Complete genome sequence of uropathogenic Escherichia coli isolate UPEC 26-1

  • Bindu Subhadra
  • Dong Ho Kim
  • Jaeseok Kim
  • Kyungho Woo
  • Kyung Mok Sohn
  • Hwa-Jung Kim
  • Kyudong Han
  • Man Hwan Oh
  • Chul Hee Choi
Research Article
  • 13 Downloads

Abstract

Urinary tract infections (UTIs) are among the most common infections in humans, predominantly caused by uropathogenic Escherichia coli (UPEC). The diverse genomes of UPEC strains mostly impede disease prevention and control measures. In this study, we comparatively analyzed the whole genome sequence of a highly virulent UPEC strain, namely UPEC 26-1, which was isolated from urine sample of a patient suffering from UTI in Korea. Whole genome analysis showed that the genome consists of one circular chromosome of 5,329,753 bp, comprising 5064 protein-coding genes, 122 RNA genes (94 tRNA, 22 rRNA and 6 ncRNA genes), and 100 pseudogenes, with an average G+C content of 50.56%. In addition, we identified 8 prophage regions comprising 5 intact, 2 incomplete and 1 questionable ones and 63 genomic islands, suggesting the possibility of horizontal gene transfer in this strain. Comparative genome analysis of UPEC 26-1 with the UPEC strain CFT073 revealed an average nucleotide identity of 99.7%. The genome comparison with CFT073 provides major differences in the genome of UPEC 26-1 that would explain its increased virulence and biofilm formation. Nineteen of the total GIs were unique to UPEC 26-1 compared to CFT073 and nine of them harbored unique genes that are involved in virulence, multidrug resistance, biofilm formation and bacterial pathogenesis. The data from this study will assist in future studies of UPEC strains to develop effective control measures.

Keywords

UPEC UTI Genome annotation Genome sequencing Genomic islands Pathogenic genes 

Notes

Acknowledgements

This work was supported by research fund of Chungnam National University (2015). Also, it was supported by Chungnam National University Hospital Research Fund, 2013.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

The article does not contain any studies with human participants performed by any of the authors.

Supplementary material

13258_2018_665_MOESM1_ESM.xls (160 kb)
Supplementary material 1 (XLS 160 KB)
13258_2018_665_MOESM2_ESM.xls (35 kb)
Supplementary material 2 (XLS 35 KB)

