전체메뉴
검색
Article Search

JMB Journal of Microbiolog and Biotechnology

QR Code QR Code

Research article

Food Microbiology and Biotechnology (FMB)  |  Probiotics and Foodborne Microorganisms

Genomic Insights and Its Comparative Analysis with Yersinia enterocolitica Reveals the Potential Virulence Determinants and Further Pathogenicity for Foodborne Outbreaks

Gopalsamy Gnanasekaran 1, 2, Eun Jung Na 1, 2, Han Young Chung 1, 2, Suyeon Kim 1, 2, You-Tae Kim 2, 3, Woori Kwak 1, 2, Heebal Kim 1, 2, Sangryeol Ryu 1, 2, Sang Ho Choi 1, 2 and Ju-Hoon Lee 2, 3*

1Department of Agricultural Biotechnology, Seoul National University, Seoul 08826, Republic of Korea, 2Food-borne Pathogen Omics Research Center (FORC), Seoul National University, Seoul 08826, Republic of Korea, 3Department of Food Science and Biotechnology, Kyung Hee University, Yongin 17104, Republic of Korea

Received: November 17, 2016; Accepted: November 24, 2016

J. Microbiol. Biotechnol. 2017; 27(2): 262-270

Published February 28, 2017 https://doi.org/10.4014/jmb.1611.11048

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Yersinia enterocolitica is a well-known foodborne pathogen causing gastrointestinal infections worldwide. The strain Y. enterocolitica FORC_002 was isolated from the gill of flatfish (plaice) and its genome was sequenced. The genomic DNA consists of 4,837,317 bp with a GC content of 47.1%, and is predicted to contain 4,221 open reading frames, 81 tRNA genes, and 26 rRNA genes. Interestingly, genomic analysis revealed pathogenesis and host immune evasionassociated genes encoding guanylate cyclase (Yst), invasin (Ail and Inv), outer membrane protein (Yops), autotransporter adhesin A (YadA), RTX-like toxins, and a type III secretion system. In particular, guanylate cyclase is a heat-stable enterotoxin causing Yersinia-associated diarrhea, and RTX-like toxins are responsible for attachment to integrin on the target cell for cytotoxic action. This genome can be used to identify virulence factors that can be applied for the development of novel biomarkers for the rapid detection of this pathogen in foods.

Keywords

Yersinia enterocolitica, genome, Type III secretion system, virulence factor, food poisoning, gastroenteritis

