2,250
Views
4
CrossRef citations to date
0
Altmetric
Research Paper

The aggregate-forming pili (AFP) mediates the aggregative adherence of a hybrid-pathogenic Escherichia coli (UPEC/EAEC) isolated from a urinary tract infection

ORCID Icon, , ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 3073-3093 | Received 28 Jul 2021, Accepted 11 Nov 2021, Published online: 20 Dec 2021

References

  • Croxen MA, Law RJ, Scholz R, et al. Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev. 2013;26(4):822–880.
  • Gomes TAT, Elias WP, Scaletsky IC, et al. Diarrheagenic Escherichia coli. Braz J Microbiol. 2016;47(Suppl 1):3–30.
  • Smith JL, Fratamico PM, Gunther NW. Extraintestinal pathogenic Escherichia coli. Foodborne Pathog Dis. 2007;4(2):134–163.
  • Boxall MD, Day MR, Greig DR, et al. Antimicrobial resistance profiles of diarrhoeagenic Escherichia coli isolated from travelers returning to the UK, 2015–2017. J Med Microbiol. 2020;69(7):932–943.
  • Hebbelstrup Jensen B, Olsen KE, Struve C, et al. Epidemiology and clinical manifestations of enteroaggregative Escherichia coli. Clin Microbiol Rev. 2014;27(3):614–630.
  • Huang DB, Nataro JP, DuPont HL, et al. Enteroaggregative Escherichia coli is a cause of acute diarrheal illness: a meta-analysis. Clin Infect Dis. 2006;43(5):556–563.
  • Jiang ZD, DuPont HL. Etiology of travellers’ diarrhea. J Travel Med. 2017;24(suppl_1):S13–S16.
  • Nataro JP, Kaper JB, Robins-Browne R, et al. Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Pediatr Infect Dis J. 1987;6(9):829–831.
  • Navarro-Garcia F, Elias WP. A utotransporters and virulence of enteroaggregative E. coli. Gut Microbes. 2011;2(1):13–24.
  • Nataro JP, Deng Y, Cookson S, et al. Heterogeneity of enteroaggregative Escherichia coli virulence demonstrated in volunteers. J Infect Dis. 1995;171(2):465–468.
  • Bernier C, Gounon P, Le Bouguénec C. Identification of an aggregative adhesion fimbria (AAF) type III-encoding operon in enteroaggregative Escherichia coli as a sensitive probe for detecting the AAF-encoding operon family. Infect Immun. 2002;70(8):4302–4311.
  • Boisen N, Struve C, Scheutz F, et al. New adhesin of enteroaggregative Escherichia coli related to the Afa/Dr/AAF family. Infect Immun. 2008;76(7):3281–3292.
  • Czeczulin JR, Balepur S, Hicks S, et al. Aggregative adherence fimbria II, a second fimbrial antigen mediating aggregative adherence in enteroaggregative Escherichia coli. Infect Immun. 1997;65(10):4135–4145.
  • Dudley EG, Thomson NR, Parkhill J, et al. Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity Island in enteroaggregative Escherichia coli. Mol Microbiol. 2006;61(5):1267–1282.
  • Eslava C, Navarro-García F, Czeczulin JR, et al. Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect Immun. 1998;66(7):3155–3163.
  • Henderson IR, Czeczulin J, Eslava C, et al. Characterization of pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli. Infect Immun. 1999;67(11):5587–5596.
  • Jønsson R, Struve C, Boisen N, et al. Novel aggregative adherence fimbria variant of enteroaggregative Escherichia coli. Infect Immun. 2015;83(4):1396–1405.
  • Nataro JP, Deng Y, Maneval DR, et al. Aggregative adherence fimbriae I of enteroaggregative Escherichia coli mediate adherence to HEp-2 cells and hemagglutination of human erythrocytes. Infect Immun. 1992;60(6):2297–2304.
  • Sheikh J, Czeczulin JR, Harrington S, et al. A novel dispersin protein in enteroaggregative Escherichia coli. J Clin Invest. 2002;110(9):1329–1337.
