Determination of evolutionary relationships of outbreakassociated Listeria monocytogenes strains of serotypes 1/2a and 1/2b by wholegenome sequencing

Applied and Environmental Microbiology

Volumn 82, Issue 3, 2016, Pages 928-938

  Bergholz, Teresa M ^a   Den Bakker, Henk C ^b,f   Katz, Lee S ^c   Silk, Benjamin J ^c   Jackson, Kelly A ^c   Kucerova, Zuzana ^c   Joseph, Lavin A ^c   Turnsek, Maryann ^c   Gladney, Lori M ^c   Halpin, Jessica L ^c   Xavier, Karen ^d   Gossack, Joseph ^d   Ward, Todd J ^e   Frace, Michael ^c   Tarr, Cheryl L ^c  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^d Colorado Department of Public Health and Environment ^*  (United States)

^e AGRICULTURAL RESEARCH SERVICE   (United States)

^f TEXAS TECH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLONING; DISEASES; EPIDEMIOLOGY; GENE TRANSFER; LISTERIA;

BACTERIAL COMMUNITY; EVOLUTIONARY RELATIONSHIPS; HORIZONTAL GENE TRANSFER; LISTERIA MONOCYTOGENES; ORDERS OF MAGNITUDE; PAIR-WISE COMPARISON; STRUCTURAL DIVERSITY; WHOLE GENOME SEQUENCING; PRODUCTION FACILITY;

GENES;

BACTERIUM; COMPLEXITY; EPIDEMIC; EPIDEMIOLOGY; GENE TRANSFER; GENETIC VARIATION; GENOME; MUTATION; POPULATION OUTBREAK;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES;

BACTERIAL GENOME; DNA SEQUENCE; EPIDEMIC; GENETIC VARIATION; GENETICS; HORIZONTAL GENE TRANSFER; HUMAN; ISOLATION AND PURIFICATION; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICROBIOLOGY; MOLECULAR EVOLUTION; PHYLOGENY; POINT MUTATION; SEROTYPE; SEROTYPING; UNITED STATES;

DISEASE OUTBREAKS; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GENETIC VARIATION; GENOME, BACTERIAL; HUMANS; LISTERIA MONOCYTOGENES; LISTERIOSIS; PHYLOGENY; POINT MUTATION; SEQUENCE ANALYSIS, DNA; SEROGROUP; SEROTYPING; UNITED STATES;

EID: 84957640617     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02440-15     Document Type: Article

References (54)

