Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

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

  • Gnanasekaran, Gopalsamy (Department of Agricultural Biotechnology, Seoul National University) ;
  • Na, Eun Jung (Department of Agricultural Biotechnology, Seoul National University) ;
  • Chung, Han Young (Department of Agricultural Biotechnology, Seoul National University) ;
  • Kim, Suyeon (Department of Agricultural Biotechnology, Seoul National University) ;
  • Kim, You-Tae (Food-borne Pathogen Omics Research Center (FORC), Seoul National University) ;
  • Kwak, Woori (Department of Agricultural Biotechnology, Seoul National University) ;
  • Kim, Heebal (Department of Agricultural Biotechnology, Seoul National University) ;
  • Ryu, Sangryeol (Department of Agricultural Biotechnology, Seoul National University) ;
  • Choi, Sang Ho (Department of Agricultural Biotechnology, Seoul National University) ;
  • Lee, Ju-Hoon (Food-borne Pathogen Omics Research Center (FORC), Seoul National University)
  • Received : 2016.11.17
  • Accepted : 2016.11.24
  • Published : 2017.02.28
Download PDF
⟨ Previous Next ⟩

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 evasion-associated 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

References

  1. Tauxe RV. 1997. Emerging foodborne diseases: an evolving public health challenge. Emerg. Infect. Dis. 3: 425. https://doi.org/10.3201/eid0304.970403
  2. Toma S, Lafleur L. 1974. Survey on the incidence of Yersinia enterocolitica infection in Canada. J. Appl. Microbiol. 28: 469-473.
  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.
  4. Zadernowska A, Chajecka-Wierzchowska W, Laniewska-Trokenheim L. 2014. Yersinia enterocolitica: a dangerous, but often ignored, foodborne pathogen. Food Rev. Int. 30: 53-70. https://doi.org/10.1080/87559129.2013.853775
  5. Scott E. 2003. Food safety and foodborne disease in 21st century homes. Can. J. Infect. Dis. 14: 277. https://doi.org/10.1155/2003/363984
  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. https://doi.org/10.1016/S0168-1605(02)00232-5
  8. Bucher M, Meyer C, Grotzbach 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. https://doi.org/10.1089/fpd.2007.0076
  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. https://doi.org/10.1017/S0950268808001209
  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. https://doi.org/10.1016/0035-9203(84)90057-9
  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. https://doi.org/10.26719/2009.15.2.276
  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, Martinez 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. https://doi.org/10.1016/j.fm.2009.06.001
  14. Wauters G, Aleksic S, Charlier J, Schulze G. 1991. Somatic and flagellar antigens of Yersinia enterocolitica and related species. Contrib. Microbiol. Immunol. 12: 239.
  15. Bottone EJ. 1999. Yersinia enterocolitica: overview and epidemiologic correlates. Microbes Infect. 1: 323-333. https://doi.org/10.1016/S1286-4579(99)80028-8
  16. Brubaker RR. 1991. Factors promoting acute and chronic diseases caused by yersiniae. Clin. Microbiol. Rev. 4: 309-324. https://doi.org/10.1128/CMR.4.3.309
  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.
  18. Bottone EJ. 1997. Yersinia enterocolitica: the charisma continues. Clin. Microbiol. Rev. 10: 257-276.
  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.
  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.
  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. https://doi.org/10.1093/clinids/9.1.64
  22. Cornelis GR. 2006. The type III secretion injectisome. Nat. Rev. Microbiol. 4: 811-825. https://doi.org/10.1038/nrmicro1526
  23. Galan JE, Collmer A. 1999. Type III secretion m achines: bacterial devices for protein delivery into host cells. Science 284: 1322-1328. https://doi.org/10.1126/science.284.5418.1322
  24. Jin Q, Thilmony R, Zwiesler-Vollick J, He S-Y. 2003. Type III protein secretion in Pseudomonas syringae. Microbes Infect. 5: 301-310. https://doi.org/10.1016/S1286-4579(03)00032-7
  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.
  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. https://doi.org/10.1073/pnas.0507749103
  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 C4b-binding protein. PLoS Pathog. 4: e1000140. https://doi.org/10.1371/journal.ppat.1000140
  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. https://doi.org/10.1371/journal.ppat.1000067
  29. Home SM, Pruss 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. https://doi.org/10.1007/s00203-005-0077-1
  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.
  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. https://doi.org/10.1093/nar/gkq543
  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. https://doi.org/10.1038/nmeth.2474
  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. https://doi.org/10.1186/1471-2164-13-375
  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. https://doi.org/10.1186/1471-2105-11-319
  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. https://doi.org/10.1186/1471-2164-9-75
  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. https://doi.org/10.1186/1471-2164-12-444
  39. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. 2009. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25: 119-120. https://doi.org/10.1093/bioinformatics/btn578
  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. https://doi.org/10.1099/ijs.0.64483-0
  41. Paradis E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289-290. https://doi.org/10.1093/bioinformatics/btg412
  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. https://doi.org/10.1186/1471-2105-7-142
  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.
  45. Kanazawa Y, Kuramata T. 1976. Drug sensitivity of Yersinia enterocolitica and Yersinia pseudotuberculosis. Jpn. J. Antibiot. 29: 366-376. https://doi.org/10.7164/antibiotics.29.366
  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. https://doi.org/10.1016/j.freeradbiomed.2013.12.020
  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. https://doi.org/10.1128/jb.177.4.981-986.1995
  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. https://doi.org/10.1128/jb.171.1.254-262.1989
  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. https://doi.org/10.1186/1471-2180-8-214
  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. https://doi.org/10.1128/IAI.73.9.5961-5977.2005
  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. https://doi.org/10.1073/pnas.90.14.6473
  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 ${\beta}1$ integrins apically expressed on M-like cells. Cell. Microbiol. 2: 173-185. https://doi.org/10.1046/j.1462-5822.2000.00047.x
  53. Fabrega A, Vila J. 2012. Yersinia enterocolitica: pathogenesis, virulence and antimicrobial resistance. Enferm. Infecc. Microbiol. Clin. 30: 24-32. https://doi.org/10.1016/j.eimc.2011.07.017
  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. https://doi.org/10.1074/jbc.M306413200
  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. https://doi.org/10.1126/science.280.5372.2129
  56. Fallman M, Deleuil F, McGee K. 2001. Resistance to phagocytosis by Yersinia. Int. J. Med. Microbiol. 291: 501-509. https://doi.org/10.1078/1438-4221-00159
  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. https://doi.org/10.1186/1471-2105-8-172
  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. https://doi.org/10.1093/molbev/mst197

Cited by

  1. Isolation and Characterization of a Lytic and Highly Specific Phage against Yersinia enterocolitica as a Novel Biocontrol Agent vol.28, pp.11, 2017, https://doi.org/10.4014/jmb.1808.08001
  2. Genome-Wide Profiling of Enterotoxigenic Staphylococcus aureus Strains Used for the Production of Naturally Contaminated Cheeses vol.11, pp.1, 2017, https://doi.org/10.3390/genes11010033
  3. A general view on virulence determinants and infection strategies of Yersinia enterocolitica vol.32, pp.1, 2017, https://doi.org/10.23736/s1120-4826.19.02582-5
  4. Pathogenic potential and antibiotic resistance of Yersinia enterocolitica, a foodborne pathogen limited to swine tonsils in a pork production chain from Southern Brazil vol.52, pp.4, 2021, https://doi.org/10.1007/s42770-021-00591-3