  • Morin N, Santiago AE, Ernst RK, et al. Characterization of the aggR regulon in enteroaggregative Escherichia coli. Infect Immun. 2013;81(1):122–132.
  • Nataro JP, Yikang D, Yingkang D, et al. AggR, a transcriptional activator of aggregative adherence fimbria I expression in enteroaggregative Escherichia coli. J Bacteriol. 1994;176(15):4691–4699.
  • Terlizzi ME, Gribaudo G, Maffei ME. Uropathogenic Escherichia coli (UPEC) infections: virulence factors, bladder responses, antibiotic, and non-antibiotic antimicrobial strategies. Front Microbiol. 2017;8:1566.
  • Flores-Mireles AL, Walker JN, Caparon M, et al. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol. 2015;13(5):269–284.
  • Foxman B. The epidemiology of urinary tract infection. Nat Rev Urol. 2010;7(12):653–660.
  • Johnson JR, Stell AL. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis. 2000;181(1):261–272.
  • Khairy RM, Mohamed ES, Abdel-Ghany HM, et al. Phylogenic classification and virulence genes profiles of uropathogenic E. coli and diarrheagenic E. coli strains isolated from community acquired infections. PLoS One. 2019;14(9):e0222441.
  • Spurbeck RR, Dinh PC Jr, Walk ST, et al. Escherichia coli isolates that carry vat, fyuA, chuA, and yfcV efficiently colonize the urinary tract. Infect Immun. 2012;80(12):4115–4122.
  • Boll EJ, Overballe-Petersen S, Hasman H, et al. Emergence of enteroaggregative Escherichia coli within the ST131 lineage as a cause of extraintestinal infections. mBio. 2020;11(3):e00353–20.
  • Freire CA, Santos ACM, Pignatari AC, et al. Serine protease autotransporters of Enterobacteriaceae (SPATEs) are largely distributed among Escherichia coli isolated from the bloodstream. Braz J Microbiol. 2020;51(2):447–454.
  • Herzog K, Engeler Dusel J, Hugentobler M, et al. Diarrheagenic enteroaggregative Escherichia coli causing urinary tract infection and bacteremia leading to sepsis. Infection. 2014;42(2):441–444.
  • Lara FB, Nery DR, de Oliveira PM, et al. Virulence markers and phylogenetic analysis of Escherichia coli strains with hybrid EAEC/UPEC genotypes recovered from sporadic cases of extraintestinal infections. Front Microbiol. 2017;8:146.
  • Mandomando I, Vubil D, Boisen N, et al. Escherichia coli ST131 clones harbouring aggR and AAF/V fimbriae causing bacteremia in Mozambican children: emergence of new variant of fimH27 subclone. PLoS Negl Trop Dis. 2020;14(5):e0008274.
  • Nascimento JAS, Santos FF, Valiatti TB, et al. Frequency and diversity of hybrid Escherichia coli strains isolated from urinary tract infections. Microorganisms. 2021;9(4):693.
  • Nazemi A, Mirinargasi M, Merikhi N, et al. Distribution of pathogenic genes aatA, aap, aggR, among uropathogenic Escherichia coli (UPEC) and their linkage with stbA gene. Indian J Microbiol. 2011;51(3):355–358.
  • Park HK, Jung YJ, Chae HC, et al. Comparison of Escherichia coli uropathogenic genes (kps, usp and ireA) and enteroaggregative genes (aggR and aap) via multiplex polymerase chain reaction from suprapubic urine specimens of young children with fever. Scand J Urol Nephrol. 2009;43(1):51–57.
  • Toval F, Köhler CD, Vogel U, et al. Characterization of Escherichia coli isolates from hospital inpatients or outpatients with urinary tract infection. J Clin Microbiol. 2014;52(2):407–418.
  • Flament-Simon SC, Nicolas-Chanoine MH, García V, et al. Clonal structure, virulence factor-encoding genes and antibiotic resistance of Escherichia coli, causing urinary tract infections and other extraintestinal infections in humans in Spain and France during 2016. Antibiotics (Basel). 2020;9(4):161.