References

  1. Tauxe RV. 1997. Emerging foodborne diseases: an evolving public health challenge. Emerg. Infect. Dis. 3: 425.
    Pubmed PMC CrossRef
  2. Toma S, Lafleur L. 1974. Survey on the incidence of Yersinia enterocolitica infection in Canada. J. Appl. Microbiol. 28: 469473.
  3. Kay BA, Wachsmuth K, Gemski P, Feeley JC, Quan TJ, Brenner D. 1983. Virulence and phenotypic characterization of Yersinia enterocolitica isolated from humans in the United States. J. Clin. Microbiol. 17: 128-138.
    Pubmed PMC
  4. Zadernowska A, Chajęcka-Wierzchowska W, ŁaniewskaTrokenheim Ł. 2014. Yersinia enterocolitica: a dangerous, but often ignored, foodborne pathogen. Food Rev. Int. 30: 53-70.
    CrossRef
  5. Scott E. 2003. Food safety and foodborne disease in 21st century homes. Can. J. Infect. Dis. 14: 277.
    Pubmed PMC CrossRef
  6. Edward JB. 1997. Yersinia enterocolitica: the charisma continues. Clin. Microbiol. Rev. 10: 257-276.
  7. Tauxe RV. 2002. Emerging foodborne pathogens. Int. J. Food Microbiol. 78: 31-41.
    CrossRef
  8. Bucher M, Meyer C, Grötzbach B, Wacheck S, Stolle A, Fredriksson-Ahomaa M. 2008. Epidemiological data on pathogenic Yersinia enterocolitica in Southern Germany during 2000-2006. Foodborne Pathog. Dis. 5: 273-280.
    Pubmed CrossRef
  9. Boqvist S, Pettersson H, Svensson Å, Andersson Y. 2009. Sources of sporadic Yersinia enterocolitica infection in children in Sweden, 2004: a case-control study. Epidemiol. Infect. 137: 897-905.
    Pubmed CrossRef
  10. Butler T, Islam M, Islam M, Azad A, Huq M, Speelman P, Roy S. 1984. Isolation of Yersinia enterocolitica and Y. intermedia from fatal cases of diarrhoeal illness in Bangladesh. Trans. R. Soc. Trop. Med. Hyg. 78: 449-450.
    CrossRef
  11. Kanan T, Abdulla Z. 2009. Isolation of Yersinia spp. from cases of diarrhoea in Iraqi infants and children. East Mediterr. Health J. 15: 276-284.
    Pubmed
  12. Soltan-Dallal M, Moezardalan K. 2003. Frequency of Yersinia species infection in paediatric acute diarrhoea in Tehran. East Mediterr. Health J. 10: 152-158.
  13. Okwori AE, Martínez PO, Fredriksson-Ahomaa M, Agina SE, Korkeala H. 2009. Pathogenic Yersinia enterocolitica 2/O:9 and Yersinia pseudotuberculosis 1/O:1 strains isolated from human and non-human sources in the Plateau State of Nigeria. Food Microbiol. 26: 872-875.
    Pubmed CrossRef
  14. Wauters G, Aleksić S, Charlier J, Schulze G. 1991. Somatic and flagellar antigens of Yersinia enterocolitica and related species. Contrib. Microbiol. Immunol. 12: 239.
    Pubmed
  15. Bottone EJ. 1999. Yersinia enterocolitica: overview and epidemiologic correlates. Microbes Infect. 1: 323-333.
    CrossRef
  16. Brubaker RR. 1991. Factors promoting acute and chronic diseases caused by yersiniae. Clin. Microbiol. Rev. 4: 309-324.
    Pubmed PMC CrossRef
  17. Cornelis GR, Boland A, Boyd AP, Geuijen C, Iriarte M, Neyt C, et al. 1998. The virulence plasmid of Yersinia, an antihost genome. Microbiol. Mol. Biol. Rev. 62: 1315-1352.
    Pubmed PMC
  18. Bottone EJ. 1997. Yersinia enterocolitica: the charisma continues. Clin. Microbiol. Rev. 10: 257-276.
    Pubmed PMC
  19. Miller V, Falkow S. 1988. Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect. Immun. 56: 1242-1248.
    Pubmed PMC
  20. Miller V, Farmer J, Hill W, Falkow S. 1989. The ail locus is found uniquely in Yersinia enterocolitica serotypes commonly associated with disease. Infect. Immun. 57: 121-131.
    Pubmed PMC
  21. Cornelis G, Laroche Y, Balligand G, Sory M-P, Wauters G. 1987. Yersinia enterocolitica, a primary model for bacterial invasiveness. Rev. Infect. Dis. 9: 64-87.
    Pubmed CrossRef
  22. Cornelis GR. 2006. The type III secretion injectisome. Nat. Rev. Microbiol. 4: 811-825.
    Pubmed CrossRef
  23. Galan J E, C ollmer A. 1 999. T y pe I II s ecretion m achines:bacterial devices for protein delivery into host cells. Science 284: 1322-1328.
    Pubmed
  24. Jin Q, Thilmony R, Zwiesler-Vollick J, He S-Y. 2003. Type III protein secretion in Pseudomonas syringae. Microbes Infect. 5:301-310.
    CrossRef
  25. Galindo CL, Rosenzweig JA, Kirtley ML, Chopra AK. 2011. Pathogenesis of Y. enterocolitica and Y. pseudotuberculosis in human yersiniosis. J. Pathog. 2011: 1-16.
    Pubmed PMC CrossRef
  26. Heise T, Dersch P. 2006. Identification of a domain in Yersinia virulence factor YadA that is crucial for extracellular matrixspecific cell adhesion and uptake. Proc. Natl. Acad. Sci. USA 103: 3375-3380.
    Pubmed PMC CrossRef
  27. Kirjavainen V, Jarva H, Biedzka-Sarek M, Blom AM, Skurnik M, Meri S. 2008. Yersinia enterocolitica serum resistance proteins YadA and Ail bind the complement regulator C4bbinding protein. PLoS Pathog. 4: e1000140.
    Pubmed PMC CrossRef
  28. Brodsky IE, Medzhitov R. 2008. Reduced secretion of YopJ by Yersinia limits in vivo cell death but enhances bacterial virulence. PLoS Pathog. 4: e1000067.
    Pubmed PMC CrossRef
  29. Home SM, Prüß BM. 2006. Global gene regulation in Yersinia enterocolitica: effect of FliA on the expression levels of flagellar and plasmid-encoded virulence genes. Arch. Microbiol. 185: 115-126.
    Pubmed CrossRef
  30. Singh I, Virdi JS. 2005. Interaction of Yersinia enterocolitica biotype 1A strains of diverse origin with cultured cells in vitro. Jpn. J. Infect. Dis. 58: 31-33.
