Skip to main content

Advertisement

SpringerLink
Log in

Multilocus sequence typing analysis of Cronobacter spp. isolated from China

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Multilocus sequence typing (MLST) has proven to be an effective approach for the subtyping isolates of the Cronobacter genus and to exhibit a high level of discrimination between isolates. In this study, 151 Cronobacter strains were isolated from different sources and provinces across China from 2010 to 2012 and analyzed by MLST. Their sequence type profiles were compared with strains from other countries which were widely geographically and temporally distributed. Out of 151 strains in this study, the majority of strains were Cronobacter sakazakii (70.9 %), C. malonaticus (15.9 %), C. dublinensis (10.6 %), C. turicensis (2.0 %), and C. muytjensii (0.7 %). The strains were divided into 85 sequence types (STs), among which only 17 had previously been reported in other countries. The 85 identified STs for the Cronobacter genus were grouped into 14 clonal complexes and 47 singletons according to eBURST algorithm. The Cronobacter isolated from China showed a high diversity when they were subtyped using the MLST method. When compared to the Cronobacter PubMLST database, some sequence types of strains cultured from food and/or water in this study were also the same with strains isolated from patients in other countries as reported previously. This result showed the potential hazard of strains contaminating water and weaning food from China.

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

Similar content being viewed by others

References

  • Caubilla-Barron J, Hurrell E, Townsend S, Cheetham P, Loc-Carrillo C et al (2007) Genotypic and phenotypic analysis of Enterobacter sakazakii strains from an outbreak resulting in fatalities in a neonatal intensive care unit in France. J Clin Microbiol 45:3979–3985

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • CDC (2011) CDC update: investigation of Cronobacter infection among infants in the United States. http://www.cdc.gov/foodsafety/diseases/cronobacter/investigation.html/

  • Chap J, Jackson P, Siqueira R, Gaspar N, Quintas C et al (2009) International survey of Cronobacter sakazakii and other Cronobacter spp. in follow up formulas and infant foods. Int J Food Microbiol 136:185–188

    Article  CAS  PubMed  Google Scholar 

  • Drudy D, Mullane NR, Quinn T, Wall PG, Fanning S (2006) Enterobacter sakazakii: an emerging pathogen in powdered infant formula. Clin Infect Dis Off Publ Infect Dis Soc Am 42:996–1002

    Article  CAS  Google Scholar 

  • FAO-WHO (2008) Enterobacter sakazakii (Cronobacter spp.) in powdered follow-up formulae. Microbiological risk assessment series no. 15. http://www.who.int/foodsafety/publications/Microsoft/mra_followup/en/

  • Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG (2004) eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186:1518–1530

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Forsythe SJ, Dickins B, Jolley KA (2014) Cronobacter, the emergent bacterial pathogen Enterobacter sakazakii comes of age; MLST and whole genome sequence analysis. BMC Genom 15:1121

    Google Scholar 

  • Hariri S, Joseph S, Forsythe SJ (2013) Cronobacter sakazakii ST4 strains and neonatal meningitis, United States. Emerg Infect Dis 19:175–177

    Article  PubMed Central  PubMed  Google Scholar 

  • Holý O, Petrželová J, Hanulík V, Chromá M, Matoušková I, Forsythe SJ (2014) Epidemiology of Cronobacter spp. isolates from patients admitted to the Olomouc University Hospital (Czech Republic). Epidemiol Mikrobiol Imunol 63:69–72

    PubMed  Google Scholar 

  • Huson DH (1998) Splits Tree: analyzing and visualizing evolution data. Bioinformatics 14:68–73

    Article  CAS  PubMed  Google Scholar 

  • Iversen C, Mullance N, McCardell B, Tall BD, Lehner A, Fanning S, Stephan R, Joosten H (2008) Cronobacter gen. nov., a new genus to accommodate the biogroups of Enterobacter sakazakii, and proposal of Cronobacter sakazakii gen. nov., comb. nov., Cronobacter malonaticus sp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov., Cronobacter genomospecies 1, and of three subspecies, Cronobacter dublinensis subsp. dublinensis subsp. nov., Cronobacter dublinensis subsp. lausannensis subsp. nov. and Cronobacter dublinensis subsp. lactaridi subsp. nov. Int J Syst Evol Microbiol 58:1442–1447

