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Genetic Organization of ascB-dapE Internalin Cluster Serves as a Potential Marker for Listeria monocytogenes Sublineages IIA, IIB, and IIC

  • Chen, Jianshun (Zhejiang University Institute of Preventive Veterinary Medicine, and Zhejiang Provincial Key Laboratory of Preventive Veterinary Medicine) ;
  • Fang, Chun (Zhejiang University Institute of Preventive Veterinary Medicine, and Zhejiang Provincial Key Laboratory of Preventive Veterinary Medicine) ;
  • Zhu, Ningyu (Zhejiang Fisheries Technical Extension Center) ;
  • Lv, Yonghui (National Fisheries Technical Extension Center) ;
  • Cheng, Changyong (Zhejiang University Institute of Preventive Veterinary Medicine, and Zhejiang Provincial Key Laboratory of Preventive Veterinary Medicine) ;
  • Bei, Yijiang (Zhejiang Fisheries Technical Extension Center) ;
  • Zheng, Tianlun (Zhejiang Fisheries Technical Extension Center) ;
  • Fang, Weihuan (Zhejiang University Institute of Preventive Veterinary Medicine, and Zhejiang Provincial Key Laboratory of Preventive Veterinary Medicine)
  • Received : 2011.10.17
  • Accepted : 2012.01.08
  • Published : 2012.05.28

Abstract

Listeria monocytogenes is an important foodborne pathogen that comprises four genetic lineages: I, II, III, and IV. Of these, lineage II is frequently recovered from foods and environments and responsible for the increasing incidence of human listeriosis. In this study, the phylogenetic structure of lineage II was determined through sequencing analysis of the ascB-dapE internalin cluster. Fifteen sequence types proposed by multilocus sequence typing based on nine housekeeping genes were grouped into three distinct sublineages, IIA, IIB, and IIC. Organization of the ascB-dapE internalin cluster could serve as a molecular marker for these sublineages, with inlGHE, inlGC2DE, and inlC2DE for IIA, IIB, and IIC, respectively. These sublineages displayed specific genetic and phenotypic characteristics. IIA and IIC showed a higher frequency of recombination (${\rho}/{\theta}$). However, recombination events had greater effect (r/m) on IIB, leading to its high nucleotide diversity. Moreover, IIA and IIB harbored a wider range of internalin and stress-response genes, and possessed higher nisin tolerance, whereas IIC contained the largest portion of low-virulent strains owing to premature stop codons in inlA. The results of this study indicate that IIA, IIB, and IIC might occupy different ecological niches, and IIB might have a better adaptation to a broad range of environmental niches.

