Skip to main content
SpringerLink
Log in

Genome sequence of lung pathogenic Escherichia coli O78, a chimeric strain isolated from pneumonia forest musk deer

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

Pneumonia is one of the major diseases of forest musk deer (FMD) that affects the survival of musk deer breeding farms. Lung pathogenic Escherichia coli (LPEC) strains were found to be one of the principal bacterial pathogens, and O78 was found to be the dominant serotype and the most poisonous, thus it was selected as further study. Here we have finished the LPEC O78 genome sequence, genomic comparative analysis and genome annotation. In the genome of LPEC O78, genes encoded major virulence factors (VFs) of urinary tract infection (UTI) and neonatal meningitis-causing E. coli (NMEC) were detected. The phylogenetic analysis indicated that LPEC O78 belongs to the D group of E. coli and clustered with human uropathogenic E. coli (UPEC) UMNO26. Orthologous analysis showed that LPEC O78 was close to UMNO26 in evolutionary relationships, the results were consistent with phylogenetic analysis. Additionally, analysis of the specific genes using COG, GO and Swiss-Prot databases revealed specific functions in the LPEC O78, some of these differences might reflect the pathogenicity of LPEC O78. It was the first time that LPEC from FMD was sequenced, through the virulence gene analysis, an example of a genome of chimeric pathogenic properties was found. The results were in favor of the possibility that strain of animal origin LPEC O78 was dangerous for public health and consequently constitute a zoonotic risk. Moreover, the functions study of specific genes will facilitate understand the pathogenicity of LPEC O78, and aid in the development of control measures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT et al (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 9:75

    Article  Google Scholar 

  • Bailone A, Bäckman A, Sommer S, Célérier J, Bagdasarian MM, Bagdasarian M, Devoret R (1988) PsiB polypeptide prevents activation of RecA protein in Escherichia coli. Mol Gen Genet 214:389–395

    Article  CAS  PubMed  Google Scholar 

  • Bauer AW, Kirby WM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45:493–496

    CAS  PubMed  Google Scholar 

  • Blanco J, Mora A, Mamani R, Lopez C, Blanco M, Dahbi G, Herrera A, Blanco JE, Alonso MP, Garcia-Garrote F et al (2011) National survey of Escherichia coli causing extraintestinal infections reveals the spread of drug-resistant clonal groups O25b:H4-B2-ST131, O15:H1-D-ST393 and CGA-D-ST69 with high virulence gene content in Spain. J Antimicrob Chemother 66:2011–2021

    Article  CAS  PubMed  Google Scholar 

  • Bonacorsi S, Bingen E (2005) Molecular epidemiology of Escherichia coli causing neonatal meningitis. Int J Med Microbiol 295:373–381

    Article  CAS  PubMed  Google Scholar 

  • Boutet E, Lieberherr D, Tognolli M, Schneider M, Bairoch A (2007) UniProtKB/Swiss-Prot. Methods Mol Biol 406:89–112

    CAS  PubMed  Google Scholar 

  • Cagnacci S, Gualco L, Debbia E, Schito GC, Marchese A (2008) European emergence of ciproflo- xacin-resistant Escherichia coli clonal groups O25:H4-ST 131 and O15:K52:H1 causing community-acquired uncomplicated cystitis. J Clin Microbiol 46:2605–2612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cavalli SL, Edwards AW (1967) Phylogenetic analysis Models and estimation procedures. Am J Hum Genet 19:233–257

    Google Scholar 

  • Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y, Jin Q (2005) VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 33:D325–D328

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Xiong Z, Sun L, Yang J, Jin Q (2012). http://www.mgc.ac.cn/VFs/main.htm. Accessed 20 March 2016

  • Clermont O, Christenson JK, Denamur E, Gordon DM (2013) The Clermont Escherichia coli phylotyping method revisited improvement of specificity and detection of new phylogroups. Environ Microbiol Rep 5:58–65

    Article  CAS  PubMed  Google Scholar 

  • Coque TM, Novais A, Carattoli A, Poirel L, Pitout J, Peixe L, Baquero F, Canton R, Nordmann P (2008) Dissemination of clonally related Escherichia coli strains expressing extended-spectrum beta-lactamase CTX-M-15. Emerg Infect Dis 14:195–200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui HM, Shu GS, Cheng AC, Zhang HX, Cai YH, Dai XY (1996) Pathological observation of colibacillosis in domestic musk deer. Chin J Vet Sci Technol 26:34–35