    Article  CAS  PubMed  Google Scholar 

  • Joseph S, Forsythe SJ (2012) Insights into the emergent bacterial pathogen Cronobacter spp., generated by multilocus sequence typing and analysis. Front Microbiol 3:397

    Article  PubMed Central  PubMed  Google Scholar 

  • Joseph S, Cetinkaya E, Drahovska H, Levican A, Figueras MJ et al (2012a) Cronobacter condimenti sp. nov., isolated from spiced meat, and Cronobacter universalis sp. nov., a species designation for Cronobacter sp. genomospecies 1, recovered from a leg infection, water and food ingredients. Int J Syst Evol Microbiol 62:1277–1283

    Article  CAS  PubMed  Google Scholar 

  • Joseph S, Desai P, Ji Y, Cummings CA, Shih R, Degoricija L, Rico A, Brzoska P, Hamby SE, Masood N, Hariri S, Sonbol H, Chuzhanova N, McClelland M, Furtado MR, Forsythe SJ (2012b) Comparative analysis of genome sequences covering the seven Cronobacter species. PLoS Osne 7:e49455

    Article  CAS  Google Scholar 

  • Joseph S, Sonbol H, Hariri S, Desai P, McClelland M et al (2012c) Diversity of the Cronobacter genus as revealed by multilocus sequence typing. J Clin Microbiol 50:3031–3039

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Joseph S, Hariri S, Forsythe SJ (2013) Lack of continuity between Cronobacter biotypes and species as determined using multilocus sequence typing. Mol Cell Probes 27:137–139

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Yang Y, Cui J, Liu L, Hu G, Shi Y, Li J (2013) Evaluation and implementation of a membrane filter method for Cronobacter detection in drinking water. FEMS Microbiol Lett 344:60–68

    Article  PubMed  Google Scholar 

  • Pan Z, Cui J, Lyu G, Du X, Qin L, Guo Y, Xu B, Li W, Cui Z, Zhao C (2014) Isolation and molecular typing of Cronobacter spp. in commercial powdered infant formula and follow-up formula. Foodborne Pathog Dis 11:456–461

    Article  CAS  PubMed  Google Scholar 

  • Reij MW, Jongenburger I, Gkogka E, Gorris LG, Zwietering MH (2009) Perspective on the risk to infants in the Netherlands associated with Cronobacter spp. occurring in powdered infant formula. Int J Food Microbiol 136:232–237

    Article  CAS  PubMed  Google Scholar 

  • Seo KH, Brackett RE (2005) Rapid, specific detection of Enterobacter sakazakii in infant formula using a real-time PCR assay. J Food Prot 68:59–63

    CAS  PubMed  Google Scholar 

  • Townsend S, Hurrell E, Forsythe S (2008) Virulence studies of Enterobacter sakazakii isolates associated with a neonatal intensive care unit outbreak. BMC Microbiol 8:64

    Article  PubMed Central  PubMed  Google Scholar 

  • Urmenyi AM, Franklin AW (1961) Neonatal death from pigmented coliform infection. Lancet 1:313–315

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Science and Technology Key Project, China (No. 2012ZX10004-215).

Author information

Authors and Affiliations

  1. National Institute for Communicable Disease Control and Prevention and State Key Laboratory for Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, Beijing, China

    Jing-Hua Cui, Xiao-Li Du, Hai-Jian Zhou, Wei Li & Zhi-Gang Cui

  2. Qinghai Institute for Endemic Diseases Prevention and Control, Xining, China

    Rong-Jie Wei

  3. Pathogen Research Group, School of Science and Technology, Nottingham Trent University, Clifton Lane, Nottingham, NG11 8NS, UK

    Stephen Forsythe

Authors
  1. Jing-Hua Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiao-Li Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rong-Jie Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hai-Jian Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stephen Forsythe
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhi-Gang Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhi-Gang Cui.

Additional information

Communicated by Erko Stackebrandt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cui, JH., Du, XL., Wei, RJ. et al. Multilocus sequence typing analysis of Cronobacter spp. isolated from China. Arch Microbiol 197, 665–672 (2015). https://doi.org/10.1007/s00203-015-1097-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-015-1097-0

Keywords

Search

Navigation