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Research article

Molecular Biology and Omics

Comparative Genomic Analysis Reveals That the 20K and 38K Prophages in Listeria monocytogenes Serovar 4a Strains Lm850658 and M7 Contribute to Genetic Diversity but Not to Virulence

Chun Fang 1, Tong Cao 1, Ying Shan 1, Ye Xia 1, Yongping Xin 1, Changyong Cheng 2, Houhui Song 2, John Bowman 3, Xiaoliang Li 1, Xiangyang Zhou 4 and Weihuan Fang 1, 2*

1Zhejiang University Institute of Preventive Veterinary Medicine, and Zhejiang Provincial Key Laboratory of Preventive Veterinary Medicine, Hangzhou, Zhejiang 310058, P.R. China, 2College of Animal Science and Technology, Zhejiang A&F University, Lin'an, Zhejiang 311300, P.R. China, 3School of Agricultural Science, University of Tasmania, Hobart 7001, Tasmania, Australia, 4Zhoushan Entry-Exit Inspection and Quarantine Bureau, Zhoushan, Zhejiang 316000, P.R. China

Received: April 28, 2015; Accepted: October 13, 2015

J. Microbiol. Biotechnol. 2016; 26(1): 197-206

Published January 28, 2016 https://doi.org/10.4014/jmb.1504.04075

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Listeria monocytogenes is a foodborne pathogen of considerable genetic diversity with varying pathogenicity. Initially, we found that the strain M7 was far less pathogenic than the strain Lm850658 though both are serovar 4a strains belonging to the lineage III. Comparative genomic approaches were then attempted to decipher the genetic basis that might govern the strain-dependent pathotypes. There are 2,761 coding sequences of 100% nucleotide identity between the two strains, accounting for 95.7% of the total genes in Lm850658 and 92.7% in M7. Lm850658 contains 33 specific genes, including a novel 20K prophage whereas strain M7 has 130 specific genes, including two large prophages (38K and 44K). To examine the roles of these specific prophages in pathogenicity, the 20K and 38K prophages were deleted from their respective strains. There were virtually no differences of pathogenicity between the deletion mutants and their parent strains, although some putative virulent factors like VirB4 are present in the 20K region or holin-lysin in the 38K region. In silico PCR analysis of 29 listeria genomes show that only strain SLCC2540 has the same 18 bp integration hotspot as Lm850658, whereas the sequence identity of their 20K prophages is very low (21.3%). The 38K and 44K prophages are located in two other different hotspots and are conserved in low virulent strains M7, HCC23, and L99. In conclusion, the 20K and 38K prophages of L. monocytogenes serovar 4a strains Lm850658 and M7 are not related to virulence but contribute to genetic diversity.

