Genomes of sequence type 121 Listeria monocytogenes strains harbor highly conserved plasmids and prophages

Frontiers in Microbiology

Volumn 6, Issue APR, 2015, Pages

  Schmitz Esser, Stephan ^a   Müller, Anneliese ^a   Stessl, Beatrix ^a   Wagner, Martin ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

Genome; Listeria monocytogenes; Persistence; Plasmid; Prophage; Sequence type 121

Indexed keywords

ARTICLE; BACTERIAL STRAIN; DNA ISOLATION; FOOD INDUSTRY; GENE SEQUENCE; GENETIC ANALYSIS; HABITUAL ADAPTATION; LISTERIA MONOCYTOGENES; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLASMID; POLYMERASE CHAIN REACTION; PROPHAGE; SEQUENCE ANALYSIS; TRANSPOSON;

LISTERIA INNOCUA; LISTERIA MONOCYTOGENES;

EID: 84930938363     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00380     Document Type: Article

References (66)

1. Allerberger, F., and Wagner, M. (2010). Listeriosis: a resurgent foodborne infection. Clin. Microbiol. Infect. 16, 16-23. doi: 10.1111/j.1469-0691.2009.03109.x.
2. Althaus, D., Lehner, A., Brisse, S., Maury, M., Tasara, T., and Stephan, R. (2014). Characterization of Listeria monocytogenes strains isolated during 2011-2013 from human infections in Switzerland. Foodborne Pathog. Dis. 11, 753-758. doi: 10.1089/fpd.2014.1747.
3. Aziz, R. K., Bartels, D., Best, A. A., Dejongh, M., Disz, T., Edwards, R. A., et al. (2008). The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. doi: 10.1186/1471-2164-9-75.
4. Brown Kav, A., Sasson, G., Jami, E., Doron-Faigenboim, A., Benhar, I., and Mizrahi, I. (2012). Insights into the bovine rumen plasmidome. Proc. Natl. Acad. Sci. U.S.A. 109, 5452-5457. doi: 10.1073/pnas.1116410109.
5. Busby, J. N., Panjikar, S., Landsberg, M. J., Hurst, M. R., and Lott, J. S. (2013). The BC component of ABC toxins is an RHS-repeat-containing protein encapsulation device. Nature 501, 547-550. doi: 10.1038/nature12465.
6. Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., et al. (2009). BLAST+: architecture and applications. BMC Bioinformatics 10:421. doi: 10.1186/1471-2105-10-421.
7. Canchaya, C., Giubellini, V., Ventura, M., de los Reyes-Gavilan, C. G., and Margolles, A. (2010). Mosaic-like sequences containing transposon, phage, and plasmid elements among Listeria monocytogenes plasmids. Appl. Environ. Microbiol. 76, 4851-4857. doi: 10.1128/AEM.02799-09.
8. Carpentier, B., and Cerf, O. (2011). Review-persistence of Listeria monocytogenes in food industry equipment and premises. Int. J. Food Microbiol. 145, 1-8. doi: 10.1016/j.ijfoodmicro.2011.01.005.
9. Casey, A., Fox, E. M., Schmitz-Esser, S., Coffey, A., McAuliffe, O., and Jordan, K. (2014). Transcriptome analysis of Listeria monocytogenes exposed to biocide stress reveals a multi-system response involving cell wall synthesis, sugar uptake, and motility. Front. Microbiol. 5:68. doi: 10.3389/fmicb.2014.00068.
10. Chenal-Francisque, V., Lopez, J., Cantinelli, T., Caro, V., Tran, C., Leclercq, A., et al. (2011). Worldwide distribution of major clones of Listeria monocytogenes. Emerging Infect. Dis. 17, 1110-1112. doi: 10.3201/eid/1706.101778.
11. Chiara, M., D'erchia, A. M., Manzari, C., Minotto, A., Montagna, C., Addante, N., et al. (2014). Draft genome sequences of six Listeria monocytogenes strains isolated from dairy products from a processing plant in southern Italy. Genome Announc. 2:e00282-14. doi: 10.1128/genomeA.00282-14.