    Google Scholar 

  • De Pace F, Nakazato G, Pacheco A, de Paiva JB, Sperandio V, Da SW (2010) The type VI secretion system plays a role in type 1 fimbria expression and pathogenesis of an avian pathogenic Escherichia coli strain. Infect Immun 78:4990–4998

    Article  PubMed  PubMed Central  Google Scholar 

  • Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dutreix M, Backman A, Celerier J, Bagdasarian MM, Sommer S, Bailone A, Devoret R, Bagdasarian M (1988) Identification of psiB genes of plasmids F and R6-5. Molecular basis for psiB enhanced expression in plasmid R6-5. Nucleic Acids Res 16:10669–10679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gibreel TM, Dodgson AR, Cheesbrough J, Fox AJ, Bolton FJ, Upton M (2012) Population structure, virulence potential and antibiotic susceptibility of uropathogenic Escherichia coli from Northwest England. J Antimicrob Chemother 67:346–356

    Article  CAS  PubMed  Google Scholar 

  • Gillings MR, Stokes HW (2012) Are humans increasing bacterial evolvability?. Trends Ecol Evol 27:346–352

    Article  PubMed  Google Scholar 

  • Glode MP, Sutton A, Moxon ER, Robbins JB (1977) Pathogenesis of neonatal Escherichia coli meningitis: induction of bacteremia and meningitis in infant rats fed E coli K1. Infect Immun 16:75–80

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goerke C, Pantucek R, Holtfreter S, Schulte B, Zink M, Grumann D, Broker BM, Doskar J, Wolz C (2009) Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J Bacteriol 191:3462–3468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golub EI, Bailone A, Devoret R (1988) A gene encoding an SOS inhibitor is present in different conjugative plasmids. J Bacteriol 170:4392–4394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grissa I, Vergnaud G, Pourcel C (2007) CRISPR Finder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35:W52–W57

    Article  PubMed  PubMed Central  Google Scholar 

  • Guerra B, Junker E, Schroeter A, Malorny B, Lehmann S, Helmuth R (2003) Phenotypic and genotypic characterization of antimicrobial resistance in German Escherichia coli isolates from cattle, swine and poultry. J Antimicrob Chemother 52:489–492

    Article  CAS  PubMed  Google Scholar 

  • Herzer PJ, Inouye S, Inouye M, Whittam TS (1990) Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J Bacteriol 172:6175–6181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffman JA, Badger JL, Zhang Y, Huang SH, Kim KS (2000) Escherichia coli K1 aslA contributes to invasion of brain microvascular endothelial cells in vitro and in vivo. Infect Immun 68:5062–5067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howland CJ, Rees CED, Barth PT, Wilkins BM (1989) The ssb gene of plasmid ColIb-P9. J Bacteriol 171:2466–2473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iguchi A, Thomson NR, Ogura Y, Saunders D, Ooka T, Henderson IR, Harris D, Asadulghani M, Kurokawa K, Dean P (2009) Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127 H6 strain E2348/69. J Bacteriol 191:347–354

    Article  CAS  PubMed  Google Scholar 

  • Jakobsen L, Hammerum AM, Frimodt-Moller N (2010) Detection of clonal group A Escherichia coli isolates from broiler chickens, broiler chicken meat, community-dwelling humans, and urinary tract infection (UTI) patients and their virulence in a mouse UTI model. Appl Environ Microbiol 76:8281–8284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janben T, Schwarz C, Preikschat P, Voss M, Philipp HC, Wieler LH (2001) Virulence-associated genes in avian pathogenic Escherichia coli (APEC) isolated from internal organs of poultry having died from colibacillosis. Int J Med Microbiol 291:371–378

    Article  CAS  PubMed  Google Scholar 

  • Jeong H, Barbe V, Lee CH, Vallenet D, Yu DS, Choi SH, Couloux A, Lee SW, Yoon SH, Cattolico L (2009) Genome sequences of Escherichia coli B strains REL606 and BL21 (DE3). J Mol Biol 394:644–652

    Article  CAS  PubMed  Google Scholar 

  • Jeong H, Zhao F, Igori D, Oh KH, Kim SY, Kang SG, Kim BK, Kwon SK, Lee CH, Song JY (2012) Genome sequence of the hemolytic-uremic syndrome-causing strain Escherichia coli NCCP15647. J Bacteriol 194:3747–3748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson JR, Menard M, Johnston B, Kuskowski MA, Nichol K, Zhanel GG (2009) Epidemic clonal groups of Escherichia coli as a cause of antimicrobial-resistant urinary tract infections in Canada, 2002 to 2004. Antimicrob Agents Chemother 53:2733–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson JR, Menard ME, Lauderdale TL, Kosmidis C, Gordon D, Collignon P, Maslow JN, Andrasevic AT, Kuskowski MA (2011) Global distribution and epidemiologic associations of Escherichia coli clonal group A, 1998–2007. Emerg Infect Dis 17:2001–2009