Keywords

Listeria monocytogenes, Prophage, Genetic diversity, Virulence

References

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    Pubmed PMC
  2. Braun L, Dramsi S, Dehoux P, Bierne H, Lindahl G, Cossart P. 1997. InlB: an invasion protein of Listeria monocytogenes with a novel type of surface association. Mol. Microbiol. 25: 285-294.
    Pubmed CrossRef
  3. Brussow H, Canchaya C, Hardt WD. 2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68: 560-602.
    Pubmed PMC CrossRef
  4. Camilli A, Tilney LG, Portnoy DA. 1993. Dual roles of plcA in Listeria monocytogenes pathogenesis. Mol. Microbiol. 8: 143-157.
    Pubmed PMC CrossRef
  5. Chen J, Chen Q, Jiang L, Cheng C, Bai F, Wang J, 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.
    Pubmed PMC CrossRef
  6. Chen J, Cheng C, Xia Y, Zhao H, Fang C, Shan Y, 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.
    Pubmed CrossRef
  7. Chen J, Jiang L, Chen Q, Zhao H, Luo X, Chen X, Fang W. 2009. Lmo0038 is involved in acid and heat stress responses and specific for Listeria monocytogenes lineages I and II, and Listeria ivanovii. Foodborne Pathog. Dis. 6: 365-376.
    Pubmed CrossRef
  8. 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.
    Pubmed PMC CrossRef
  9. Chung IY, Jang HJ, Bae HW, Cho YH. 2014. A phage protein that inhibits the bacterial ATPase required for type IV pilus assembly. Proc. Natl. Acad. Sci. USA 111: 11503-11508.
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  10. Coleman D, Knights J, Russell R, Shanley D, Birkbeck TH, Dougan G, Charles I. 1991. Insertional inactivation of the Staphylococcus aureus beta-toxin by bacteriophage phi 13 occurs by site- and orientation-specific integration of the phi 13 genome. Mol. Microbiol. 5: 933-939.
    Pubmed CrossRef
  11. DeBardeleben HK, Lysenko ES, Dalia AB, Weiser JN. 2014. Tolerance of a phage element by Streptococcus pneumoniae leads to a fitness defect during colonization. J. Bacteriol. 196:2670-2680.
    Pubmed PMC CrossRef
  12. 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.
    Pubmed PMC CrossRef
  13. Deng X, Phillippy AM, Li Z, Salzberg SL, Zhang W. 2010. Probing the pan-genome of Listeria monocytogenes: new insights into intraspecific niche expansion and genomic diversification. BMC Genomics 11: 500.
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    Pubmed
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    CrossRef
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  20. Hain T, Steinweg C, Chakraborty T. 2006. Comparative and functional genomics of Listeria spp. J. Biotechnol. 126: 37-51.
    Pubmed CrossRef
  21. Hamon M, Bierne H, Cossart P. 2006. Listeria monocytogenes: a multifaceted model. Nat. Rev. Microbiol. 4: 423-434.
    Pubmed CrossRef
  22. Jiang LL, Xu JJ, Chen N, Shuai JB, Fang WH. 2006. Virulence phenotyping and molecular characterization of a low-pathogenicity isolate of Listeria monocytogenes from cow’s milk. Acta Biochim. Biophys. Sin. (Shanghai) 38: 262-270.
    CrossRef
  23. Jonquieres R, Bierne H, Fiedler F, Gounon P, Cossart P. 1999. Interaction between the protein InlB of Listeria monocytogenes and lipoteichoic acid: a novel mechanism of protein association at the surface of gram-positive bacteria. Mol. Microbiol. 34: 902-914.
    Pubmed CrossRef
  24. Kahrstrom CT. 2014. Structural biology: solving the T4SS structural mystery. Nat. Rev. Microbiol. 12: 312.
    Pubmed CrossRef
  25. Kapyrina NA. 1971. [Prophage induction in Listeria monocytogenes]. Veterinariia 9: 39-41.
    Pubmed
  26. Kuenne C, Billion A, Mraheil MA, 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.
    Pubmed PMC CrossRef
  27. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35: 3100-3108.
    Pubmed PMC CrossRef
  28. Liu D. 2004. Listeria monocytogenes: comparative interpretation of mouse virulence assay. FEMS Microbiol. Lett. 233: 159-164.
    Pubmed CrossRef
  29. Liu D, Lawrence ML, Wiedmann M, Gorski L, Mandrell RE, Ainsworth AJ, Austin FW. 2006. Listeria monocytogenes subgroups IIIA, IIIB, and IIIC delineate genetically distinct populations with varied pathogenic potential. J. Clin. Microbiol. 44: 4229-4233.
    Pubmed PMC CrossRef
  30. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.
    Pubmed PMC CrossRef
  31. Monk IR, Gahan CG, Hill C. 2008. Tools for functional postgenomic analysis of Listeria monocytogenes. Appl. Environ. Microbiol. 74: 3921-3934.
    Pubmed PMC CrossRef
  32. Orsi RH, Borowsky ML, Lauer P, Young SK, Nusbaum C, Galagan JE, et al. 2008. Short-term genome evolution of Listeria monocytogenes in a non-controlled environment. BMC Genomics 9: 539.
    Pubmed PMC CrossRef
  33. Paredes-Cervantes V, Flores-Mejia R, Moreno-Lafont MC, Lanz-Mendoza H, Tello-Lopez AT, Castillo-Vera J, et al. 2011. Comparative proteome analysis of Brucella abortus 2308 and its virB type IV secretion system mutant reveals new T4SS-related candidate proteins. J. Proteomics 74: 2959-2971.
    Pubmed CrossRef
  34. 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.
    Pubmed PMC CrossRef
  35. Roberts A, Nightingale K, Jeffers G, Fortes E, Kongo JM, Wiedmann M. 2006. Genetic and phenotypic characterization of Listeria monocytogenes lineage III. Microbiology 152: 685-693.
    Pubmed CrossRef
  36. Schaferkordt S, Chakraborty T. 1997. Identification, cloning, and characterization of the Ima operon, whose gene products are unique to Listeria monocytogenes. J. Bacteriol. 179: 2707-2716.
    Pubmed PMC
  37. Schattner P, Brooks AN, Lowe TM. 2005. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 33: W686-W689.
    Pubmed PMC CrossRef
  38. 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.
    Pubmed PMC CrossRef
  39. Stelma GN Jr, Reyes AL, Peeler JT, Francis DW, Hunt JM, Spaulding PL, et al. 1987. Pathogenicity test for Listeria monocytogenes using immunocompromised mice. J. Clin. Microbiol. 25: 2085-2089.
    Pubmed PMC
  40. Sun AN, Camilli A, Portnoy DA. 1990. Isolation of Listeria monocytogenes small-plaque mutants defective for intracellular growth and cell-to-cell spread. Infect. Immun. 58: 3770-3778.
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    Pubmed PMC CrossRef
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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(1): 197-206

