALMONINE;

VIRULENCE FACTOR;

ANIMALS; COMPUTATIONAL BIOLOGY; FOOD HANDLING; FOOD MICROBIOLOGY; FOOD SAFETY; GENETIC LOCI; GENOME, BACTERIAL; LISTERIA MONOCYTOGENES; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; PLASMIDS; POLYMORPHISM, SINGLE NUCLEOTIDE; POULTRY; PROPHAGES; SALMON; SEQUENCE ANALYSIS, DNA; VIRULENCE FACTORS;

EID: 84961133413     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0151117     Document Type: Article

References (73)

1. Møretrø T, Langsrud S. Listeria monocytogenes: biofilm formation and persistence in food-processing environments. Biofilms. 2004; 1(02):107-121.
2. Ferreira V, Wiedmann M, Teixeira P, Stasiewicz MJ. Listeria monocytogenes persistence in food-associated environments: epidemiology, strain characteristics, and implications for public health. J Food Protect. 2014; 77(1):150-170.
3. Carpentier B, Cerf O. Review - Persistence of Listeria monocytogenes in food industry equipment and premises. Int J FoodMicrobiol. 2011; 145(1):1-8. doi: 10.1016/j.ijfoodmicro.2011.01.005 PMID: 21276634
4. Larsen MH, Dalmasso M, Ingmer H, Langsrud S, Malakauskas M, Mader A, et al. Persistence of foodborne pathogens and their control in primary and secondary food production chains. Food Control. 2014; 44:92-109.
5. Salipante SJ, SenGupta DJ, Cummings LA, Land TA, Hoogestraat DR, Cookson BT. Application of whole-genome sequencing for bacterial strain typing in molecular epidemiology. J Clin Microbiol. 2015; 53(4):1072-1079. doi: 10.1128/JCM.03385-14 PMID: 25631811
6. Parkhill J, Wren BW. Bacterial epidemiology and biology - lessons from genome sequencing. Genome Biol. 2011; 12(10):230. doi: 10.1186/gb-2011-12-10-230 PMID: 22027015
7. Gardy J, Loman NJ, Rambaut A. Real-time digital pathogen surveillance - the time is now. Genome Biol. 2015; 16:155.
8. Gilmour MW, Graham M, Van Domselaar G, Tyler S, Kent H, Trout-Yakel KM, et al. High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak. BMC Genomics. 2010; 11:120. doi: 10.1186/1471-2164-11-120 PMID: 20167121
9. Orsi RH, Borowsky ML, Lauer P, Young SK, Nusbaum C, Galagan JE, et al. Short-term genome evolution of Listeria monocytogenes in a non-controlled environment. BMC Genomics. 2008; 9:539. doi: 10.1186/1471-2164-9-539 PMID: 19014550
10. Rychli K, Müller A, Zaiser A, Schoder D, Allerberger F, Wagner M, 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(2):e89964. doi: 10.1371/journal.pone.0089964 PMID: 24587155
11. Schmid D, Allerberger F, Huhulescu S, Pietzka A, Amar C, Kleta S, et al. Whole genome sequencing as a tool to investigate a cluster of seven cases of listeriosis in Austria and Germany, 2011-2013. Clin Microbiol Infect. 2014; 20(5):431-436. doi: 10.1111/1469-0691.12638 PMID: 24698214
12. Holch A, Webb K, Lukjancenko O, Ussery D, Rosenthal BM, Gram L. 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(9):2944-2951. doi: 10.1128/ AEM.03715-12 PMID: 23435887