    Pubmed
  31. Travers KJ, Chin C-S, Rank DR, Eid JS, Turner SW. 2010. A flexible and efficient template format for circular consensus sequencing and SNP detection. Nucleic Acids Res. 38: e159.
    Pubmed PMC CrossRef
  32. Chin C-S, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, et al. 2013. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10: 563-569.
    Pubmed CrossRef
  33. Carneiro MO, Russ C, Ross MG, Gabriel SB, Nusbaum C, DePristo MA. 2012. Pacific biosciences sequencing technology for genotyping and variation discovery in human data. BMC Genomics 13: 375.
    Pubmed PMC CrossRef
  34. Delcher AL, Salzberg SL, Phillippy AM. 2003. Using MUMmer to identify similar regions in large sequence sets. Curr. Protoc. Bioinformatics 10: Unit 10.3.
  35. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95-98.
  36. Disz T, Akhter S, Cuevas D, Olson R, Overbeek R, Vonstein V, et al. 2010. Accessing the SEED genome databases via web services API: tools for programmers. BMC Bioinformatics 11:319.
    Pubmed PMC CrossRef
  37. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. 2008. The RAST server: rapid annotations using subsystems technology. BMC Genomics 9: 75.
    Pubmed PMC CrossRef
  38. Wu S, Zhu Z, Fu L, Niu B, Li W. 2011. WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics 12: 444.
    Pubmed PMC CrossRef
  39. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. 2009. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25: 119-120.
    Pubmed PMC CrossRef
  40. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. 2007. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int. J. Syst. Evol. Microbiol. 57: 81-91.
    Pubmed CrossRef
  41. Paradis E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289-290.
    Pubmed CrossRef
  42. Waack S, Keller O, Asper R, Brodag T, Damm C, Fricke WF, et al. 2006. Score-based prediction of genomic islands in prokaryotic genomes using Hidden Markov models. BMC Bioinformatics 7: 142.
    Pubmed PMC CrossRef
  43. Bissett ML, Powers C, Abbott SL, Janda JM. 1990. Epidemiologic investigations of Yersinia enterocolitica and related species:sources, frequency, and serogroup distribution. J. Clin. Microbiol. 5: 910-912
  44. Sedgwick AK, Tilton RC. 1971. Biochemical and serological characteristics of a Yersinia enterocolitica isolate. Appl. Microbiol. 21: 383-384.
    PMC
  45. Kanazawa Y, Kuramata T. 1976. Drug sensitivity of Yersinia enterocolitica and Yersinia pseudotuberculosis. Jpn. J. Antibiot. 29: 366-376.
    Pubmed
  46. Yao P, Chen X, Yan Y, Liu F, Zhang Y, Guo X, Xu B. 2014. Glutaredoxin 1, glutaredoxin 2, thioredoxin 1, and thioredoxin peroxidase 3 play important roles in antioxidant defense in Apis cerana cerana. Free Radic. Biol. Med. 68: 335-346.
    Pubmed CrossRef
  47. Carlin A, Shi W, Dey S, Rosen BP. 1995. The ars operon of Escherichia coli confers arsenical and antimonial resistance. J. Bacteriol. 177: 981-986.
    Pubmed PMC CrossRef
  48. Cornelis G, Sluiters C, De Rouvroit CL, Michiels T. 1989. Homology between VirF, the transcriptional activator of the Yersinia virulence regulon, and AraC, the Escherichia coli arabinose operon regulator. J. Bacteriol. 171: 254-262.
    Pubmed PMC CrossRef
  49. Fuchs TM, Bresolin G, Marcinowski L, Schachtner J, Scherer S. 2008. Insecticidal genes of Yersinia spp.: taxonomical distribution, contribution to toxicity towards Manduca sexta and Galleria mellonella, and evolution. BMC Microbiol. 8: 214.
    Pubmed PMC CrossRef
  50. Venecia K, Young GM. 2005. Environmental regulation and virulence attributes of the Ysa type III secretion system of Yersinia enterocolitica biovar 1B. Infect. Immun. 73: 5961-5977.
    Pubmed PMC CrossRef
  51. Pepe JC, Miller VL. 1993. Yersinia enterocolitica invasin: a primary role in the initiation of infection. Proc. Natl. Acad. Sci. USA 90: 6473-6477.
    Pubmed PMC CrossRef
  52. Schulte R, Kerneis S, Klinke S, Bartels H, Preger S, Kraehenbuhl JP, et al. 2000. Translocation of Yersinia enterocolitica across reconstituted intestinal epithelial monolayers is triggered by Yersinia invasin binding to β1 integrins apically expressed on M-like cells. Cell. Microbiol. 2: 173-185.
    Pubmed CrossRef
  53. Fabrega A, Vila J. 2012. Yersinia enterocolitica: pathogenesis, virulence and antimicrobial resistance. Enferm. Infecc. Microbiol. Clin. 30: 24-32.
    Pubmed CrossRef
  54. Nishi J, Sheikh J, Mizuguchi K, Luisi B, Burland V, Boutin A, et al. 2003. The export of coat protein from enteroaggregative Escherichia coli by a specific ATP-binding cassette transporter system. J. Biol. Chem. 278: 45680-45689.
    Pubmed CrossRef
  55. Bowen D, Rocheleau TA, Blackburn M, Andreev O, Golubeva E, Bhartia R. 1998. Insecticidal toxins from the bacterium Photorhabdus luminescens. Science 280: 2129-2132.
    Pubmed CrossRef
  56. Fällman M, Deleuil F, McGee K. 2001. Resistance to phagocytosis by Yersinia. Int. J. Med. Microbiol. 291: 501-509.
    CrossRef
  57. Grissa I, Vergnaud G, Pourcel C. 2007. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 8: 172.
    Pubmed PMC CrossRef
  58. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729.
    Pubmed PMC CrossRef