12. Darling, A. E., Mau, B., and Perna, N. T. (2010). progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5:e11147. doi: 10.1371/journal.pone.0011147.
13. den Bakker, H. C., Cummings, C. A., Ferreira, V., Vatta, P., Orsi, R. H., Degoricija, L., et al. (2010). Comparative genomics of the bacterial genus Listeria: genome evolution is characterized by limited gene acquisition and limited gene loss. BMC Genomics 11:688. doi: 10.1186/1471-2164-11-688.
14. den Bakker, H. C., Desjardins, C. A., Griggs, A. D., Peters, J. E., Zeng, Q., Young, S. K., et al. (2013). Evolutionary dynamics of the accessory genome of Listeria monocytogenes. PLoS ONE 8:e67511. doi: 10.1371/journal.pone.0067511.
15. Denes, T., Vongkamjan, K., Ackermann, H. W., Moreno Switt, A. I., Wiedmann, M., and den Bakker, H. C. (2014). Comparative genomic and morphological analyses of Listeria phages isolated from farm environments. Appl. Environ. Microbiol. 80, 4616-4625. doi: 10.1128/AEM.00720-14.
16. Dorscht, J., Klumpp, J., Bielmann, R., Schmelcher, M., Born, Y., Zimmer, M., et al. (2009). Comparative genome analysis of Listeria bacteriophages reveals extensive mosaicism, programmed translational frameshifting, and a novel prophage insertion site. J. Bacteriol. 191, 7206-7215. doi: 10.1128/JB.01041-09.
17. Dutta, V., Elhanafi, D., and Kathariou, S. (2013). Conservation and distribution of the benzalkonium chloride resistance cassette bcrABC in Listeria monocytogenes. Appl. Environ. Microbiol. 79, 6067-6074. doi: 10.1128/AEM.01751-13.
18. Edlin, G., Lin, L., and Bitner, R. (1977). Reproductive fitness of P1, P2, and Mu lysogens of Escherichia coli. J. Virol. 21, 560-564.
19. Elhanafi, D., Dutta, V., and Kathariou, S. (2010). Genetic characterization of plasmid-associated benzalkonium chloride resistance determinants in a Listeria monocytogenes strain from the 1998-1999 outbreak. Appl. Environ. Microbiol. 76, 8231-8238. doi: 10.1128/AEM.02056-10.
20. Eurosurveillance Editorial, T. (2012). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. Euro Surveill. 17:2597. doi: 10.2903/j.efsa.2012.2597.
21. Ferreira, V., Wiedmann, M., Teixeira, P., and Stasiewicz, M. J. (2014). Listeria monocytogenes persistence in food-associated environments: epidemiology, strain characteristics, and implications for public health. J. Food Prot. 77, 150-170. doi: 10.4315/0362-028X.JFP-13-150.
22. Fortier, L. C., and Sekulovic, O. (2013). Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4, 354-365. doi: 10.4161/viru.24498.
23. Fox, E., Hunt, K., O'brien, M., and Jordan, K. (2011a). Listeria monocytogenes in Irish farmhouse cheese processing environments. Int. J. Food Microbiol. 145(Suppl. 1), S39-S45. doi: 10.1016/j.ijfoodmicro.2010.10.012.
24. Fox, E. M., Leonard, N., and Jordan, K. (2011b). Physiological and transcriptional characterization of persistent and nonpersistent Listeria monocytogenes isolates. Appl. Environ. Microbiol. 77, 6559-6569. doi: 10.1128/AEM.05529-11.
25. Gilmour, M., Graham, M., Van Domselaar, G., Tyler, S., Kent, H., Trout-Yakel, K., et al. (2010). High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak. BMC Genomics 11:120. doi: 10.1186/1471-2164-11-120.
