Skip to main content
Log in

Investigation of the biofilm formation in extra-intestinal pathogenic Escherichia coli ST131 strains and its correlation with the presence of fimH, afa, and kpsMSTII genes

  • Microbial Genetics • Original Paper
  • Published:
Journal of Applied Genetics Aims and scope Submit manuscript

Abstract

Escherichia coli sequence type 131 (ST131) is a multidrug-resistant strain with the global dissemination. Biofilm formation-related factors include the most important virulence factors in extra-intestinal pathogenic E. coli (ExPEC) ST131 strains causing infections with treatment-limited subjects. This study aims to investigate the biofilm formation ability and its correlation with the presence of fimH, afa, and kpsMSTII genes in clinical isolates of ExPEC ST131. In this regard, the prevalence and characteristics of these strains collected and evaluated. The results revealed strong, moderate, and weak attachment abilities related to biofilm formation attributes in 45%, 20%, and 35% of strains, respectively. In the meantime, the frequency of the fimH, afa, and kpsMSTII genes among the isolates was observed as follows: fimH positive: 65%; afa positive: 55%; and kpsMSTII positive: 85%. The results convey a significant different of biofilm formation ability between clinical E. coli ST131 and non-ST131 isolates. Furthermore, while 45% of ST131 isolates produced strong biofilms, only 2% of non-ST131 isolates showed the ability to form strong biofilms. The attending of fimH, afa, and kpsMSTII genes in the majority of ST131 strains demonstrated a key role leading to biofilm formation. These findings suggested the application of fimH, afa, and kpsMSTII gene suppressors for treating biofilm infections caused by drug-resistant ST131 strains.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article. The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Arthur M, Johnson CE, Rubin RH, Arbeit RD, Campanelli C, Kim C et al (1989) Molecular epidemiology of adhesin and hemolysin virulence factors among uropathogenic Escherichia coli. Infect Immun 57:303–313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banerjee R, Johnson JR (2014) A new clone sweeps clean: the enigmatic emergence of Escherichia coli sequence type 131. Antimicrob Agents Chemother 58(9):4997–5004

  • Barrett JF, Hoch JA (1998) Two-component signal transduction as a target for microbial anti-infective therapy. Antimicrob Agents Chemother 42(7):1529–1536

  • Beloin C, Roux A, Ghigo JM (2008) Escherichia coli biofilms. Bacterial Biofilms 249–89

  • Clermont O, Lavollay M, Vimont S, Deschamps C, Forestier C, Branger C et al (2008) The CTX-M-15-producing Escherichia coli diffusing clone belongs to a highly virulent B2 phylogenetic subgroup. J Antimicrob Chemother 61:1024–1028

    Article  CAS  PubMed  Google Scholar 

  • Clermont O, Gordon D, Denamur E (2015) Guide to the various phylogenetic classification schemes for Escherichia coli and the correspondence among schemes. Microbiol (United Kingdom). Microbiology Society 161:980–8

  • Coelho A, Mora A, Mamani R, López C, González-López JJ, Larrosa MN et al (2011) Spread of Escherichia coli O25b:H4-B2-ST131 producing CTX-M-15 and SHV-12 with high virulence gene content in Barcelona (Spain). J Antimicrob Chemother 66:517–526

    Article  CAS  PubMed  Google Scholar 

  • Cristea VC, Gheorghe I, Czobor Barbu I, Popa LI, Ispas B, Grigore GA, . . . Velican A (2019) Snapshot of phylogenetic groups, virulence, and resistance markers in Escherichia coli uropathogenic strains isolated from outpatients with urinary tract infections in Bucharest, Romania. Biomed Res Int 2019:5712371. https://doi.org/10.1155/2019/5712371

  • Croxall G, Hale J, Weston V, Manning G, Cheetham P, Achtman M et al (2011) Molecular epidemiology of extraintestinal pathogenic Escherichia coli isolates from a regional cohort of elderly patients highlights the prevalence of ST131 strains with increased antimicrobial resistance in both community and hospital care settings. J Antimicrob Chemother 66:2501–2508

    Article  CAS  PubMed  Google Scholar 

  • Da Silva LC, De Mello Santos AC, Silva RM (2017) Uropathogenic Escherichia coli pathogenicity islands and other ExPEC virulence genes may contribute to the genome variability of enteroinvasive E. coli. BMC Microbiol. BioMed Central Ltd. 17

  • Danese PN, Pratt LA, Kolter R (2000) Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J Bacteriol 182:3593–3596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doumith M, Day MJ, Hope R, Wain J, Woodford N (2012) Improved multiplex PCR strategy for rapid assignment of the four major Escherichia coli phylogenetic groups. J Clin Microbiol 50:3108–3110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doumith M, Day M, Ciesielczuk H, Hope R, Underwood A, Reynolds R, et al (2015) Rapid identification of major Escherichia coli sequence types causing urinary tract and bloodstream infections. J Clin Microbiol. American Society for Microbiology 53:160–6