    PubMed  Google Scholar 

  • Kaper JB, Nataro JP, Mobley HL (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2:123–140

    Article  CAS  PubMed  Google Scholar 

  • Kerenyi M, Allison HE, Batai I, Sonnevend A, Emody L, Plaveczky N, Pal T (2005) Occurrence of hlyA and sheA genes in extraintestinal Escherichia coli strains. J Clin Microbiol 43:2965–2968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim KS (2003) Pathogenesis of bacterial meningitis from bacteraemia to neuronal injury. Nat Rev Neurosci 4:376–385

    Article  CAS  PubMed  Google Scholar 

  • Kim KS, Itabashi H, Gemski P, Sadoff J, Warren RL, Cross AS (1992) The K1 capsule is the critical determinant in the development of Escherichia coli meningitis in the rat. J Clin Invest 90:897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim BK, Song GC, Hong GH, Seong WK, Kim SY, Jeong H, Kang SG, Kwon SK, Lee CH, Song JY et al (2012) Genome sequence of the Shiga toxin-producing Escherichia coli strain NCCP15657. J Bacteriol 194:3751–3752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kluge AG, Farris JS (1969) Quantitative phyletics and the evolution of the anurans. Syst Zool 18:1–32

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langermann S, Palaszynski S, Barnhart M, Auguste G, Pinkner JS, Burlein J, Barren P, Koenig S, Leath S, Jones CH et al (1997) Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science 276:607–611

    Article  CAS  PubMed  Google Scholar 

  • Lee MY, Choi HJ, Choi JY, Song M, Song Y, Kim SW, Chang HH, Jung SI, Kim YS, Ki HK (2010) Dissemination of ST131 and ST393 community-onset, ciprofloxacin-resistant Escherichia coli clones causing urinary tract infections in Korea. J Infect 60:146–153

    Article  PubMed  Google Scholar 

  • Leonard SR, Lacher DW, Lampel KA (2015) Draft Genome Sequences of the Enteroinvasive Escherichia coli Strains M4163 and 4608-58. Genome Announc 3:e01395–14

    Article  PubMed  PubMed Central  Google Scholar 

  • Li L, Stoeckert CJ, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13:2178–2189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu B, Pop M (2009). http://ardb.cbcb.umd.edu/. Accessed 10 May 2016

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y et al (2012a) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 1:18

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo Y, Wang P, Zhao HM, Feng YW, Wu GL, Cheng JG, Zou LK, Kang JP, Ma BC, Li B (2012b) Isolation and identification of lung pathogenic Escherichia coli from musk deer and PCR detection of the virulence genes. Chin J Prev Vet Med 34:615–618

    CAS  Google Scholar 

  • Mokady D, Gophna U, Ron EZ (2005) Virulence factors of septicemic Escherichia coli strains. Int J Med Microbiol 295:455–462

    Article  CAS  PubMed  Google Scholar 

  • Muhammad AA, Alam S, Hassan SM, Shirin M (2009) Antibiotic resistance of Escherichia coli isolated from poultry and poultry environment of Bangladesh. Int J food Saf 11:19–23

    Google Scholar 

  • Novais A, Vuotto C, Pires J, Montenegro C, Donelli G, Coque TM, Peixe L (2013) Diversity and biofilm-production ability among isolates of Escherichia coli phylogroup D belonging to ST69, ST393 and ST405 clonal groups. BMC Microbiol 13(1):144

    Article  PubMed  PubMed Central  Google Scholar 

  • Olesen B, Scheutz F, Menard M, Skov MN, Kolmos HJ, Kuskowski MA, Johnson JR (2009) Three-decade epidemiological analysis of Escherichia coli O15:K52:H1. J Clin Microbiol 47:1857–1862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prasadarao N, Wass C, Weiser JN, Stins MF, Huang SH, Kim KS (1996) Identification of membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect Immun 64:146–153

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rahman M, Rahman BM, Rahman B (2008) Antibiogram and plasmid profile analysis of isolated Escherichia coli from broiler and layer. Res J Microbiol 3:82–90