1. Silk BJ, Date KA, Jackson KA, Pouillot R, Holt KG, Graves LM, Ong KL, Hurd S, Meyer R, Marcus R, Shiferaw B, Norton DM, Medus C, Zansky SM, Cronquist AB, Henao OL, Jones TF, Vugia DJ, Farley MM, Mahon BE. 2012. Invasive listeriosis in the Foodborne Diseases Active Surveillance Network (FoodNet), 2004-2009: further targeted prevention needed for higher-risk groups. Clin Infect Dis 54(Suppl 5):S396-S404.
2. Cartwright EJ, Jackson KA, Johnson SD, Graves LM, Silk BJ, Mahon BE. 2013. Listeriosis outbreaks and associated food vehicles, United States, 1998-2008. Emerg Infect Dis 19:1-9; quiz, 184. http://dx.doi.org/10.3201/eid1901.120393.
3. Ward TJ, Gorski L, Borucki MK, Mandrell RE, Hutchins J, Pupedis K. 2004 Intraspecific phylogeny and lineage group identification based on the prfA virulence gene cluster of Listeria monocytogenes. J Bacteriol 186: 4994-5002. http://dx.doi.org/10.1128/JB.186.15.4994-5002.2004.
4. McCollum JT, Cronquist AB, Silk BJ, Jackson KA, O'Connor KA, Cosgrove S, Gossack JP, Parachini SS, Jain NS, Ettestad P, Ibraheem M, Cantu V, Joshi M, DuVernoy T, Fogg NW, Jr, Gorny JR, Mogen KM, Spires C, Teitell P, Joseph LA, Tarr CL, Imanishi M, Neil KP, Tauxe RV, Mahon BE. 2013. Multistate outbreak of listeriosis associated with cantaloupe. N Engl J Med 369:944-953. http://dx.doi.org/10.1056/NEJMoa1215837.
5. Ragon M, Wirth T, Hollandt F, Lavenir R, Lecuit M, Le Monnier A, Brisse S. 2008. A new perspective on Listeria monocytogenes evolution. PLoS Pathog 4:e1000146. http://dx.doi.org/10.1371/journal.ppat.1000146.
6. Zhang W, Jayarao BM, Knabel SJ. 2004. Multi-virulence-locus sequence typing of Listeria monocytogenes. Appl Environ Microbiol 70:913-920. http://dx.doi.org/10.1128/AEM.70.2.913-920.2004.
7. Knabel SJ, Reimer A, Verghese B, Lok M, Ziegler J, Farber J, Pagotto F, Graham M, Nadon CA, Canadian Public Health Laboratory N, Gilmour MW. 2012. Sequence typing confirms that a predominant Listeria monocytogenes clone caused human listeriosis cases and outbreaks in Canada from 1988 to 2010. J Clin Microbiol 50:1748-1751. http://dx.doi.org/10.1128/JCM.06185-11.
8. Cantinelli T, Chenal-Francisque V, Diancourt L, Frezal L, Leclercq A, Wirth T, Lecuit M, Brisse S. 2013. "Epidemic clones" of Listeria monocytogenes are widespread and ancient clonal groups. J Clin Microbiol 51: 3770-3779. http://dx.doi.org/10.1128/JCM.01874-13.
9. Lomonaco S, Verghese B, Gerner-Smidt P, Tarr C, Gladney L, Joseph L, Katz L, Turnsek M, Frace M, Chen Y, Brown E, Meinersmann R, Berrang M, Knabel S. 2013. Novel epidemic clones of Listeria monocytogenes, United States, 2011. Emerg Infect Dis 19:147-150. http://dx.doi.org/10.3201/eid1901.121167.
10. Ward TJ, Ducey TF, Usgaard T, Dunn KA, Bielawski JP. 2008. Multilocus genotyping assays for single nucleotide polymorphism-based subtyping of Listeria monocytogenes isolates. Appl Environ Microbiol 74: 7629-7642. http://dx.doi.org/10.1128/AEM.01127-08.
11. Zerbino DR. 2010. Using the Velvet de novo assembler for short-read sequencing technologies. Curr Protoc Bioinformatics Chapter 11:Unit 11.5.
12. Heiman KE, Garalde VB, Gronostaj M, Jackson KA, Beam S, Joseph L, Saupe A, Ricotta E, Waechter H, Wellman A, Adams-Cameron M, Ray G, Fields A, Chen Y, Datta A, Burall L, Sabol A, Kucerova Z, Trees E, Metz M, Leblanc P, Lance S, Griffin PM, Tauxe RV, Silk BJ. 30 June 2015 Multistate outbreak of listeriosis caused by imported cheese and evidence of cross-contamination of other cheeses, USA, 2012. Epidemiol Infect http://dx.doi.org/10.1017/S095026881500117X.
13. Gardner SN, Hall BG. 2013. When whole-genome alignments just won't work: kSNP v2 software for alignment-free SNP discovery and phylogenetics of hundreds of microbial genomes. PLoS One 8:e81760. http://dx.doi.org/10.1371/journal.pone.0081760.
14. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. http://dx.doi.org/10.1093/bioinformatics/btl446.
15. Katz LS, Petkau A, Beaulaurier J, Tyler S, Antonova ES, Turnsek MA, Guo Y, Wang S, Paxinos EE, Orata F, Gladney LM, Stroika S, Folster JP, Rowe L, Freeman MM, Knox N, Frace M, Boncy J, Graham M, Hammer BK, Boucher Y, Bashir A, Hanage WP, Van Domselaar G, Tarr CL. 2013 Evolutionary dynamics of Vibrio cholerae O1 following a singlesource introduction to Haiti. mBio 4(4):e00398-13. http://dx.doi.org/10.1128/mBio.00398-13.
16. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM. 2012. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 6:80-92. http://dx.doi.org/10.4161/fly.19695.
17. Benedict MN, Henriksen JR, Metcalf WW, Whitaker RJ, Price ND. 2014. ITEP: an integrated toolkit for exploration of microbial pan-genomes. BMC Genomics 15:8. http://dx.doi.org/10.1186/1471-2164-15-8.
18. Rissman AI, Mau B, Biehl BS, Darling AE, Glasner JD, Perna NT. 2009. Reordering contigs of draft genomes using the Mauve aligner. Bioinformatics 25:2071-2073. http://dx.doi.org/10.1093/bioinformatics/btp356.
19. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. 2011. PHAST: a fast phage search tool. Nucleic Acids Res 39:W347-W352. http://dx.doi.org/10.1093/nar/gkr485.
20. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121.
21. Chenal-Francisque V, Lopez J, Cantinelli T, Caro V, Tran C, Leclercq A, Lecuit M, Brisse S. 2011. Worldwide distribution of major clones of Listeria monocytogenes. Emerg Infect Dis 17:1110-1112. http://dx.doi.org/10.3201/eid/1706.101778,http://dx.doi.org/10.3201/eid1706.101778.
22. den Bakker HC, Allard MW, Bopp D, Brown EW, Fontana J, Iqbal Z, Kinney A, Limberger R, Musser KA, Shudt M, Strain E, Wiedmann M, Wolfgang WJ. 2014. Rapid whole-genome sequencing for surveillance of Salmonella enterica serovar Enteritidis. Emerg Infect Dis 20:1306-1314. http://dx.doi.org/10.3201/eid2008.131399.
23. Jackson BR, Salter M, Tarr C, Conrad A, Harvey E, Steinbock L, Saupe A, Sorenson A, Katz L, Stroika S, Jackson KA, Carleton H, Kucerova Z, Melka D, Strain E, Parish M, Mody RK, Centers for Disease Control and Prevention. 2015. Notes from the field: listeriosis associated with stone fruit-United States, 2014. MMWR Morb Mortal Wkly Rep 64: 282-283.
24. CDC. 2015. Multistate outbreak of listeriosis linked to Blue Bell Creameries products (final update). Centers for Disease Control and Prevention, Atlanta, GA. http://www.cdc.gov/listeria/outbreaks/ice-cream-03-15/index.html.Accessed 13 October 2015.
25. Chiara M, D'Erchia AM, Manzari C, Minotto A, Montagna C, Addante N, Santagada G, Latorre L, Pesole G, Horner DS, Parisi A. 2014. Draft genome sequences of six Listeria monocytogenes strains isolated from dairy products from a processing plant in southern Italy. Genome Announc 2(2):e00282-14. http://dx.doi.org/10.1128/genomeA.00282-14.
26. Gilmour MW, Graham M, Van Domselaar G, Tyler S, Kent H, Trout-Yakel KM, Larios O, Allen V, Lee B, Nadon C. 2010. High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak. BMC Genomics 11:120. http://dx.doi.org/10.1186/1471-2164-11-120.
27. Orsi RH, Borowsky ML, Lauer P, Young SK, Nusbaum C, Galagan JE, Birren BW, Ivy RA, Sun Q, Graves LM, Swaminathan B, Wiedmann M. 2008 Short-term genome evolution of Listeria monocytogenes in a noncontrolled environment. BMC Genomics 9:539. http://dx.doi.org/10.1186/1471-2164-9-539.
28. Wang Q, Holmes N, Martinez E, Howard P, Hill-Cawthorne G, Sintchenko V. 26 August 2015. It is not all about SNPs: comparison of mobile genetic elements and deletions in Listeria monocytogenes genomes links cases of hospital-acquired listeriosis to the environmental source. J Clin Microbiol http://dx.doi.org/10.1128/JCM.00202-15.