  • Foxman B (2010) The epidemiology of urinary tract infection. Nat Rev Urol 7:653–660

    Article  PubMed  Google Scholar 

  • Gonzalez Moreno C, Torres Luque A, Oliszewski R, Rosa RJ, Otero MC (2020) Characterization of native Escherichia coli populations from bovine vagina of healthy heifers and cows with postpartum uterine disease. PLoS One 15(6):e0228294

  • Griebling TL (2005) Urologic diseases in America project: Trends in resource use for urinary tract infections in women. J Urol. Lippincott Williams and Wilkins 173:1281–7

  • Hojati Z, Zamanzad B, Hashemzadeh M, Molaie R, Gholipour A (2015) The FimH gene in uropathogenic Escherichia coli strains isolated from patients with urinary tract infection. Jundishapur Journal of Microbiology 8(2):S1

  • Hussain A, Ewers C, Nandanwar N, Guenther S, Jadhav S, Wieler LH et al (2012) Multiresistant uropathogenic Escherichia coli from a region in India where urinary tract infections are endemic: genotypic and phenotypic characteristics of sequence type 131 isolates of the CTX-M-15 extended-spectrum-β- lactamase-producing lineage. Antimicrob Agents Chemother 56:6358–6365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain A, Ranjan A, Nanwar N, Babbar A, Jadhav S, Ahmed N (2014) Genotypic and phenotypic profiles of escherichia coli isolates belonging to clinical sequence type 131 (ST131), clinical non-ST131, and fecal non-ST131 lineages from India. Antimicrob Agents Chemother. American Society for Microbiology 58:7240–9

  • Ito A, Taniuchi A, May T, Kawata K, Okabe S (2009) Increased antibiotic resistance of Escherichia coli in mature biofilms. Appl Environ Microbiol 75:4093–4100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson DW, Suzuki K, Oakford L, Simecka JW, Hart ME, Romeo T (2002) Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J Bacteriol 184:290–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson JR (1991) Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev 4:80–128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson JR, Johnston B, Clabots C, Kuskowski MA, Castanheira M (2010) Escherichia coli sequence type ST131 as the major cause of serious multidrug-resistant E. coli infections in the United States. Clin Infect Dis 51:286–94

    Article  PubMed  Google Scholar 

  • Jorgensen I, Seed PC (2012) How to make it in the urinary tract: a tutorial by Escherichia coli. PLoS Pathog 8

  • Kakkanat A, Totsika M, Schaale K, Duell BL, Lo AW, Phan MD, . . . Ulett GC (2015) The role of H4 flagella in Escherichia coli ST131 virulence. Sci Rep 5(1):16149

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

  • Khairy RM, Mohamed ES, Ghany HMA, Abdelrahim SS (2019) Phylogenic classification and virulence genes profiles of uropathogenic E. coli and diarrhegenic E. coli strains isolated from community acquired infections. PLoS One 14(9):e0222441

  • Kudinha T, Johnson JR, Andrew SD, Kong F, Anderson P, Gilbert GL (2013) Escherichia coli sequence type 131 as a prominent cause of antibiotic resistance among urinary Escherichia coli isolates from reproductive-age women. J Clin Microbiol 51:3270–3276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Bouguénec C, Lalioui L, Du Merle L, Jouve M, Courcoux P, Bouzari S et al (2001) Characterization of AfaE adhesins produced by extraintestinal and intestinal human escherichia coli isolates: PCR assays for detection of afa adhesins that do or do not recognize Dr blood group antigens. J Clin Microbiol 39:1738–1745

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee MY, Choi HJ, Choi JY, Song M, Song Y, Kim SW et al (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 

  • Mittal S, Sharma M, Chaudhary U (2015) Biofilm and multidrug resistance in uropathogenic Escherichia coli. Pathog Glob Health. Maney Publishing 109:26–9

  • Naseer U, Haldorsen B, Tofteland S, Hegstad K, Scheutz F, Simonsen GS et al (2009) Molecular characterization of CTX-M-15-producing clinical isolates of Escherichia coli reveals the spread of multidrug-resistant ST131 (O25:H4) and ST964 (O102:H6) strains in Norway. APMIS 117:526–536

    Article  CAS  PubMed  Google Scholar 

  • Naves P, del Prado G, Huelves L, Gracia M, Ruiz V, Blanco J et al (2008) Correlation between virulence factors and in vitro biofilm formation by Escherichia coli strains. Microb Pathog 45:86–91

    Article  CAS  PubMed  Google Scholar 

  • Novais Â, Pires J, Ferreira H, Costa L, Montenegro C, Vuotto C et al (2012) Characterization of globally spread Escherichia coli ST131 isolates (1991 to 2010). Antimicrob Agents Chemother 56:3973–3976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olesen B, Frimodt-Møller J, Leihof RF, Struve C, Johnston B, Hansen DS, et al (2014) Temporal trends in antimicrobial resistance and virulence-associated traits within the Escherichia coli sequence type 131 clonal group and its H30 and H30-Rx Subclones, 1968 to 2012. Antimicrob Agents Chemother. American Society for Microbiology 58:6886–95