Published online January 28, 2016 https://doi.org/10.4014/jmb.1504.04075

Copyright © The Korean Society for Microbiology and Biotechnology.

Comparative Genomic Analysis Reveals That the 20K and 38K Prophages in Listeria monocytogenes Serovar 4a Strains Lm850658 and M7 Contribute to Genetic Diversity but Not to Virulence

Chun Fang 1, Tong Cao 1, Ying Shan 1, Ye Xia 1, Yongping Xin 1, Changyong Cheng 2, Houhui Song 2, John Bowman 3, Xiaoliang Li 1, Xiangyang Zhou 4 and Weihuan Fang 1, 2*

1Zhejiang University Institute of Preventive Veterinary Medicine, and Zhejiang Provincial Key Laboratory of Preventive Veterinary Medicine, Hangzhou, Zhejiang 310058, P.R. China, 2College of Animal Science and Technology, Zhejiang A&F University, Lin'an, Zhejiang 311300, P.R. China, 3School of Agricultural Science, University of Tasmania, Hobart 7001, Tasmania, Australia, 4Zhoushan Entry-Exit Inspection and Quarantine Bureau, Zhoushan, Zhejiang 316000, P.R. China

Received: April 28, 2015; Accepted: October 13, 2015

Abstract

Listeria monocytogenes is a foodborne pathogen of considerable genetic diversity with varying
pathogenicity. Initially, we found that the strain M7 was far less pathogenic than the strain
Lm850658 though both are serovar 4a strains belonging to the lineage III. Comparative
genomic approaches were then attempted to decipher the genetic basis that might govern the
strain-dependent pathotypes. There are 2,761 coding sequences of 100% nucleotide identity
between the two strains, accounting for 95.7% of the total genes in Lm850658 and 92.7% in M7.
Lm850658 contains 33 specific genes, including a novel 20K prophage whereas strain M7 has
130 specific genes, including two large prophages (38K and 44K). To examine the roles of these
specific prophages in pathogenicity, the 20K and 38K prophages were deleted from their
respective strains. There were virtually no differences of pathogenicity between the deletion
mutants and their parent strains, although some putative virulent factors like VirB4 are
present in the 20K region or holin-lysin in the 38K region. In silico PCR analysis of 29 listeria
genomes show that only strain SLCC2540 has the same 18 bp integration hotspot as Lm850658,
whereas the sequence identity of their 20K prophages is very low (21.3%). The 38K and 44K
prophages are located in two other different hotspots and are conserved in low virulent strains
M7, HCC23, and L99. In conclusion, the 20K and 38K prophages of L. monocytogenes serovar 4a
strains Lm850658 and M7 are not related to virulence but contribute to genetic diversity.