    Article  Google Scholar 

  • Rasko DA, Rosovitz MJ, Myers GS, Mongodin EF, Fricke WF (2008) The pangenome structure of Escherichia coli: comparative genomic analysis of E coli commensal and pathogenic isolates. J Bacteriol 190:6881–6893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sheng HL, Liu ZX (2007) The Musk Deer in China. Shanghai Scientific & Technical Publishers, Shanghai

    Google Scholar 

  • Song JY, Yoo RH, Jang SY, Seong WK, Kim SY, Jeong H, Kang SG, Kim BK, Kwon SK, Lee CH et al (2012) Genome sequence of enterohemorrhagic Escherichia coli NCCP15658. J Bacteriol 194:3749–3750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 60. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang J, Li FR, Wang YQ, Liu WH (2011) Epidemiological Survey on Suppurate Disease among Musk Deer in Shaanxi Province. Spec Wild Econ Anim Plant Res 63–64

  • Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000). https://www.ncbi.nlm.nih.gov/COG/. Accessed 20 Aug 2016

  • Urwin R, Maiden MC (2003) Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol 11:479–487

    Article  CAS  PubMed  Google Scholar 

  • Wang Y (2002) The function of OmpA in Escherichia coli. Biochem Biophys Res Commun 292:396–401

    Article  CAS  PubMed  Google Scholar 

  • Wayne PA (2009) Performance Standards for Antimicrobial Susceptibility Testing; Nineteenth Informational Supplement Clinical and Laboratory Standards Institute

  • Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MCJ, Ochman H et al (2006). http://mlst.warwick.ac.uk/mlst. Accessed 26 March 2016

  • Woodford N, Turton JF, Livermore DM (2011) Multiresistant gram-negative bacteria: the role of high-risk clones in the dissemination of antibiotic resistance. FEMS Microbiol Rev 35:736–755

    Article  CAS  PubMed  Google Scholar 

  • Zang YT, Yan YL, Gao H, Gao LB, Zhao R, Li XF, Shao ZY, Lu Q, Cui YY (2012) Progress on the HPI of pathogenic Escherichia coli. Prog Vet Med 33:153–156

    Google Scholar 

  • Zhang E (1998) Musk Deer. In: Wemmer C, (ed) Deer, status survey and conservation action plan, Gland IUCN, Cambridge, pp 72–77

    Google Scholar 

  • Zhao S, Maurer JJ, Hubert S, De Villena JF, McDermott PF, Meng J, Ayers S, English L, White DG (2005) Antimicrobial susceptibility and molecular characterization of avian pathogenic Escherichia coli isolates. Vet Microbiol 107:215–224

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39:347–352

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Science and Technology Support Program of Sichuan Provincial Science and Technology Department and the Academic and Technical Leaders Nurturing Fund of Sichuan Provincial Human Resources and Social Security Department.

Author information

Author notes

    Authors and Affiliations

    1. College of Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People’s Republic of China

      Qing Tian, Xin Zhou, Yan Luo, Wei Zhao & Wuyou Wang

    2. Sichuan Institute of Musk Deer Breeding, Dujiangyan, 611830, People’s Republic of China

      Jianguo Cheng

    3. Department of Veterinary Microbiology and Preventive Medicine, Iowa State University, Ames, IA, 50011, USA

      Lei Dai

    Authors
    1. Qing Tian
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Xin Zhou
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Jianguo Cheng
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Yan Luo
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Lei Dai
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Wei Zhao
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Wuyou Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Yan Luo.

    Ethics declarations

    Conflict of interest

    Qing Tian declares that he/she does not have conflict of interest. Xin Zhou declares that he/she does not have conflict of interest. Jianguo Cheng declares that he/she does not have conflict of interest. Yan Luo declares that he/she does not have conflict of interest. Lei Dai declares that he/she does not have conflict of interest. Wei Zhao declares that he/she does not have conflict of interest. Wuyou Wang declares that he/she does not have conflict of interest.

    Ethical approval

    All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the Sichuan Agricultural University on the human and animal research ethical committee.

    Informed consent

    Informed consent was obtained from all individual participants included in the study.

    Additional information

    Qing Tian and Xin Zhou have contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (DOCX 339 KB)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Tian, Q., Zhou, X., Cheng, J. et al. Genome sequence of lung pathogenic Escherichia coli O78, a chimeric strain isolated from pneumonia forest musk deer. Genes Genom 39, 805–815 (2017). https://doi.org/10.1007/s13258-017-0545-4

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s13258-017-0545-4

    Keyword

    Search

    Navigation