Related articles in JMB

More Related Articles

Article

Research article

J. Microbiol. Biotechnol. 2017; 27(2): 262-270

Published online February 28, 2017 https://doi.org/10.4014/jmb.1611.11048

Copyright © The Korean Society for Microbiology and Biotechnology.

Genomic Insights and Its Comparative Analysis with Yersinia enterocolitica Reveals the Potential Virulence Determinants and Further Pathogenicity for Foodborne Outbreaks

Gopalsamy Gnanasekaran 1, 2, Eun Jung Na 1, 2, Han Young Chung 1, 2, Suyeon Kim 1, 2, You-Tae Kim 2, 3, Woori Kwak 1, 2, Heebal Kim 1, 2, Sangryeol Ryu 1, 2, Sang Ho Choi 1, 2 and Ju-Hoon Lee 2, 3*

1Department of Agricultural Biotechnology, Seoul National University, Seoul 08826, Republic of Korea, 2Food-borne Pathogen Omics Research Center (FORC), Seoul National University, Seoul 08826, Republic of Korea, 3Department of Food Science and Biotechnology, Kyung Hee University, Yongin 17104, Republic of Korea

Received: November 17, 2016; Accepted: November 24, 2016

Abstract

Yersinia enterocolitica is a well-known foodborne pathogen causing gastrointestinal infections
worldwide. The strain Y. enterocolitica FORC_002 was isolated from the gill of flatfish (plaice)
and its genome was sequenced. The genomic DNA consists of 4,837,317 bp with a GC content
of 47.1%, and is predicted to contain 4,221 open reading frames, 81 tRNA genes, and 26 rRNA
genes. Interestingly, genomic analysis revealed pathogenesis and host immune evasionassociated
genes encoding guanylate cyclase (Yst), invasin (Ail and Inv), outer membrane
protein (Yops), autotransporter adhesin A (YadA), RTX-like toxins, and a type III secretion
system. In particular, guanylate cyclase is a heat-stable enterotoxin causing Yersinia-associated
diarrhea, and RTX-like toxins are responsible for attachment to integrin on the target cell for
cytotoxic action. This genome can be used to identify virulence factors that can be applied for
the development of novel biomarkers for the rapid detection of this pathogen in foods.