Keywords

References

  1. Abe, K., H. Hayashi, and P. C. Maloney. 1996. Exchange of aspartate and alanine. Mechanism for development of a protonmotive force in bacteria. J. Biol. Chem. 271: 3079-3084. https://doi.org/10.1074/jbc.271.6.3079
  2. Allerberger, F. and M. Wagner. 2010. Listeriosis: A resurgent foodborne infection. Clin. Microbiol. Infect. 16: 16-23. https://doi.org/10.1111/j.1469-0691.2009.03109.x
  3. Autret, N., I. Dubail, P. Trieu-Cuot, P. Berche, and A. Charbit. 2001. Identification of new genes involved in the virulence of Listeria monocytogenes by signature-tagged transposon mutagenesis. Infect. Immun. 69: 2054-2065. https://doi.org/10.1128/IAI.69.4.2054-2065.2001
  4. Bakker, H. C., X. Didelot, E. D. Fortes, K. K. Nightingale, and M. Wiedmann. 2008. Lineage specific rates and microevolution in Listeria monocytogenes. BMC Evol. Biol. 8: 277. https://doi.org/10.1186/1471-2148-8-277
  5. Begley, M., P. D. Cotter, C. Hill, and R. P. Ross. 2010. Glutamate decarboxylase-mediated nisin resistance in Listeria monocytogenes. Appl. Environ. Microbiol. 76: 6541-6546. https://doi.org/10.1128/AEM.00203-10
  6. Bierne, H., C. Sabet, N. Personnic, and P. Cossart. 2007. Internalins: A complex family of leucine-rich repeat-containing proteins in Listeria monocytogenes. Microbes Infect. 9: 1156-1166. https://doi.org/10.1016/j.micinf.2007.05.003
  7. Bille, J., D. S. Blanc, H. Schmid, K. Boubaker, A. Baumgartner, H. H. Siegrist, et al. 2006. Outbreak of human listeriosis associated with Tomme cheese in northwest Switzerland, 2005. Euro. Surveill. 11: 91-93.
  8. Bonnet, M., M. M. Rafi, M. L. Chikindas, and T. J. Montville. 2006. Bioenergetic mechanism for nisin resistance, induced by the acid tolerance response of Listeria monocytogenes. Appl. Environ. Microbiol. 72: 2556-2563. https://doi.org/10.1128/AEM.72.4.2556-2563.2006
  9. Chen, J., X. Zhang, L. Mei, L. Jiang, and W. Fang. 2009. Prevalence of Listeria in Chinese food products from 13 provinces between 2000 and 2007 and virulence characterization of Listeria monocytogenes isolates. Foodborne Pathog. Dis. 6: 7-14. https://doi.org/10.1089/fpd.2008.0139
  10. Chen, J., L. Jiang, Q. Chen, H. Zhao, X. Luo, X. Chen, and W. Fang. 2009. lmo0038 is involved in acid and heat stress responses and specific for L. monocytogenes lineages I and II, and L. ivanovii. Foodborne Pathog. Dis. 6: 365-376. https://doi.org/10.1089/fpd.2008.0207
  11. Chen, J., X. Luo, L. Jiang, P. Jin, W. Wei, D. Liu, and W. Fang. 2009. Molecular characteristics and virulence potential of Listeria monocytogenes isolates from Chinese food systems. Food Microbiol. 26: 103-111. https://doi.org/10.1016/j.fm.2008.08.003
  12. Chen, J., L. Jiang, X. Chen, X. Luo, Y. Chen, Y. Yu, et al. 2009. Listeria monocytogenes serovar 4a is a possible evolutionary intermediate between L. monocytogenes serovars 1/2a and 4b and L. innocua. J. Microbiol. Biotechnol. 19: 238-249.
  13. Chen, J., Q. Chen, L. Jiang, C. Cheng, F. Bai, J. Wang, et al. 2010. Internalin profiling and multilocus sequence typing suggest four Listeria innocua subgroups with different evolutionary distances from Listeria monocytogenes. BMC Microbiol. 10: 97. https://doi.org/10.1186/1471-2180-10-97
  14. Chen, J., Q. Chen, J. Jiang, H. Hu, J. Ye, and W. Fang. 2010. Serovar 4b complex predominates among Listeria monocytogenes isolates from imported aquatic products in China. Foodborne Pathog. Dis. 7: 31-41. https://doi.org/10.1089/fpd.2009.0353
  15. Chen, J., C. Cheng, Y. Xia, H. Zhao, C. Fang, Y. Shan, et al. 2011. Lmo0036, an ornithine and putrescine carbamoyltransferase in Listeria monocytogenes, participates in arginine deiminase and agmatine deiminase pathways and mediates acid tolerance. Microbiology 157: 3150-3161. https://doi.org/10.1099/mic.0.049619-0
  16. Chen, J., C. Fang, T. Zheng, N. Zhu, Y. Bei, and W. Fang. 2012. Genomic presence of GadD1 glutamate decarboxylase correlates with the organization of ascB-dapE internalin cluster in Listeria monocytogenes. Foodborne Pathog. Dis. 9: 175-178. https://doi.org/10.1089/fpd.2011.1022
  17. Clark, C. G., J. Farber, F. Pagotto, N. Ciampa, K. Doré, C. Nadon, et al. 2010. Surveillance for Listeria monocytogenes and listeriosis, 1995-2004. Epidemiol. Infect. 138: 559-572. https://doi.org/10.1017/S0950268809990914