29. den Bakker HC, Cummings CA, Ferreira V, Vatta P, Orsi RH, Degoricija L, Barker M, Petrauskene O, Furtado MR, Wiedmann M. 2010. Comparative genomics of the bacterial genus Listeria: genome evolution is characterized by limited gene acquisition and limited gene loss. BMC Genomics 11:688. http://dx.doi.org/10.1186/1471-2164-11-688.
30. Kuenne C, Billion A, Mraheil MA, Strittmatter A, Daniel R, Goesmann A, Barbuddhe S, Hain T, Chakraborty T. 2013. Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome. BMC Genomics 14:47. http://dx.doi.org/10.1186/1471-2164-14-47.
31. CDC. 1985. Listeriosis outbreak associated with Mexican-style cheese-California. MMWR Morb Mortal Wkly Rep 34:357-359.
32. Nelson KE, Fouts DE, Mongodin EF, Ravel J, DeBoy RT, Kolonay JF, Rasko DA, Angiuoli SV, Gill SR, Paulsen IT, Peterson J, White O, Nelson WC, Nierman W, Beanan MJ, Brinkac LM, Daugherty SC, Dodson RJ, Durkin AS, Madupu R, Haft DH, Selengut J, Van Aken S, Khouri H, Fedorova N, Forberger H, Tran B, Kathariou S, Wonderling LD, Uhlich GA, Bayles DO, Luchansky JB, Fraser CM. 2004. Whole genome comparisons of serotype 4b and 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species. Nucleic Acids Res 32:2386-2395. http://dx.doi.org/10.1093/nar/gkh562.
33. Haase JK, Murphy RA, Choudhury KR, Achtman M. 2011. Revival of Seeliger's historical 'Special Listeria Culture Collection.' Environ Microbiol 13:3163-3171. http://dx.doi.org/10.1111/j.1462-2920.2011.02610.x.
34. Weinmaier T, Riesing M, Rattei T, Bille J, Arguedas-Villa C, Stephan R, Tasara T. 2013. Complete genome sequence of Listeria monocytogenes LL195, a serotype 4b strain from the 1983-1987 listeriosis epidemic in Switzerland. Genome Announc 1(1):e00152-12. http://dx.doi.org/10.1128/genomeA.00152-12.
35. Aureli P, Fiorucci GC, Caroli D, Marchiaro G, Novara O, Leone L, Salmaso S. 2000. An outbreak of febrile gastroenteritis associated with corn contaminated by Listeria monocytogenes. N Engl J Med 342:1236-1241 http://dx.doi.org/10.1056/NEJM200004273421702.
36. den Bakker HC, Desjardins CA, Griggs AD, Peters JE, Zeng Q, Young SK, Kodira CD, Yandava C, Hepburn TA, Haas BJ, Birren BW, Wiedmann M. 2013. Evolutionary dynamics of the accessory genome of Listeria monocytogenes. PLoS One 8:e67511. http://dx.doi.org/10.1371/journal.pone.0067511.
37. Fleming DW, Cochi SL, MacDonald KL, Brondum J, Hayes PS, Plikaytis BD, Holmes MB, Audurier A, Broome CV, Reingold AL. 1985. Pasteurized milk as a vehicle of infection in an outbreak of listeriosis. N Engl J Med 312: 404-407. http://dx.doi.org/10.1056/NEJM198502143120704.
38. Briers Y, Klumpp J, Schuppler M, Loessner MJ. 2011. Genome sequence of Listeria monocytogenes Scott A, a clinical isolate from a food-borne listeriosis outbreak. J Bacteriol 193:4284-4285. http://dx.doi.org/10.1128/JB.05328-11.
39. Schwartz B, Hexter D, Broome CV, Hightower AW, Hirschhorn RB, Porter JD, Hayes PS, Bibb WF, Lorber B, Faris DG. 1989. Investigation of an outbreak of listeriosis: new hypotheses for the etiology of epidemic Listeria monocytogenes infections. J Infect Dis 159:680-685. http://dx.doi.org/10.1093/infdis/159.4.680.
40. Dalton CB, Austin CC, Sobel J, Hayes PS, Bibb WF, Graves LM, Swaminathan B, Proctor ME, Griffin PM. 1997. An outbreak of gastroenteritis and fever due to Listeria monocytogenes in milk. N Engl J Med 336:100-105. http://dx.doi.org/10.1056/NEJM199701093360204.
41. Alonzo F, III, Bobo LD, Skiest DJ, Freitag NE. 2011. Evidence for subpopulations of Listeria monocytogenes with enhanced invasion of cardiac cells. J Med Microbiol 60:423-434. http://dx.doi.org/10.1099/jmm.0.027185-0.
42. McMullen PD, Gillaspy AF, Gipson J, Bobo LD, Skiest DJ, Freitag NE. 2012 Genome sequence of Listeria monocytogenes 07PF0776, a cardiotropic serovar 4b strain. J Bacteriol 194:3552. http://dx.doi.org/10.1128/JB.00616-12.
43. Franciosa G, Pourshaban M, Gianfranceschi M, Aureli P. 1998. Genetic typing of human and food isolates of Listeria monocytogenes from episodes of listeriosis. Eur J Epidemiol 14:205-210. http://dx.doi.org/10.1023/A:1007448210169.