Keywords: Yersinia enterocolitica, genome, Type III secretion system, virulence factor, food poisoning, gastroenteritis

References

  1. Tauxe RV. 1997. Emerging foodborne diseases: an evolving public health challenge. Emerg. Infect. Dis. 3: 425.
    Pubmed KoreaMed CrossRef
  2. Toma S, Lafleur L. 1974. Survey on the incidence of Yersinia enterocolitica infection in Canada. J. Appl. Microbiol. 28: 469473.
  3. Kay BA, Wachsmuth K, Gemski P, Feeley JC, Quan TJ, Brenner D. 1983. Virulence and phenotypic characterization of Yersinia enterocolitica isolated from humans in the United States. J. Clin. Microbiol. 17: 128-138.
    Pubmed KoreaMed
  4. Zadernowska A, Chajęcka-Wierzchowska W, ŁaniewskaTrokenheim Ł. 2014. Yersinia enterocolitica: a dangerous, but often ignored, foodborne pathogen. Food Rev. Int. 30: 53-70.
    CrossRef
  5. Scott E. 2003. Food safety and foodborne disease in 21st century homes. Can. J. Infect. Dis. 14: 277.
    Pubmed KoreaMed CrossRef
  6. Edward JB. 1997. Yersinia enterocolitica: the charisma continues. Clin. Microbiol. Rev. 10: 257-276.
  7. Tauxe RV. 2002. Emerging foodborne pathogens. Int. J. Food Microbiol. 78: 31-41.
    CrossRef
  8. Bucher M, Meyer C, Grötzbach B, Wacheck S, Stolle A, Fredriksson-Ahomaa M. 2008. Epidemiological data on pathogenic Yersinia enterocolitica in Southern Germany during 2000-2006. Foodborne Pathog. Dis. 5: 273-280.
    Pubmed CrossRef
  9. Boqvist S, Pettersson H, Svensson Å, Andersson Y. 2009. Sources of sporadic Yersinia enterocolitica infection in children in Sweden, 2004: a case-control study. Epidemiol. Infect. 137: 897-905.
    Pubmed CrossRef
  10. Butler T, Islam M, Islam M, Azad A, Huq M, Speelman P, Roy S. 1984. Isolation of Yersinia enterocolitica and Y. intermedia from fatal cases of diarrhoeal illness in Bangladesh. Trans. R. Soc. Trop. Med. Hyg. 78: 449-450.
    CrossRef
  11. Kanan T, Abdulla Z. 2009. Isolation of Yersinia spp. from cases of diarrhoea in Iraqi infants and children. East Mediterr. Health J. 15: 276-284.
    Pubmed
  12. Soltan-Dallal M, Moezardalan K. 2003. Frequency of Yersinia species infection in paediatric acute diarrhoea in Tehran. East Mediterr. Health J. 10: 152-158.
  13. Okwori AE, Martínez PO, Fredriksson-Ahomaa M, Agina SE, Korkeala H. 2009. Pathogenic Yersinia enterocolitica 2/O:9 and Yersinia pseudotuberculosis 1/O:1 strains isolated from human and non-human sources in the Plateau State of Nigeria. Food Microbiol. 26: 872-875.
    Pubmed CrossRef
  14. Wauters G, Aleksić S, Charlier J, Schulze G. 1991. Somatic and flagellar antigens of Yersinia enterocolitica and related species. Contrib. Microbiol. Immunol. 12: 239.
    Pubmed
  15. Bottone EJ. 1999. Yersinia enterocolitica: overview and epidemiologic correlates. Microbes Infect. 1: 323-333.
    CrossRef
  16. Brubaker RR. 1991. Factors promoting acute and chronic diseases caused by yersiniae. Clin. Microbiol. Rev. 4: 309-324.
    Pubmed KoreaMed CrossRef
  17. Cornelis GR, Boland A, Boyd AP, Geuijen C, Iriarte M, Neyt C, et al. 1998. The virulence plasmid of Yersinia, an antihost genome. Microbiol. Mol. Biol. Rev. 62: 1315-1352.
    Pubmed KoreaMed
  18. Bottone EJ. 1997. Yersinia enterocolitica: the charisma continues. Clin. Microbiol. Rev. 10: 257-276.
    Pubmed KoreaMed
  19. Miller V, Falkow S. 1988. Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect. Immun. 56: 1242-1248.
    Pubmed KoreaMed
  20. Miller V, Farmer J, Hill W, Falkow S. 1989. The ail locus is found uniquely in Yersinia enterocolitica serotypes commonly associated with disease. Infect. Immun. 57: 121-131.