  18. Cotter, P. D., C. G. Gahan, and C. Hill. 2001. A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Mol. Microbiol. 40: 465-475. https://doi.org/10.1046/j.1365-2958.2001.02398.x
  19. Cotter, P. D., S. Ryan, C. G. Gahan, and C. Hill. 2005. Presence of GadD1 glutamate decarboxylase in selected Listeria monocytogenes strains is associated with an ability to grow at low pH. Appl. Environ. Microbiol. 71: 2832-2839. https://doi.org/10.1128/AEM.71.6.2832-2839.2005
  20. Dawson, S. J., M. R. Evans, D. Willby, J. Bardwell, N. Chamberlain, and D. A. Lewis. 2006. Listeria outbreak associated with sandwich consumption from a hospital retail shop, United Kingdom. Euro. Surveill. 11: 89-91.
  21. Didelot, X. and D. Falush. 2007. Inference of bacterial microevolution using multilocus sequence data. Genetics 175: 1251-1266.
  22. Doumith, M., C. Cazalet, N. Simoes, L. Frangeul, C. Jacquet, F. Kunst, et al. 2004. New aspects regarding evolution and virulence of Listeria monocytogenes revealed by comparative genomics and DNA arrays. Infect. Immun. 72: 1072-1083. https://doi.org/10.1128/IAI.72.2.1072-1083.2004
  23. Fretz, R., J. Pichler, U. Sagel, P. Much, W. Ruppitsch, A. T. Pietzka, et al. 2010. Update: Multinational listeriosis outbreak due to 'Quargel', a sour milk curd cheese, caused by two different L. monocytogenes serotype 1/2a strains, 2009-2010. Euro. Surveill 15: 19543.
  24. Gilmour, M. W., M. Graham, G. V. Domselaar, S. Tyler, H. Kent, K. M. Trout-Yakel, et al. 2010. High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak. BMC Genomics 11: 120. https://doi.org/10.1186/1471-2164-11-120
  25. Gray, M. J., R. N. Zadoks, E. D. Fortes, B. Dogan, S. Cai, Y. Chen, et al. 2004. Listeria monocytogenes isolates from foods and humans form distinct but overlapping populations. Appl. Environ. Microbiol. 70: 5833-5841. https://doi.org/10.1128/AEM.70.10.5833-5841.2004
  26. Guttman, D. S. and D. E. Dykhuizen. 1994. Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 266: 1380-1383. https://doi.org/10.1126/science.7973728
  27. Higuchi, T., H. Hayashi, and K. Abe. 1997. Exchange of glutamate and gamma-aminobutyrate in a Lactobacillus strain. Appl. Environ. Microbiol. 179: 3362-3364.
  28. Jacquet, C., M. Doumith, J. I. Gordon, P. M. Martin, P. Cossart, and M. Lecuit. 2004. A molecular marker for evaluating the pathogenic potential of foodborne Listeria monocytogenes. J Infect. Dis. 189: 2094-2100. https://doi.org/10.1086/420853
  29. Kathariou, S. 2002. Listeria monocytogenes virulence and pathogenicity, a food safety perspective. J. Food Prot. 65: 1811-1829.
  30. Kirchner, M. and D. E. Higgins. 2008. Inhibition of ROCK activity allows InlF-mediated invasion and increased virulence of Listeria monocytogenes. Mol. Microbiol. 68: 749-767. https://doi.org/10.1111/j.1365-2958.2008.06188.x
  31. Leistner, L. 2000. Basic aspects of food preservation by hurdle technology. Int. J. Food Microbiol. 55: 181-186. https://doi.org/10.1016/S0168-1605(00)00161-6
  32. Liu, D. 2006. Identification, subtyping and virulence determination of Listeria monocytogenes, an important foodborne pathogen. J. Med. Microbiol. 55: 645-659. https://doi.org/10.1099/jmm.0.46495-0
  33. Liu, D., M. L. Lawrence, M. Wiedmann, L. Gorski, R. E. Mandrell, A. J. Ainsworth, and F. K. Austin. 2006. Listeria monocytogenes subgroups IIIA, IIIB, and IIIC delineate genetically distinct populations with varied pathogenic potential. J. Clin. Microbiol. 44: 4229-4233. https://doi.org/10.1128/JCM.01032-06
  34. Milkman, R. and M. Bridges. 1990. Molecular evolution of the Escherichia coli chromosome. III. Clonal frames. Genetics 126: 505-517.
  35. Milillo, S. R. and M. Wiedmann. 2009. Contributions of six lineage-specific internalin-like genes to invasion efficiency of Listeria monocytogenes. Foodborne Pathog. Dis. 6: 57-70. https://doi.org/10.1089/fpd.2008.0140
  36. Molenaar, D., J. S. Bosscher, B. ten Brink, A. J. Driessen, and W. N. Konings. 1993. Generation of a proton motive force by histidine decarboxylation and electrogenic histidine/histamine antiport in Lactobacillus buchneri. J. Bacteriol. 175: 8264-2870.