Keywords: Listeria monocytogenes, Prophage, Genetic diversity, Virulence

References

  1. Al Mamun AA, Tominaga A, Enomoto M. 1997. Cloning and characterization of the region III flagellar operons of the four Shigella subgroups: genetic defects that cause loss of flagella of Shigella boydii and Shigella sonnei. J. Bacteriol. 179: 4493-4500.
    Pubmed KoreaMed
  2. Braun L, Dramsi S, Dehoux P, Bierne H, Lindahl G, Cossart P. 1997. InlB: an invasion protein of Listeria monocytogenes with a novel type of surface association. Mol. Microbiol. 25: 285-294.
    Pubmed CrossRef
  3. Brussow H, Canchaya C, Hardt WD. 2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68: 560-602.
    Pubmed KoreaMed CrossRef
  4. Camilli A, Tilney LG, Portnoy DA. 1993. Dual roles of plcA in Listeria monocytogenes pathogenesis. Mol. Microbiol. 8: 143-157.
    Pubmed KoreaMed CrossRef
  5. Chen J, Chen Q, Jiang L, Cheng C, Bai F, Wang J, 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.
    Pubmed KoreaMed CrossRef
  6. Chen J, Cheng C, Xia Y, Zhao H, Fang C, Shan Y, 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.
    Pubmed CrossRef
  7. Chen J, Jiang L, Chen Q, Zhao H, Luo X, Chen X, Fang W. 2009. Lmo0038 is involved in acid and heat stress responses and specific for Listeria monocytogenes lineages I and II, and Listeria ivanovii. Foodborne Pathog. Dis. 6: 365-376.
    Pubmed CrossRef
  8. 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.
    Pubmed KoreaMed CrossRef
  9. Chung IY, Jang HJ, Bae HW, Cho YH. 2014. A phage protein that inhibits the bacterial ATPase required for type IV pilus assembly. Proc. Natl. Acad. Sci. USA 111: 11503-11508.
    Pubmed KoreaMed CrossRef
  10. Coleman D, Knights J, Russell R, Shanley D, Birkbeck TH, Dougan G, Charles I. 1991. Insertional inactivation of the Staphylococcus aureus beta-toxin by bacteriophage phi 13 occurs by site- and orientation-specific integration of the phi 13 genome. Mol. Microbiol. 5: 933-939.
    Pubmed CrossRef
  11. DeBardeleben HK, Lysenko ES, Dalia AB, Weiser JN. 2014. Tolerance of a phage element by Streptococcus pneumoniae leads to a fitness defect during colonization. J. Bacteriol. 196:2670-2680.
    Pubmed KoreaMed CrossRef
  12. 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.
    Pubmed KoreaMed CrossRef
  13. Deng X, Phillippy AM, Li Z, Salzberg SL, Zhang W. 2010. Probing the pan-genome of Listeria monocytogenes: new insights into intraspecific niche expansion and genomic diversification. BMC Genomics 11: 500.
    Pubmed KoreaMed CrossRef
  14. Doumith M, Cazalet C, Simoes N, Frangeul L, Jacquet C, Kunst F, et al. 2004. New aspects regarding evolution and virulence of Listeria monocytogenes revealed by comparative genomics and DNA arrays. Infect. Immun. 72: 1072-1083.
    Pubmed KoreaMed CrossRef
  15. Farber JM, Peterkin PI. 1991. Listeria monocytogenes, a foodborne pathogen. Microbiol. Rev. 55: 476-511.
    Pubmed KoreaMed
  16. Freitag NE, Port GC, Miner MD. 2009. Listeria monocytogenes from saprophyte to intracellular pathogen. Nat. Rev. Microbiol. 7: 623-628.
    Pubmed KoreaMed CrossRef
  17. Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, Baquero F, et al. 2001. Comparative genomics of Listeria species. Science 294: 849-852.
    Pubmed
  18. Gracieux P, Roche SM, Pardon P, Velge P. 2003. Hypovirulent Listeria monocytogenes strains are less frequently recovered than virulent strains on PALCAM and Rapid' L. mono media. Int. J. Food Microbiol. 83: 133-145.
    CrossRef
  19. Hain T, Ghai R, Billion A, Kuenne CT, Steinweg C, Izar B, et al. 2012. Comparative genomics and transcriptomics of lineages I, II, and III strains of Listeria monocytogenes. BMC Genomics 13: 144.
    Pubmed KoreaMed CrossRef
  20. Hain T, Steinweg C, Chakraborty T. 2006. Comparative and functional genomics of Listeria spp. J. Biotechnol. 126: 37-51.
    Pubmed CrossRef
  21. Hamon M, Bierne H, Cossart P. 2006. Listeria monocytogenes: a multifaceted model. Nat. Rev. Microbiol. 4: 423-434.