44. CDC. 2011. Outbreak of invasive listeriosis associated with the consumption of hog head cheese-Louisiana, 2010. MMWR Morb Mortal Wkly Rep 60:401-405.
45. Bécavin C, Bouchier C, Lechat P, Archambaud C, Creno S, Gouin E, Wu Z, Kuhbacher A, Brisse S, Pucciarelli MG, Garcia-del Portillo F, Hain T, Portnoy DA, Chakraborty T, Lecuit M, Pizarro-Cerda J, Moszer I, Bierne H, Cossart P. 2014. Comparison of widely used Listeria monocytogenes strains EGD, 10403S, and EGD-e highlights genomic variations underlying differences in pathogenicity. mBio 5:e00969-14. http://dx.doi.org/10.1128/mBio.00969-14.
46. Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, Baquero F, Berche P, Bloecker H, Brandt P, Chakraborty T, Charbit A, Chetouani F, Couve E, de Daruvar A, Dehoux P, Domann E, Dominguez-Bernal G, Duchaud E, Durant L, Dussurget O, Entian KD, Fsihi H, Portillo FG, Garrido P, Gautier L, Goebel W, Gomez-Lopez N, Hain T, Hauf J, Jackson D, Jones LM, Kaerst U, Kreft J, Kuhn M, Kunst F, Kurapkat G, Madueno E, Maitournam A, Vicente JM, Ng E, Nedjari H, Nordsiek G, Novella S, de Pablos B, Perez-Diaz JC, Purcell R, Remmel B, Rose M, Schlueter T, Simoes N, Tierrez A, Vázquez-Boland J-A, Voss H, Wehland J, Cossart P. 2001. Comparative genomics of Listeria species. Science 294:849-852.
47. Olsen SJ, Patrick M, Hunter SB, Reddy V, Kornstein L, MacKenzie WR, Lane K, Bidol S, Stoltman GA, Frye DM, Lee I, Hurd S, Jones TF, LaPorte TN, Dewitt W, Graves L, Wiedmann M, Schoonmaker-Bopp DJ, Huang AJ, Vincent C, Bugenhagen A, Corby J, Carloni ER, Holcomb ME, Woron RF, Zansky SM, Dowdle G, Smith F, Ahrabi-Fard S, Ong AR, Tucker N, Hynes NA, Mead P. 2005. Multistate outbreak of Listeria monocytogenes infection linked to delicatessen turkey meat. Clin Infect Dis 40:962-967. http://dx.doi.org/10.1086/428575.
48. Jackson KA, Biggerstaff M, Tobin-D'Angelo M, Sweat D, Klos R, Nosari J, Garrison O, Boothe E, Saathoff-Huber L, Hainstock L, Fagan RP. 2011 Multistate outbreak of Listeria monocytogenes associated with Mexican-style cheese made from pasteurized milk among pregnant, Hispanic women. J Food Prot 74:949-953. http://dx.doi.org/10.4315/0362-028X.JFP-10-536.
49. Gaul LK, Farag NH, Shim T, Kingsley MA, Silk BJ, Hyytia-Trees E. 2012 Hospital-acquired listeriosis outbreak caused by contaminated diced celery-Texas, 2010. Clin Infect Dis http://dx.doi.org/10.1093/cid/cis817.
50. Holch A, Webb K, Lukjancenko O, Ussery D, Rosenthal BM, Gram L. 2013 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 79:2944-2951. http://dx.doi.org/10.1128/AEM.03715-12.
51. Steele CL, Donaldson JR, Paul D, Banes MM, Arick T, Bridges SM, Lawrence ML. 2011. Genome sequence of lineage III Listeria monocytogenes strain HCC23. J Bacteriol 193:3679-3680. http://dx.doi.org/10.1128/JB.05236-11.
52. Hain T, Ghai R, Billion A, Kuenne CT, Steinweg C, Izar B, Mohamed W, Mraheil MA, Domann E, Schaffrath S, Karst U, Goesmann A, Oehm S, Puhler A, Merkl R, Vorwerk S, Glaser P, Garrido P, Rusniok C, Buchrieser C, Goebel W, Chakraborty T. 2012. Comparative genomics and transcriptomics of lineages I, II, and III strains of Listeria monocytogenes. BMC Genomics 13:144. http://dx.doi.org/10.1186/1471-2164-13-144.
53. Chen J, Xia Y, Cheng C, Fang C, Shan Y, Jin G, Fang W. 2011. Genome sequence of the nonpathogenic Listeria monocytogenes serovar 4a strain M7. J Bacteriol 193:5019-5020. http://dx.doi.org/10.1128/JB.05501-11.
54. den Bakker HC, Bowen BM, Rodriguez-Rivera LD, Wiedmann M. 2012. FSL J1-208, a virulent uncommon phylogenetic lineage IV Listeria monocytogenes strain with a small chromosome size and a putative virulence plasmid carrying internalin-like genes. Appl Environ Microbiol 78:1876-1889 http://dx.doi.org/10.1128/AEM.06969-11.