    Pubmed KoreaMed
  21. Cornelis G, Laroche Y, Balligand G, Sory M-P, Wauters G. 1987. Yersinia enterocolitica, a primary model for bacterial invasiveness. Rev. Infect. Dis. 9: 64-87.
    Pubmed CrossRef
  22. Cornelis GR. 2006. The type III secretion injectisome. Nat. Rev. Microbiol. 4: 811-825.
    Pubmed CrossRef
  23. Galan J E, C ollmer A. 1 999. T y pe I II s ecretion m achines:bacterial devices for protein delivery into host cells. Science 284: 1322-1328.
    Pubmed
  24. Jin Q, Thilmony R, Zwiesler-Vollick J, He S-Y. 2003. Type III protein secretion in Pseudomonas syringae. Microbes Infect. 5:301-310.
    CrossRef
  25. Galindo CL, Rosenzweig JA, Kirtley ML, Chopra AK. 2011. Pathogenesis of Y. enterocolitica and Y. pseudotuberculosis in human yersiniosis. J. Pathog. 2011: 1-16.
    Pubmed KoreaMed CrossRef
  26. Heise T, Dersch P. 2006. Identification of a domain in Yersinia virulence factor YadA that is crucial for extracellular matrixspecific cell adhesion and uptake. Proc. Natl. Acad. Sci. USA 103: 3375-3380.
    Pubmed KoreaMed CrossRef
  27. Kirjavainen V, Jarva H, Biedzka-Sarek M, Blom AM, Skurnik M, Meri S. 2008. Yersinia enterocolitica serum resistance proteins YadA and Ail bind the complement regulator C4bbinding protein. PLoS Pathog. 4: e1000140.
    Pubmed KoreaMed CrossRef
  28. Brodsky IE, Medzhitov R. 2008. Reduced secretion of YopJ by Yersinia limits in vivo cell death but enhances bacterial virulence. PLoS Pathog. 4: e1000067.
    Pubmed KoreaMed CrossRef
  29. Home SM, Prüß BM. 2006. Global gene regulation in Yersinia enterocolitica: effect of FliA on the expression levels of flagellar and plasmid-encoded virulence genes. Arch. Microbiol. 185: 115-126.
    Pubmed CrossRef
  30. Singh I, Virdi JS. 2005. Interaction of Yersinia enterocolitica biotype 1A strains of diverse origin with cultured cells in vitro. Jpn. J. Infect. Dis. 58: 31-33.
    Pubmed
  31. Travers KJ, Chin C-S, Rank DR, Eid JS, Turner SW. 2010. A flexible and efficient template format for circular consensus sequencing and SNP detection. Nucleic Acids Res. 38: e159.
    Pubmed KoreaMed CrossRef
  32. Chin C-S, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, et al. 2013. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10: 563-569.
    Pubmed CrossRef
  33. Carneiro MO, Russ C, Ross MG, Gabriel SB, Nusbaum C, DePristo MA. 2012. Pacific biosciences sequencing technology for genotyping and variation discovery in human data. BMC Genomics 13: 375.
    Pubmed KoreaMed CrossRef
  34. Delcher AL, Salzberg SL, Phillippy AM. 2003. Using MUMmer to identify similar regions in large sequence sets. Curr. Protoc. Bioinformatics 10: Unit 10.3.
  35. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95-98.
  36. Disz T, Akhter S, Cuevas D, Olson R, Overbeek R, Vonstein V, et al. 2010. Accessing the SEED genome databases via web services API: tools for programmers. BMC Bioinformatics 11:319.
    Pubmed KoreaMed CrossRef
  37. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. 2008. The RAST server: rapid annotations using subsystems technology. BMC Genomics 9: 75.
    Pubmed KoreaMed CrossRef
  38. Wu S, Zhu Z, Fu L, Niu B, Li W. 2011. WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics 12: 444.
    Pubmed KoreaMed CrossRef
  39. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. 2009. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25: 119-120.
    Pubmed KoreaMed CrossRef
  40. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. 2007. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int. J. Syst. Evol. Microbiol. 57: 81-91.