13. Schmitz-Esser S, Müller A, Stessl B, Wagner M. Genomes of sequence type 121 Listeria monocytogenes strains harbor highly conserved plasmids and prophages. Front Microbiol. 2015; 6:380. doi: 10.3389/fmicb.2015.00380 PMID: 25972859
14. Stasiewicz MJ, Oliver HF, Wiedmann M, den Bakker HC. Whole-genome sequencing allows for improved identification of persistent Listeria monocytogenes in food-associated environments. Appl Environ Microbiol. 2015; 81(17):6024-6037. doi: 10.1128/AEM.01049-15 PMID: 26116683
15. Fonnesbech Vogel B, Huss HH, Ojeniyi B, Ahrens P, Gram L. Elucidation of Listeria monocytogenes contamination routes in cold-smoked salmon processing plants detected by DNA-based typing methods. Appl Environ Microbiol. 2001; 67(6):2586-2595. PMID: 11375167
16. Schmitz-Esser S, Gram L, Wagner M. Complete genome sequence of the persistent Listeria monocytogenes strain R479a. Genome Announc. 2015; 3(2):e00150-15. doi: 10.1128/genomeA.00150-15 PMID: 25792065
17. Martín B, Perich A, Gómez D, Yangüela J, Rodríguez A, Garriga M, et al. Diversity and distribution of Listeria monocytogenes in meat processing plants. Food Microbiol. 2014; 44:119-127. doi: 10.1016/j. fm.2014.05.014 PMID: 25084653
18. Wang Y, Zhao A, Zhu R, Lan R, Jin D, Cui Z, et al. Genetic diversity and molecular typing of Listeria monocytogenes in China. BMC Microbiol. 2012; 12:119. doi: 10.1186/1471-2180-12-119 PMID: 22727037
19. Ciolacu L, Nicolau AI, Wagner M, Rychli K. Listeria monocytogenes isolated from food samples from a Romanian black market show distinct virulence profiles. Int J Food Microbiol. 2015; 209:44-51. doi: 10.1016/j.ijfoodmicro.2014.08.035 PMID: 25241012
20. Chiara M, D'Erchia AM, Manzari C, Minotto A, Montagna C, Addante N, et al. Draft genome sequences of six Listeria monocytogenes strains isolated from dairy products from a processing plant in southern Italy. Genome Announc. 2014; 2(2):e00282-14. doi: 10.1128/genomeA.00282-14 PMID: 24723720
21. Ebner R, Stephan R, Althaus D, Brisse S, Maury M, Tasara T. Phenotypic and genotypic characteristics of Listeria monocytogenes strains isolated during 2011-2014 from different food matrices in Switzerland. Food Control. 2015; 57:321-326.
22. Knabel SJ, Reimer A, Verghese B, Lok M, Ziegler J, Farber J, et al. Sequence typing confirms that a predominant Listeria monocytogenes clone caused human listeriosis cases and outbreaks in Canada from 1988 to 2010. J Clin Microbiol. 2012; 50(5):1748-1751. doi: 10.1128/JCM.06185-11 PMID: 22337989
23. Mammina C, Parisi A, Guaita A, Aleo A, Bonura C, Nastasi A, et al. Enhanced surveillance of invasive listeriosis in the Lombardy region, Italy, in the years 2006-2010 reveals major clones and an increase in serotype 1/2a. BMC Infect Dis. 2013; 13:152. doi: 10.1186/1471-2334-13-152 PMID: 23530941
24. Ragon M, Wirth T, Hollandt F, Lavenir R, Lecuit M, Le Monnier A, et al. A new perspective on Listeria monocytogenes evolution. PLoS Pathog. 2008; 4(9):e1000146. doi: 10.1371/journal.ppat.1000146 PMID: 18773117