References

  1. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA (2011) BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genom 12:402CrossRefGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  3. Alva V, Nam SZ, Söding J, Lupas AN (2016) The MPI bioinformatics Toolkit as an integrative platform for advanced protein sequence and structure analysis. Nucleic Acids Res 44:W410–W415CrossRefPubMedPubMedCentralGoogle Scholar
  4. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M et al (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genom 9:75CrossRefGoogle Scholar
  5. Bergsten G, Wullt B, Svanborg C (2005) Escherichia coli, fimbriae, bacterial persistence and host response induction in the human urinary tract. Int J Med Microbiol 295:487–502CrossRefPubMedGoogle Scholar
  6. Brenner DJ (1984) Family I. Enterobacteriaceae Rahn 1937, Nom. fam. cons. Opin. 15, Jud. Com. 1958, 73; Ewing, Farmer, and Brenner 1980, 674; Judicial Commission 1981, 104. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology, 1st edn. The Williams & Wilkins Co., Baltimore, pp 408–420Google Scholar
  7. Cloud-Hansen KA, Peterson SB, Stabb EV, Goldman WE, McFall-Ngai MJ, Handelsman J (2006) Breaching the great wall: peptidoglycan and microbial interactions. Nat Rev Microbiol 4:710–716CrossRefPubMedGoogle Scholar
  8. Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679CrossRefPubMedPubMedCentralGoogle Scholar
  9. Dhillon BK, Laird MR, Shay JA, Winsor GL, Lo R, Nizam F, Pereira SK, Waglechner N, McArthur AG, Langille MG et al (2015) IslandViewer 3: more flexible, interactive genomic island discovery, visualization and analysis. Nucleic Acids Res 43:W104–W108CrossRefPubMedPubMedCentralGoogle Scholar
  10. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefPubMedPubMedCentralGoogle Scholar
  11. Escherich T (1886) Die Darmbakterien des Säuglings und ihre Beziehungen zur Physiologie der Verdauung. Ferdinand Enke, Stuttgart, pp 63–74Google Scholar
  12. Farshad S, Ranjbar R, Japoni A, Hosseini M, Anvarinejad M, Mohammadzadegan R (2012) Microbial susceptibility, virulence factors, and plasmid profiles of uropathogenic Escherichia coli strains isolated from children in Jahrom, Iran. Arch Iran Med 15:312–316PubMedGoogle Scholar
  13. Foxman B (2010) The epidemiology of urinary tract infection. Nat Rev Urol 7:653–660CrossRefPubMedGoogle Scholar
  14. Foxman B, Brown P (2003) Epidemiology of urinary tract infections: transmission and risk factors, incidence, and costs. Infect Dis Clin North Am 17:227–241CrossRefPubMedGoogle Scholar
  15. Fukiya S, Mizoguchi H, Tobe T, Mori H (2004) Extensive genomic diversity in pathogenic Escherichia coli and Shigella Strains revealed by comparative genomic hybridization microarray. J Bacteriol 186:3911–3921CrossRefPubMedPubMedCentralGoogle Scholar
  16. Grissa I, Vergnaud G, Pourcel C (2007) CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35:W52–W57CrossRefPubMedPubMedCentralGoogle Scholar
  17. Käll L, Krogh A, Sonnhammer EL (2007) Advantages of combined transmembrane topology and signal peptide prediction—the Phobius web server. Nucleic Acids Res 35:W429–W432CrossRefPubMedPubMedCentralGoogle Scholar
  18. Kim DH, Choi CH (2017) Clonal and Virulence distribution of Uropathogenic Escherichia coli Isolated from Children in Korea. J Bacteriol Virol 7:54–63CrossRefGoogle Scholar
  19. Kim YC, Tarr AW, Penfold CN (2014) Colicin import into E. coli cells: a model system for insights into the import mechanisms of bacteriocins. ‎Biochim Biophys Acta 1843:1717–1731CrossRefPubMedGoogle Scholar
  20. Kulkarni R, Dhakal BK, Slechta ES, Kurtz Z, Mulvey MA, Thanassi DG (2009) Roles of putative type II secretion and type IV pilus systems in the virulence of uropathogenic Escherichia coli. PLoS One 4:e4752CrossRefPubMedPubMedCentralGoogle Scholar
  21. Kurtz S, Phillippy A, Delcher AL, Smoot M, Schumway M, Antonescu C, Salzberg SL (2004) Versatile and open software for comparing large genomes. Genome Biol 5:R12CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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 35:3100–3108CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lee JH, Subhadra B, Son YJ, Kim DH, Park HS, Kim JM, Koo SH, Oh MH, Kim HJ, Choi CH (2016) Phylogenetic group distributions, virulence factors and antimicrobial resistance properties of uropathogenic Escherichia coli strains isolated from patients with urinary tract infections in South Korea. Lett Appl Microbiol 62:84–90CrossRefPubMedGoogle Scholar
  24. Lloyd AL, Rasko DA, Mobley HL (2007) Defining genomic islands and uropathogen-specific genes in uropathogenic Escherichia coli. J Bacteriol 189:3532–3546CrossRefPubMedPubMedCentralGoogle Scholar
  25. Lloyd AL, Henderson TA, Vigil PD, Mobley HL (2009) Genomic islands of uropathogenic Escherichia coli contribute to virulence. J Bacteriol 191:3469–3481CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964CrossRefPubMedPubMedCentralGoogle Scholar
  27. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI et al (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43:D222–D226CrossRefPubMedGoogle Scholar
  28. Møller TSB, Overgaard M, Nielsen SS, Bortolaia V, Sommer MOA, Guardabassi L, Olsen JE (2016) Relation between tetR and tetA expression in tetracycline resistant Escherichia coli. BMC Microbiol 16:39CrossRefPubMedPubMedCentralGoogle Scholar
  29. Mulvey MA (2002) Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol 4:257–271CrossRefPubMedGoogle Scholar
  30. Mutschler H, Meinhart A (2011) Epsilon/zeta systems: their role in resistance, virulence, and their potential for antibiotic development. J Mol Med (Berl) 89:1183–1194CrossRefPubMedCentralGoogle Scholar
  31. Oliveira FA, Paludo KS, Arend LN, Farah SM, Pedrosa FO, Souza EM, Surek M, Picheth G, Fadel-Picheth CM (2011) Virulence characteristics and antimicrobial susceptibility of uropathogenic Escherichia coli strains. Genet Mol Res 10:4114–4125CrossRefPubMedGoogle Scholar
  32. Scheutz F, Strockbine NA (2005) Genus I. Escherichia Castellani and Chalmers 1919. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology. Springer, New York, pp 607–624Google Scholar
  33. Sun Z, Shi J, Liu C, Jin Y, Li K, Chen R, Jin S, Wu W (2014) PrtR homeostasis contributes to Pseudomonas aeruginosa pathogenesis and resistance against ciprofloxacin. Infect Immun 82:1638–1647CrossRefPubMedPubMedCentralGoogle Scholar
  34. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  35. Tatusov RL, Koonin EV, Lipman DJ (1997) A genomic perspective on protein families. Science 278:631–637CrossRefPubMedGoogle Scholar
  36. Vila J, Pal T (2010) Update on antibacterial resistance in low-income countries: factors favoring the emergence of resistance. Open Infect Dis J 4:38–54Google Scholar
  37. Welch RA (2005) 3.3.3 The genus Escherichia. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes, 3rd edn. Springer, Berlin, pp 62–71Google Scholar
  38. Welch RA, Burland V, Plunkett G 3rd, Redford P, Roesch P, Rasko D, Buckles EL, Liou SR, Boutin A, Hackett J et al (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 99:17020–17024CrossRefPubMedPubMedCentralGoogle Scholar
  39. Withman B, Gunasekera TS, Beesetty P, Agans R, Paliy O (2013) Transcriptional responses of uropathogenic Escherichia coli to increased environmental osmolality caused by salt or urea. Infect Immun 81:80–89CrossRefPubMedPubMedCentralGoogle Scholar
  40. Wood JM, Bremer E, Csonka LN, Kraemer R, Poolman B, van der Heide T, Smith LT (2001) Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem Physiol A Mol Integr Physiol 130:437–460CrossRefPubMedGoogle Scholar
  41. Yamada M, Nakazawa A (1984) Factors necessary for the export process of colicin E1 across cytoplasmic membrane of Escherichia coli. Eur J Biochem 140:249–255CrossRefPubMedGoogle Scholar
  42. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39:W347–W352CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Genetics Society of Korea and Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Microbiology and Medical ScienceChungnam National University School of MedicineDaejeonRepublic of Korea
  2. 2.Division of Infectious DiseasesChungnam National University HospitalDaejeonRepublic of Korea
  3. 3.Department of Nanobiomedical ScienceDankook UniversityCheonanRepublic of Korea
  4. 4.BK21 PLUS NBM Global Research Center for Regenerative MedicineDankook UniversityCheonanRepublic of Korea

Personalised recommendations