  37. Nielsen, R. 2001. Statistical tests of selective neutrality in the age of genomics. Heredity 86: 641-647. https://doi.org/10.1046/j.1365-2540.2001.00895.x
  38. Nightingale, K., K. Windham, and M. Wiedmann. 2005. Evolution and molecular phylogeny of Listeria monocytogenes isolated from human and animal listeriosis cases and foods. J. Bacteriol. 187: 5537-5551. https://doi.org/10.1128/JB.187.16.5537-5551.2005
  39. Orsi, R. H., H. C. den Bakker, and M. Wiedmann. 2010. Listeria monocytogenes lineages: Genomics, evolution, ecology, and phenotypic characteristics. Int. J. Med. Microbiol. 301: 79-96.
  40. Parihar, V. S., G. Lopez-Valladares, M. L. Danielsson-Tham, I. Peiris, S. Helmersson, M. Unemo, et al. 2008. Characterization of human invasive isolates of Listeria monocytogenes in Sweden, 1986-2007. Foodborne Pathog. Dis. 5: 755-761. https://doi.org/10.1089/fpd.2008.0123
  41. Perez-Losada, M., E. B. Browne, A. Madsen, T. Wirth, R. P. Viscidi, and K. A. Crandall. 2006. Population genetics of microbial pathogens estimated from multilocus sequence typing (MLST) data. Infect. Genet. Evol. 6: 97-112. https://doi.org/10.1016/j.meegid.2005.02.003
  42. Ragon, M., T. Wirth, F. Hollandt, R. Lavenir, M. Lecuit, A. L. Monnier, and S. Brisse. 2008. A new perspective on Listeria monocytogenes evolution. PLoS Pathog. 4: 1-14.
  43. Ross, A. I., M. W. Griffiths, G. S. Mittal, and H. C. Deeth. 2003. Combining nonthermal technologies to control foodborne microorganisms. Int. J. Food Microbiol. 89: 125-138. https://doi.org/10.1016/S0168-1605(03)00161-2
  44. Rozas, J., J. Sunchez-DelBarrio, X. Messeguer, and R. Rozas. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497. https://doi.org/10.1093/bioinformatics/btg359
  45. Simonsen, K., G. Churchill, and C. Aquadro. 1995. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141: 413-429.
  46. Swaminathan, B. and P. Gerner-Smidt. 2007. The epidemiology of human listeriosis. Microbes Infect. 9: 1236-1243. https://doi.org/10.1016/j.micinf.2007.05.011
  47. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
  48. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599. https://doi.org/10.1093/molbev/msm092
  49. Urwin, R. and M. C. J. Maiden. 2003. Multi-locus sequence typing: A tool for global epidemiology. Trends Microbiol. 11: 479-487. https://doi.org/10.1016/j.tim.2003.08.006
  50. van Stelten, A. and K. K. Nightingale. 2008. Development and implementation of a multiplex single-nucleotide polymorphism genotyping assay for detection of virulence-attenuating mutations in the Listeria monocytogenes virulence-associated gene inlA. Appl. Environ. Microbiol. 74: 7365-7375. https://doi.org/10.1128/AEM.01138-08
  51. van Stelten, A., J. M. Simpson, T. J. Ward, and K. K. Nightingale. 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. https://doi.org/10.1128/AEM.02651-09
  52. Ward, T. J., T. F. Ducey, T. Usgaard, K. A. Dunn, and J. P. Bielawski. 2008. Multilocus genotyping assays for single nucleotide polymorphism-based subtyping of Listeria monocytogenes isolates. Appl. Environ. Microbiol. 74: 7629-7642. https://doi.org/10.1128/AEM.01127-08
  53. Ward, T. J., P. Evans, M. Wiedmann, T. Usgaard, S. E. Roof, S. G. Stroika, and K. Hise. 2010. Molecular and phenotypic characterization of Listeria monocytogenes from U.S. Department of Agriculture Food Safety and Inspection Service surveillance of ready-to-eat foods and processing facilities. J. Food Prot. 73: 861-869.
  54. Wiedmann, M., J. L. Bruce, C. Keatine, A. E. Johnson, P. L. McDonough, and C. A. Batt. 1997. Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potential. Infect. Immun. 65: 2707-2716.
  55. Wirth, T., D. Falush, R. Lan, F. Colles, P. Mensa, L. Wieler, et al. 2006. Sex and virulence in Escherichia coli: An evolutionary perspective. Mol. Microbiol. 60: 1136-1151. https://doi.org/10.1111/j.1365-2958.2006.05172.x
  56. Zhang, W., B. M. Jayarao, and S. J. Knabel. 2004. Multi-virulence-locus sequence typing of Listeria monocytogenes. Appl. Environ. Microbiol. 70: 913-920. https://doi.org/10.1128/AEM.70.2.913-920.2004

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