26. Grissa, I., Vergnaud, G., and Pourcel, C. (2007). CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 35, W52-W57. doi: 10.1093/nar/gkm360.
27. Hein, I., Klinger, S., Dooms, M., Flekna, G., Stessl, B., Leclercq, A., et al. (2011). Stress Survival Islet 1 (SSI-1) survey in Listeria monocytogenes reveals an insert common to Listeria innocua in sequence type 121 L. monocytogenes strains. Appl. Environ. Microbiol. 77, 2169-2173. doi: 10.1128/AEM.02159-10.
28. Heuer, H., Abdo, Z., and Smalla, K. (2008). Patchy distribution of flexible genetic elements in bacterial populations mediates robustness to environmental uncertainty. FEMS Microbiol. Ecol. 65, 361-371. doi: 10.1111/j.1574-6941.2008.00539.x.
29. Holch, A., Webb, K., Lukjancenko, O., Ussery, D., Rosenthal, B. M., and 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. doi: 10.1128/AEM.03715-12.
30. Jordan, S. J., Perni, S., Glenn, S., Fernandes, I., Barbosa, M., Sol, M., et al. (2008). Listeria monocytogenes biofilm-associated protein (BapL) may contribute to surface attachment of L. monocytogenes but is absent from many field isolates. Appl. Environ. Microbiol. 74, 5451-5456. doi: 10.1128/AEM.02419-07.
31. Kajfasz, J. K., Martinez, A. R., Rivera-Ramos, I., Abranches, J., Koo, H., Quivey, R. G. Jr., et al. (2009). Role of Clp proteins in expression of virulence properties of Streptococcus mutans. J. Bacteriol. 191, 2060-2068. doi: 10.1128/JB.01609-08.
32. Kastbjerg, V. G., Hein-Kristensen, L., and Gram, L. (2014). Triclosan-induced aminoglycoside-tolerant Listeria monocytogenes isolates can appear as small-colony variants. Antimicrob. Agents Chemother. 58, 3124-3132. doi: 10.1128/AAC.02266-13.
33. Koskiniemi, S., Lamoureux, J. G., Nikolakakis, K. C., T'kint de Roodenbeke, C., Kaplan, M. D., Low, D. A., et al. (2013). RHS proteins from diverse bacteria mediate intercellular competition. Proc. Natl. Acad. Sci. U.S.A. 110, 7032-7037. doi: 10.1073/pnas.1300627110.
34. Kuenne, C., Billion, A., Mraheil, M. A., Strittmatter, A., Daniel, R., Goesmann, A., et al. (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. doi: 10.1186/1471-2164-14-47.
35. Kuenne, C., Voget, S., Pischimarov, J., Oehm, S., Goesmann, A., Daniel, R., et al. (2010). Comparative analysis of plasmids in the genus Listeria. PLoS ONE 5:e12511. doi: 10.1371/journal.pone.0012511.
36. Kwong, W. K., Engel, P., Koch, H., and Moran, N. A. (2014). Genomics and host specialization of honey bee and bumble bee gut symbionts. Proc. Natl. Acad. Sci. U.S.A. 111, 11509-11514. doi: 10.1073/pnas.1405838111.
37. Larsen, M. H., Dalmasso, M., Ingmer, H., Langsrud, S., Malakauskas, M., Mader, A., et al. (2014). Persistence of foodborne pathogens and their control in primary and secondary food production chains. Food Control 44, 92-109. doi: 10.1016/j.foodcont.2014.03.039.
38. Larsen, M. V., Cosentino, S., Rasmussen, S., Friis, C., Hasman, H., Marvig, R. L., et al. (2012). Multilocus sequence typing of total-genome-sequenced bacteria. J. Clin. Microbiol. 50, 1355-1361. doi: 10.1128/JCM.06094-11.
39. Lebrun, M., Audurier, A., and Cossart, P. (1994a). Plasmid-borne cadmium resistance genes in Listeria monocytogenes are present on Tn5422, a novel transposon closely related to Tn917. J. Bacteriol. 176, 3049-3061.