  • Petty NK, Zakour NLB, Stanton-Cook M, Skippington E, Totsika M, Forde BM et al (2014) Global dissemination of a multidrug resistant Escherichia coli clone. Proc Natl Acad Sci U S A 111:5694–5699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price LB, Johnson JR, Aziz M, Clabots C, Johnston B, Tchesnokova V, . . . Stegger M (2013) The epidemic of extended-spectrum-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. MBio 4(6):e00377–00313

  • Reisner A, Krogfelt KA, Klein BM, Zechner EL, Molin S (2006) In vitro biofilm formation of commensal and pathogenic Escherichia coli strains: impact of environmental and genetic factors. J Bacteriol 188:3572–3581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarkar S, Vagenas D, Schembri MA, Totsika M (2016) Biofilm formation by multidrug resistant Escherichia coli ST131 is dependent on type 1 fimbriae and assay conditions. Pathog Dis 74(3)

  • Sarowska J, Futoma-Koloch B, Jama-Kmiecik A, Frej-Madrzak M, Ksiazczyk M, Bugla-Ploskonska G, et al (2019) Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: recent reports. Gut Pathog. BioMed Central Ltd.

  • Schaeffer EM (2014) Re: A FimH inhibitor prevents acute bladder infection and treats chronic cystitis caused by multidrug-resistant uropathogenic escherichia coli ST131: Editorial comment. J Urol 192:276

    Article  CAS  PubMed  Google Scholar 

  • Schissler JR, Hillier A, Daniels JB, Cole LK, Gebreyes WA (2009) Evaluation of clinical laboratory standards institute interpretive criteria for methicillin-resistant Staphylococcus pseudintermedius isolated from dogs. J Vet Diagnostic Investig 21:684–8

    Article  Google Scholar 

  • Sharma G, Sharma S, Sharma P, Chandola D, Dang S, Gupta S et al (2016) Escherichia coli biofilm: development and therapeutic strategies. J Appl Microbiol Blackwell Publishing Ltd 121:309–319

    Article  CAS  Google Scholar 

  • Svanborg Edén C, Jodal U, Hanson LA, Lindberg U, Sohl ÅA (1976) Variable Adherence to normal human urinary-tract epithelial cells of Escherichia coli strains associated with various forms of urinary-tract infection. Lancet 308:490–492

    Article  Google Scholar 

  • Tajbakhsh E, Ahmadi P, Abedpour-Dehkordi E, Arbab-Soleimani N, Khamesipour F (2016) Biofilm formation, antimicrobial susceptibility, serogroups and virulence genes of uropathogenic E. coli isolated from clinical samples in Iran. Antimicrob Resist Infect Control 5(1):1–8

  • Totsika M, Beatson SA, Sarkar S, Phan MD, Petty NK, Bachmann N, et al (2011) Insights into a multidrug resistant Escherichia coli pathogen of the globally disseminated ST131 lineage: Genome analysis and virulence mechanisms. PLoS One 6

  • Weinstein MP, Lewis JS (2020) The clinical and laboratory standards institute subcommittee on antimicrobial susceptibility testing: background, organization, functions, and processes. J Clin Microbiol 58(3):e01864–01819

  • Xie J, Foxman B, Zhang L, Marrs CF (2006) Molecular epidemiologic identification of Escherichia coli genes that are potentially involved in movement of the organism from the intestinal tract to the vagina and bladder. J Clin Microbiol 44:2434–2441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank Tehran University of Medical Sciences.

Author information

Authors and Affiliations

Authors

Contributions

YE and MTE conceived and designed the experiments. RFP, NM, and MN performed the experiments. AA, JH, and MAH analyzed the data. YE and MAH wrote the manuscript. All authors reviewed and approved the manuscript.

Corresponding author

Correspondence to Yousef Erfani.

Ethics declarations

Ethics approval and consent to participate

The study protocol was approved by the Ethics Committee of Tehran University of Medical Sciences (IR.TUMS.SPH.REC.1398.057). Consent to participate is not applicable for this study because the isolates included in the study were obtained from existing clinical collections routinely assembled as part of laboratory practices of tertiary hospitals. The clinical strains of E. coli were obtained by permission of the head of hospital laboratory.

Consent for publication

This is not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Communicated by Agnieszka Szalewska-Palasz

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The design of the study and collection, analysis, and interpretation of data, and writing of the manuscript was supported by Tehran University of Medical Sciences.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ebrahimi, M.T., Hedayati, M.A., Pirlar, R.F. et al. Investigation of the biofilm formation in extra-intestinal pathogenic Escherichia coli ST131 strains and its correlation with the presence of fimH, afa, and kpsMSTII genes. J Appl Genetics 64, 367–373 (2023). https://doi.org/10.1007/s13353-023-00757-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13353-023-00757-9

Keywords

Navigation