    Pubmed CrossRef
  41. Paradis E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289-290.
    Pubmed CrossRef
  42. Waack S, Keller O, Asper R, Brodag T, Damm C, Fricke WF, et al. 2006. Score-based prediction of genomic islands in prokaryotic genomes using Hidden Markov models. BMC Bioinformatics 7: 142.
    Pubmed KoreaMed CrossRef
  43. Bissett ML, Powers C, Abbott SL, Janda JM. 1990. Epidemiologic investigations of Yersinia enterocolitica and related species:sources, frequency, and serogroup distribution. J. Clin. Microbiol. 5: 910-912
  44. Sedgwick AK, Tilton RC. 1971. Biochemical and serological characteristics of a Yersinia enterocolitica isolate. Appl. Microbiol. 21: 383-384.
    KoreaMed
  45. Kanazawa Y, Kuramata T. 1976. Drug sensitivity of Yersinia enterocolitica and Yersinia pseudotuberculosis. Jpn. J. Antibiot. 29: 366-376.
    Pubmed
  46. Yao P, Chen X, Yan Y, Liu F, Zhang Y, Guo X, Xu B. 2014. Glutaredoxin 1, glutaredoxin 2, thioredoxin 1, and thioredoxin peroxidase 3 play important roles in antioxidant defense in Apis cerana cerana. Free Radic. Biol. Med. 68: 335-346.
    Pubmed CrossRef
  47. Carlin A, Shi W, Dey S, Rosen BP. 1995. The ars operon of Escherichia coli confers arsenical and antimonial resistance. J. Bacteriol. 177: 981-986.
    Pubmed KoreaMed CrossRef
  48. Cornelis G, Sluiters C, De Rouvroit CL, Michiels T. 1989. Homology between VirF, the transcriptional activator of the Yersinia virulence regulon, and AraC, the Escherichia coli arabinose operon regulator. J. Bacteriol. 171: 254-262.
    Pubmed KoreaMed CrossRef
  49. Fuchs TM, Bresolin G, Marcinowski L, Schachtner J, Scherer S. 2008. Insecticidal genes of Yersinia spp.: taxonomical distribution, contribution to toxicity towards Manduca sexta and Galleria mellonella, and evolution. BMC Microbiol. 8: 214.
    Pubmed KoreaMed CrossRef
  50. Venecia K, Young GM. 2005. Environmental regulation and virulence attributes of the Ysa type III secretion system of Yersinia enterocolitica biovar 1B. Infect. Immun. 73: 5961-5977.
    Pubmed KoreaMed CrossRef
  51. Pepe JC, Miller VL. 1993. Yersinia enterocolitica invasin: a primary role in the initiation of infection. Proc. Natl. Acad. Sci. USA 90: 6473-6477.
    Pubmed KoreaMed CrossRef
  52. Schulte R, Kerneis S, Klinke S, Bartels H, Preger S, Kraehenbuhl JP, et al. 2000. Translocation of Yersinia enterocolitica across reconstituted intestinal epithelial monolayers is triggered by Yersinia invasin binding to β1 integrins apically expressed on M-like cells. Cell. Microbiol. 2: 173-185.
    Pubmed CrossRef
  53. Fabrega A, Vila J. 2012. Yersinia enterocolitica: pathogenesis, virulence and antimicrobial resistance. Enferm. Infecc. Microbiol. Clin. 30: 24-32.
    Pubmed CrossRef
  54. Nishi J, Sheikh J, Mizuguchi K, Luisi B, Burland V, Boutin A, et al. 2003. The export of coat protein from enteroaggregative Escherichia coli by a specific ATP-binding cassette transporter system. J. Biol. Chem. 278: 45680-45689.
    Pubmed CrossRef
  55. Bowen D, Rocheleau TA, Blackburn M, Andreev O, Golubeva E, Bhartia R. 1998. Insecticidal toxins from the bacterium Photorhabdus luminescens. Science 280: 2129-2132.
    Pubmed CrossRef
  56. Fällman M, Deleuil F, McGee K. 2001. Resistance to phagocytosis by Yersinia. Int. J. Med. Microbiol. 291: 501-509.
    CrossRef
  57. Grissa I, Vergnaud G, Pourcel C. 2007. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 8: 172.
    Pubmed KoreaMed CrossRef
  58. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729.
    Pubmed KoreaMed CrossRef