40. Lebrun, M., Audurier, A., and Cossart, P. (1994b). Plasmid-borne cadmium resistance genes in Listeria monocytogenes are similar to cadA and cadC of Staphylococcus aureus and are induced by cadmium. J. Bacteriol. 176, 3040-3048.
41. Lee, S., Ward, T. J., Siletzky, R. M., and Kathariou, S. (2012). Two novel type II restriction-modification systems occupying genomically equivalent locations on the chromosomes of Listeria monocytogenes strains. Appl. Environ. Microbiol. 78, 2623-2630. doi: 10.1128/AEM.07203-11.
42. Lopez-Alonso, V., Ortiz, S., and Martinez-Suarez, J. V. (2015). Genome sequences of five disinfectant-resistant Listeria monocytogenes strains from two Iberian pork-processing plants. Genome Announc. 3:e00077-15. doi: 10.1128/genomeA.00077-15.
43. Martin, B., Perich, A., Gomez, D., Yanguela, J., Rodriguez, A., Garriga, M., et al. (2014). Diversity and distribution of Listeria monocytogenes in meat processing plants. Food Microbiol. 44, 119-127. doi: 10.1016/j.fm.2014.05.014.
44. Muller, A., Rychli, K., Muhterem-Uyar, M., Zaiser, A., Stessl, B., Guinane, C. M., et al. (2013). Tn6188-a novel transposon in Listeria monocytogenes responsible for tolerance to benzalkonium chloride. PLoS ONE 8:e76835. doi: 10.1371/journal.pone.0076835.
45. Muller, A., Rychli, K., Zaiser, A., Wieser, C., Wagner, M., and Schmitz-Esser, S. (2014). The Listeria monocytogenes transposon Tn6188 provides increased tolerance to various quaternary ammonium compounds and ethidium bromide. FEMS Microbiol. Lett. 361, 166-173. doi: 10.1111/1574-6968.12626.
46. Nightingale, K. K., Ivy, R. A., Ho, A. J., Fortes, E. D., Njaa, B. L., Peters, R. M., et al. (2008). inlA premature stop codons are common among Listeria monocytogenes isolates from foods and yield virulence-attenuated strains that confer protection against fully virulent strains. Appl. Environ. Microbiol. 74, 6570-6583. doi: 10.1128/AEM.00997-08.
47. Orsi, R. H., Borowsky, M. L., Lauer, P., Young, S. K., Nusbaum, C., Galagan, J. E., et al. (2008). Short-term genome evolution of Listeria monocytogenes in a non-controlled environment. BMC Genomics 9:539. doi: 10.1186/1471-2164-9-539.
48. Ortiz, S., Lopez, V., and Martinez-Suarez, J. V. (2014). Control of Listeria monocytogenes contamination in an Iberian pork processing plant and selection of benzalkonium chloride-resistant strains. Food Microbiol. 39, 81-88. doi: 10.1016/j.fm.2013.11.007.
49. Ortiz, S., Lopez, V., Villatoro, D., Lopez, P., Davila, J. C., and Martinez-Suarez, J. N. (2010). A 3-year surveillance of the genetic diversity and persistence of Listeria monocytogenes in an Iberian pig slaughterhouse and processing plant. Foodborne Pathog. Dis. 7, 1177-1184. doi: 10.1089/fpd.2010.0535.
50. Overbeek, R., Olson, R., Pusch, G. D., Olsen, G. J., Davis, J. J., Disz, T., et al. (2014). The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res. 42, D206-D214. doi: 10.1093/nar/gkt1226.
51. Parisi, A., Latorre, L., Normanno, G., Miccolupo, A., Fraccalvieri, R., Lorusso, V., et al. (2010). Amplified fragment length polymorphism and multi-locus sequence typing for high-resolution genotyping of Listeria monocytogenes from foods and the environment. Food Microbiol. 27, 101-108. doi: 10.1016/j.fm.2009.09.001.