25. Cao G, Zhang J, Xu X, Jin H, Yang X, Pan H, et al. Whole-genome sequences of 12 clinical strains of Listeria monocytogenes. Genome Announc. 2015; 3(1):e01203-14. doi: 10.1128/genomeA.01203-14 PMID: 25720683
26. Althaus D, Lehner A, Brisse S, Maury M, Tasara T, Stephan R. Characterization of Listeria monocytogenes strains isolated during 2011-2013 from human infections in Switzerland. Foodborne Pathog Dis. 2014; 11(10):753-758. doi: 10.1089/fpd.2014.1747 PMID: 25007293
27. Lindstedt BA, Tham W, Danielsson-Tham ML, Vardund T, Helmersson S, Kapperud G. Multiple-locus variable-number tandem-repeats analysis of Listeria monocytogenes using multicolour capillary electrophoresis and comparison with pulsed-field gel electrophoresis typing. J Microbiol Methods. 2008; 72 (2):141-148. PMID: 18096258
28. Pightling AW, Pagotto F. Genome sequence of Listeria monocytogenes strain HPB5415, collected during a 2008 listeriosis outbreak in Canada. Genome Announc. 2015; 3(3):e00637-15. doi: 10.1128/ genomeA.00637-15 PMID: 26067972
29. Tasara T, Weinmaier T, Klumpp J, Rattei T, Stephan R. Complete genome sequence of Listeria monocytogenes Lm60, a strain with an enhanced cold adaptation capacity. Genome Announc. 2014; 2(6): e01248-14. doi: 10.1128/genomeA.01248-14 PMID: 25477407
30. Magoc T, Pabinger S, Canzar S, Liu X, Su Q, Puiu D, et al. GAGE-B: an evaluation of genome assemblers for bacterial organisms. Bioinformatics. 2013; 29(14):1718-1725. doi: 10.1093/bioinformatics/ btt273 PMID: 23665771
31. Koren S, Treangen TJ, Hill CM, Pop M, Phillippy AM. Automated ensemble assembly and validation of microbial genomes. BMC Bioinformatics. 2014; 15:126. doi: 10.1186/1471-2105-15-126 PMID: 24884846
32. Aronesty E. ea-utils: "Command-line tools for processing biological sequencing data" 2011. Available: http://code.google.com/p/ea-utils
33. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012; 19(5):455-477. doi: 10.1089/cmb.2012.0021 PMID: 22506599
34. Chikhi R, Medvedev P. Informed and automated k-mer size selection for genome assembly. Bioinformatics. 2014; 30(1):31-37. doi: 10.1093/bioinformatics/btt310 PMID: 23732276
35. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013; 29(8):1072-1075. doi: 10.1093/bioinformatics/btt086 PMID: 23422339
36. Bécavin C, Bouchier C, Lechat P, Archambaud C, Creno S, Gouin E, et al. Comparison of widely used Listeria monocytogenes strains EGD, 10403S, and EGD-e highlights genomic variations underlying differences in pathogenicity. MBio. 2014; 5(2):e00969-14. doi: 10.1128/mBio.00969-14 PMID: 24667708
37. Rissman AI, Mau B, Biehl BS, Darling AE, Glasner JD, Perna NT. Reordering contigs of draft genomes using the Mauve aligner. Bioinformatics. 2009; 25(16):2071-2073. doi: 10.1093/bioinformatics/btp356 PMID: 19515959
38. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nature Methods. 2012; 9 (4):357-359. doi: 10.1038/nmeth.1923 PMID: 22388286
39. Garrison E, Marth G. Haplotype-based variant detection from short-read sequencing. arXiv Preprint; 2012. Available from: http://arxiv.org/abs/1207.3907.
40. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, et al. Versatile and open software for comparing large genomes. Genome Biol. 2004; 5(2):R12. PMID: 14759262
41. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013; 30(12):2725-2729. doi: 10.1093/molbev/mst197 PMID: 24132122
42. Dorscht J, Klumpp J, Bielmann R, Schmelcher M, Born Y, Zimmer M, et al. Comparative genome analysis of Listeria bacteriophages reveals extensive mosaicism, programmed translational frameshifting, and a novel prophage insertion site. J Bacteriol. 2009; 191(23):7206-7215. doi: 10.1128/JB.01041-09 PMID: 19783628
43. Loessner MJ, Inman RB, Lauer P, Calendar R. Complete nucleotide sequence, molecular analysis and genome structure of bacteriophage A118 of Listeria monocytogenes: implications for phage evolution. Mol Microbiol. 2000; 35(2):324-340. PMID: 10652093
44. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. PHAST: a fast phage search tool. Nucleic Acids Res. 2011; 39:W347-352. doi: 10.1093/nar/gkr485 PMID: 21672955
45. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009; 10:421. doi: 10.1186/1471-2105-10-421 PMID: 20003500
46. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics. 2011; 27 (7):1009-1010. doi: 10.1093/bioinformatics/btr039 PMID: 21278367
47. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 2007; 35:W52-57. PMID: 17537822
48. Laing C, Buchanan C, Taboada EN, Zhang Y, Kropinski A, Villegas A, et al. Pan-genome sequence analysis using Panseq: an online tool for the rapid analysis of core and accessory genomic regions. BMC Bioinformatics. 2010; 11:461. doi: 10.1186/1471-2105-11-461 PMID: 20843356
49. Zhang J, Zhang Y, Zhu L, Suzuki M, Inouye M. Interference of mRNA function by sequence-specific endoribonuclease PemK. J Biol Chem. 2004; 279(20):20678-20684. PMID: 15024022
50. Kuenne C, Billion A, Mraheil MA, Strittmatter A, Daniel R, Goesmann A, et al. Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome. BMC Genomics. 2013; 14:47. doi: 10.1186/1471-2164-14-47 PMID: 23339658
51. Loenen WA, Dryden DT, Raleigh EA, Wilson GG. Type I restriction enzymes and their relatives. Nucleic Acids Res. 2014; 42(1):20-44. doi: 10.1093/nar/gkt847 PMID: 24068554
52. Sesto N, Touchon M, Andrade JM, Kondo J, Rocha EP, Arraiano CM, et al. A PNPase dependent CRISPR System in Listeria. PLoS Genetics. 2014; 10(1):e1004065. doi: 10.1371/journal.pgen. 1004065 PMID: 24415952
53. Iyer LM, Abhiman S, Aravind L. MutL homologs in restriction-modification systems and the origin of eukaryotic MORC ATPases. Biol Direct. 2008; 3:8. doi: 10.1186/1745-6150-3-8 PMID: 18346280
54. Camejo A, Buchrieser C, Couvé E, Carvalho F, Reis O, Ferreira P, et al. In vivo transcriptional profiling of Listeria monocytogenes and mutagenesis identify new virulence factors involved in infection. PLoS Pathog. 2009; 5(5):e1000449. doi: 10.1371/journal.ppat.1000449 PMID: 19478867
55. Gaillard JL, Berche P, Frehel C, Gouin E, Cossart P. Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from Gram-positive cocci. Cell. 1991; 65 (7):1127-1141. PMID: 1905979
56. Kosman DJ. Multicopper oxidases: a workshop on copper coordination chemistry, electron transfer, and metallophysiology. J Biol Inorg Chem. 2010; 15(1):15-28. doi: 10.1007/s00775-009-0590-9 PMID: 19816718
57. Lebrun M, Audurier A, Cossart P. Plasmid-borne cadmium resistance genes in Listeria monocytogenes are present on Tn5422, a novel transposon closely related to Tn917. J Bacteriol. 1994; 176(10):3049-3061. PMID: 8188606
58. Dutta V, Elhanafi D, Kathariou S. Conservation and distribution of the benzalkonium chloride resistance cassette bcrABC in Listeria monocytogenes. Appl Environ Microbiol. 2013; 79(19):6067-6074. doi: 10.1128/AEM.01751-13 PMID: 23892748
59. Müller A, Rychli K, Zaiser A, Wieser C, Wagner M, Schmitz-Esser S. The Listeria monocytogenes transposon Tn6188 provides increased tolerance to various quaternary ammonium compounds and ethidium bromide. FEMS Microbiol Lett. 2014; 361(2):166-173. doi: 10.1111/1574-6968.12626 PMID: 25312720
60. Hawkey J, Edwards DJ, Dimovski K, Hiley L, Billman-Jacobe H, Hogg G, et al. Evidence of microevolution of Salmonella Typhimurium during a series of egg-associated outbreaks linked to a single chicken farm. BMC Genomics. 2013; 14:800. doi: 10.1186/1471-2164-14-800 PMID: 24245509
61. Croucher NJ, Harris SR, Grad YH, Hanage WP. Bacterial genomes in epidemiology - present and future. Philos Trans R Soc Lond B Biol Sci. 2013; 368(1614):20120202. doi: 10.1098/rstb.2012.0202 PMID: 23382424
62. Lundén JM, Autio TJ, Korkeala HJ. Transfer of persistent Listeria monocytogenes contamination between food-processing plants associated with a dicing machine. J Food Protect. 2002; 65(7):1129-33.