    Pubmed CrossRef
  22. Jiang LL, Xu JJ, Chen N, Shuai JB, Fang WH. 2006. Virulence phenotyping and molecular characterization of a low-pathogenicity isolate of Listeria monocytogenes from cow’s milk. Acta Biochim. Biophys. Sin. (Shanghai) 38: 262-270.
    CrossRef
  23. Jonquieres R, Bierne H, Fiedler F, Gounon P, Cossart P. 1999. Interaction between the protein InlB of Listeria monocytogenes and lipoteichoic acid: a novel mechanism of protein association at the surface of gram-positive bacteria. Mol. Microbiol. 34: 902-914.
    Pubmed CrossRef
  24. Kahrstrom CT. 2014. Structural biology: solving the T4SS structural mystery. Nat. Rev. Microbiol. 12: 312.
    Pubmed CrossRef
  25. Kapyrina NA. 1971. [Prophage induction in Listeria monocytogenes]. Veterinariia 9: 39-41.
    Pubmed
  26. Kuenne C, Billion A, Mraheil MA, 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.
    Pubmed KoreaMed CrossRef
  27. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35: 3100-3108.
    Pubmed KoreaMed CrossRef
  28. Liu D. 2004. Listeria monocytogenes: comparative interpretation of mouse virulence assay. FEMS Microbiol. Lett. 233: 159-164.
    Pubmed CrossRef
  29. Liu D, Lawrence ML, Wiedmann M, Gorski L, Mandrell RE, Ainsworth AJ, Austin FW. 2006. Listeria monocytogenes subgroups IIIA, IIIB, and IIIC delineate genetically distinct populations with varied pathogenic potential. J. Clin. Microbiol. 44: 4229-4233.
    Pubmed KoreaMed CrossRef
  30. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.
    Pubmed KoreaMed CrossRef
  31. Monk IR, Gahan CG, Hill C. 2008. Tools for functional postgenomic analysis of Listeria monocytogenes. Appl. Environ. Microbiol. 74: 3921-3934.
    Pubmed KoreaMed CrossRef
  32. Orsi RH, Borowsky ML, Lauer P, Young SK, Nusbaum C, Galagan JE, et al. 2008. Short-term genome evolution of Listeria monocytogenes in a non-controlled environment. BMC Genomics 9: 539.
    Pubmed KoreaMed CrossRef
  33. Paredes-Cervantes V, Flores-Mejia R, Moreno-Lafont MC, Lanz-Mendoza H, Tello-Lopez AT, Castillo-Vera J, et al. 2011. Comparative proteome analysis of Brucella abortus 2308 and its virB type IV secretion system mutant reveals new T4SS-related candidate proteins. J. Proteomics 74: 2959-2971.
    Pubmed CrossRef
  34. 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.
    Pubmed KoreaMed CrossRef
  35. Roberts A, Nightingale K, Jeffers G, Fortes E, Kongo JM, Wiedmann M. 2006. Genetic and phenotypic characterization of Listeria monocytogenes lineage III. Microbiology 152: 685-693.
    Pubmed CrossRef
  36. Schaferkordt S, Chakraborty T. 1997. Identification, cloning, and characterization of the Ima operon, whose gene products are unique to Listeria monocytogenes. J. Bacteriol. 179: 2707-2716.
    Pubmed KoreaMed
  37. Schattner P, Brooks AN, Lowe TM. 2005. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 33: W686-W689.
    Pubmed KoreaMed CrossRef
  38. 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.
    Pubmed KoreaMed CrossRef
  39. Stelma GN Jr, Reyes AL, Peeler JT, Francis DW, Hunt JM, Spaulding PL, et al. 1987. Pathogenicity test for Listeria monocytogenes using immunocompromised mice. J. Clin. Microbiol. 25: 2085-2089.
    Pubmed KoreaMed
  40. Sun AN, Camilli A, Portnoy DA. 1990. Isolation of Listeria monocytogenes small-plaque mutants defective for intracellular growth and cell-to-cell spread. Infect. Immun. 58: 3770-3778.
    Pubmed KoreaMed
  41. Swaminathan B, Gerner-Smidt P. 2007. The epidemiology of human listeriosis. Microbes Infect. 9: 1236-1243.
    Pubmed CrossRef
  42. Tal A, Arbel-Goren R, Costantino N, Court DL, Stavans J. 2014. Location of the unique integration site on an Escherichia coli chromosome by bacteriophage lambda DNA in vivo. Proc. Natl. Acad. Sci. USA 111: 7308-7312.
    Pubmed KoreaMed CrossRef
  43. Tamura K, D udley J, N ei M , Kumar S. 2 007 . MEGA4:Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.
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