52. Ragon, M., Wirth, T., Hollandt, F., Lavenir, R., Lecuit, M., Le Monnier, A., et al. (2008). A new perspective on Listeria monocytogenes evolution. PLoS Pathog. 4:e1000146. doi: 10.1371/journal.ppat.1000146.
53. Ryan, S., Begley, M., Hill, C., and Gahan, C. G. (2010). A five-gene stress survival islet (SSI-1) that contributes to the growth of Listeria monocytogenes in suboptimal conditions. J. Appl. Microbiol. 109, 984-995. doi: 10.1111/j.1365-2672.2010.04726.x.
54. Sauders, B. D., and Wiedmann, M. (2007). "Ecology of Listeria species and L. monocytogenes in the natural environment," in Listeria, Listeriosis and Food Safety, 3rd Edn., eds E. T. Ryser and E. H. Marth (Boca Raton, FL: CRC Press), 21-53.
55. Sesto, N., Touchon, M., Andrade, J. M., Kondo, J., Rocha, E. P., Arraiano, C. M., et al. (2014). A PNPase dependent CRISPR System in Listeria. PLoS Genet. 10:e1004065. doi: 10.1371/journal.pgen.1004065.
56. Spinelli, S. L., Kierzek, R., Turner, D. H., and Phizicky, E. M. (1999). Transient ADP-ribosylation of a 2'-phosphate implicated in its removal from ligated tRNA during splicing in yeast. J. Biol. Chem. 274, 2637-2644. doi: 10.1074/jbc.274.5.2637.
57. Stessl, B., Fricker, M., Fox, E., Karpiskova, R., Demnerova, K., Jordan, K., et al. (2014). Collaborative survey on the colonization of different types of cheese-processing facilities with Listeria monocytogenes. Foodborne Pathog. Dis. 11, 8-14. doi: 10.1089/fpd.2013.1578.
58. Suokko, A., Savijoki, K., Malinen, E., Palva, A., and Varmanen, P. (2005). Characterization of a mobile clpL gene from Lactobacillus rhamnosus. Appl. Environ. Microbiol. 71, 2061-2069. doi: 10.1128/AEM.71.4.2061-2069.2005.
59. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197.
60. Tao, L., and Biswas, I. (2013). ClpL is required for folding of CtsR in Streptococcus mutans. J. Bacteriol. 195, 576-584. doi: 10.1128/JB.01743-12.
61. Tran, T. D., Kwon, H. Y., Kim, E. H., Kim, K. W., Briles, D. E., Pyo, S., et al. (2011). Decrease in penicillin susceptibility due to heat shock protein ClpL in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 55, 2714-2728. doi: 10.1128/AAC.01383-10.
62. Vallenet, D., Belda, E., Calteau, A., Cruveiller, S., Engelen, S., Lajus, A., et al. (2013). MicroScope-an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Nucleic Acids Res. 41, D636-D647. doi: 10.1093/nar/gks1194.
63. Van Stelten, A., Simpson, J. M., Ward, T. J., and Nightingale, K. K. (2010). 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. 76, 2783-2790. doi: 10.1128/AEM.02651-09.
64. Verghese, B., Lok, M., Wen, J., Alessandria, V., Chen, Y., Kathariou, S., et al. (2011). 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. 77, 3279-3292. doi: 10.1128/AEM.00546-11.
65. Wang, G. Y., Qian, W. J., Zhang, X. X., Wang, H. H., Ye, K. P., Bai, Y., et al. (2015). Prevalence, genetic diversity and antimicrobial resistance of Listeria monocytogenes isolated from ready-to-eat meat products in Nanjing, China. Food Control 50, 202-208. doi: 10.1016/j.foodcont.2014.07.057.
66. Wang, X., Kim, Y., Ma, Q., Hong, S. H., Pokusaeva, K., Sturino, J. M., et al. (2010). Cryptic prophages help bacteria cope with adverse environments. Nat. Commun. 1:147. doi: 10.1038/ncomms1146.