63. Verghese B, Lok M, Wen J, Alessandria V, Chen Y, Kathariou S, et al. comK prophage junction fragments as markers for Listeria monocytogenes genotypes unique to individual meat and poultry processing plants and a model for rapid niche-specific adaptation, biofilm formation, and persistence. Appl Environ Microbiol. 2011; 77(10):3279-3292. doi: 10.1128/AEM.00546-11 PMID: 21441318
64. Seed KD. Battling phages: How bacteria defend against viral attack. PLoS Pathog. 2015; 11(6): e1004847. doi: 10.1371/journal.ppat.1004847 PMID: 26066799
65. Dy RL, Richter C, Salmond GPC, Fineran PC. Remarkable mechanisms in microbes to resist phage infections. Annu Rev Virol. 2014; 1:307-331.
66. Cerdeño-Tárraga AM, Patrick S, Crossman LC, Blakely G, Abratt V, Lennard N, et al. Extensive DNA inversions in the B. fragilis genome control variable gene expression. Science. 2005; 307(5714):1463-1465. PMID: 15746427
67. Sitaraman R, Dybvig K. The hsd loci of Mycoplasma pulmonis: organization, rearrangements and expression of genes. Mol Microbiol. 1997; 26(1):109-120. PMID: 9383194
68. Eugster MR, Loessner MJ. Wall teichoic acids restrict access of bacteriophage endolysin Ply118, Ply511, and PlyP40 cell wall binding domains to the Listeria monocytogenes peptidoglycan. J Bacteriol. 2012; 194(23):6498-6506. doi: 10.1128/JB.00808-12 PMID: 23002226
69. Denes T, den Bakker HC, Tokman JI, Guldimann C, Wiedmann M. Selection and characterization of phage-resistant mutant strains of Listeria monocytogenes reveals host genes linked to phage adsorption. Appl Environ Microbiol. 2015; 81(13):4295-3405. doi: 10.1128/AEM.00087-15 PMID: 25888172
70. Jensen A, Thomsen LE, Jorgensen RL, Larsen MH, Roldgaard BB, Christensen BB, et al. Processing plant persistent strains of Listeria monocytogenes appear to have a lower virulence potential than clinical strains in selected virulence models. Int J Food Microbiol. 2008; 123(3):254-261. doi: 10.1016/j. ijfoodmicro.2008.02.016 PMID: 18394737
71. Van Stelten A, Simpson JM, Ward TJ, Nightingale KK. Revelation by single-nucleotide polymorphism genotyping that mutations leading to a premature stop codon in inlA are common among Listeria monocytogenes isolates from ready-to-eat foods but not human listeriosis cases. Appl Environ Microbiol. 2010; 76(9):2783-2790. doi: 10.1128/AEM.02651-09 PMID: 20208021
72. Nightingale KK, Windham K, Martin KE, Yeung M, Wiedmann M. Select Listeria monocytogenes subtypes commonly found in foods carry distinct nonsense mutations in inlA, leading to expression of truncated and secreted internalin A, and are associated with a reduced invasion phenotype for human intestinal epithelial cells. Appl Environ Microbiol. 2005; 71(12):8764-8772. PMID: 16332872
73. Norton DM, McCamey MA, Gall KL, Scarlett JM, Boor KJ, Wiedmann M. Molecular studies on the ecology of Listeria monocytogenes in the smoked fish processing industry. Appl Environ Microbiol. 2001; 67(1):198-205. PMID: 11133446