  • Boll EJ, Struve C, Boisen N, et al. Role of enteroaggregative Escherichia coli virulence factors in uropathogenesis. Infect Immun. 2013;81(4):1164–1171.
  • Olesen B, Scheutz F, Andersen RL, et al. Enteroaggregative Escherichia coli O78:H10, the cause of an outbreak of urinary tract infection. J Clin Microbiol. 2012;50(11):3703–3711.
  • Abe CM, Salvador FA, Falsetti IN, et al. Uropathogenic Escherichia coli (UPEC) strains may carry virulence properties of diarrhoeagenic E. coli. FEMS Immunol Med Microbiol. 2008;52(3):397–406.
  • Nunes KO, Santos ACP, Bando SY, et al. Enteroaggregative Escherichia coli with uropathogenic characteristics are present in feces of diarrheic and healthy children. Pathog Dis. 2017;75(8). DOI:10.1093/femspd/ftx106
  • Gomes TAT, Abe CM, Marques LR. Detection of HeLa cell-detaching activity and alpha-hemolysin production in enteroaggregative Escherichia coli strains isolated from feces of Brazilian children. J Clin Microbiol. 1995;33(12):3364.
  • Santos ACM, Santos FF, Silva RM, et al. Diversity of hybrid- and hetero-pathogenic Escherichia coli and their potential implication in more severe diseases. Front Cell Infect Microbiol. 2020a;10:339.
  • Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing. 27th ed. Tertel ML, Christopher JP, and Martin L , et al. eds. Wayne PA: Clinical and Laboratory Standards Institute; 2017.
  • Cravioto A, Gross RJ, Scotland SM, et al. An adhesive factor found in strains of Escherichia coli belonging to the traditional infantile enteropathogenic serotypes. Curr Microbiol. 1979;3(2):95–99.
  • Munhoz DD, Nara JM, Freitas NC, et al. Distribution of major pilin subunit genes among atypical enteropathogenic Escherichia coli and influence of growth media on expression of the ecp operon. Front Microbiol. 2018;9:942.
  • Sheikh J, Hicks S, Dall’Agnol M, et al. Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli. Mol Microbiol. 2001;41(5):983–997.
  • Culler HF, Mota CM, Abe CM, et al. Atypical enteropathogenic Escherichia coli strains form biofilm on abiotic surfaces regardless of their adherence pattern on cultured epithelial cells. Biomed Res Int. 2014;2014:845147.
  • Stepanovic S, Vukovic D, Dakic I, et al. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods. 2000;40(2):175–179.
  • Castonguay MH, van der Schaaf S, Koester W, et al. Biofilm formation by Escherichia coli is stimulated by synergistic interactions and co-adhesion mechanisms with adherence-proficient bacteria. Res Microbiol. 2006;157(5):471–478.
  • Römling U, Bokranz W, Rabsch W, et al. Occurrence and regulation of the multicellular morphotype in Salmonella serovars important in human disease. Int J Med Microbiol. 2003;293(4):273–285.
  • Pugsley AP, Oudega B. Methods for studying colicins and their plasmids. In: Hardy KG, editor. Plasmids: a practical approach. Oxford: IRL Press; 1987. p. 105–161.
  • Ruiz RC, Melo KC, Rossato SS, et al. Atypical enteropathogenic Escherichia coli secretes plasmid encoded toxin. Biomed Res Int. 2014;2014:896235.
  • Birnboim HC, Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979;7(6):1513–1523.
  • Moran RA, Anantham S, Hall RM. An improved plasmid size standard, 39R861. Plasmid. 2019;102:6–9.
  • Lima MP, Yamamoto D, Santos ACM, et al. Phenotypic characterization and virulence-related properties of Escherichia albertii strains isolated from children with diarrhea in Brazil. Pathog Dis. 2019;77(2):ftz014.
  • Wick RR, Judd LM, Gorrie CL, et al. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol. 2017;13(6):e1005595.
  • Gurevich A, Saveliev V, Vyahhi N, et al. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29(8):1072–1075.
  • Carver T, Thomson N, Bleasby A, et al. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics. 2009;25(1):119–120.
  • Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–2069.
  • Beghain J, Bridier-Nahmias A, Le Nagard H, et al. Clermont Typing: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microb Genom. 2018;4(7):e000192.
  • Larsen MV, Cosentino S, Rasmussen S, et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol. 2012;50(4):1355–1361.
  • Carattoli A, Zankari E, García-Fernández A, et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58(7):3895–3903.
  • Zankari E, Hasman H, Cosentino S, et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67(11):2640–2644.
  • Joensen KG, Tetzschner AM, Iguchi A, et al. Rapid and easy in silico serotyping of Escherichia coli isolates by use of whole-genome sequencing data. J Clin Microbiol. 2015;53(8):2410–2426.
  • Croucher NJ, Page AJ, Connor TR, et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2015;43(3):e15.
  • Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–1313.
  • Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47(W1):W256–W259.
  • Leimbach A. ecoli_VF_collection: v0.1. Zenodo. 2016b. DOI:10.5281/zenodo.56686
  • Leimbach A. bac-genomics-scripts: Bovine E. coli mastitis comparative genomics edition. Zenodo. 2016a. DOI:10.5281/zenodo.215824
  • Penfold RJ, Pemberton JM. An improved suicide vector for construction of chromosomal insertion mutations in bacteria. Gene. 1992;118(1):145–146.
  • Simon R, Priefer U, Pühler AA. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat Biotechnol. 1983;1(9):784–791.
  • Elias WP Jr, Czeczulin JR, Henderson IR, et al. Organization of biogenesis genes for aggregative adherence fimbria II defines a virulence gene cluster in enteroaggregative Escherichia coli. J Bacteriol. 1999;181(6):1779–1785.
  • Chang AC, Cohen SN. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol. 1978;134(3):1141–1156.
  • Evans DG, Silver RP, Evans DJ Jr, et al. Plasmid-controlled colonization factor associated with virulence in Escherichia coli enterotoxigenic for humans. Infect Immun. 1975;12(3):656–667.
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680–685.
  • Johnson JR, Kuskowski MA, Owens K, et al. Phylogenetic origin and virulence genotype in relation to resistance to fluoroquinolones and/or extended-spectrum cephalosporins and cephamycins among Escherichia coli isolates from animals and humans. J Infect Dis. 2003;188(5):759–768.
  • Lang C, Fruth A, Holland G, et al. Novel type of pilus associated with a Shiga-toxigenic E. coli hybrid pathovar conveys aggregative adherence and bacterial virulence. Emerg Microbes Infect. 2018;7(1):203.
  • Chaudhuri RR, Sebaihia M, Hobman JL, et al. Complete genome sequence and comparative metabolic profiling of the prototypical enteroaggregative Escherichia coli strain 042. PLoS One. 2010;5(1):e8801.
  • Dias RCB, Tanabe RHS, Vieira MA, et al. Analysis of the virulence profile and phenotypic features of typical and atypical enteroaggregative Escherichia coli (EAEC) isolated from diarrheal patients in Brazil. Front Cell Infect Microbiol. 2020;10:144.
  • Santos ACM, Silva RM, Valiatti TB, et al. Virulence potential of a multidrug-resistant Escherichia coli strain belonging to the emerging clonal group ST101-B1 isolated from bloodstream infection. Microorganisms. 2020b;8(6):827.
  • Santos AC, Zidko AC, Pignatari AC, et al. Assessing the diversity of the virulence potential of Escherichia coli isolated from bacteremia in São Paulo, Brazil. Braz J Med Biol Res. 2013;46(11):968–973.
  • Binns MM, Mayden J, Levine RP. Further characterization of complement resistance conferred on Escherichia coli by the plasmid genes traT of R100 and iss of ColV,I-K94. Infect Immun. 1982;35(2):654–659.
  • Biran D, Rosenshine I, Ron EZ. Escherichia coli O-antigen capsule (group 4) is essential for serum resistance. Res Microbiol. 2020;171(2):99–101.
  • Köhler CD, Dobrindt U. What defines extraintestinal pathogenic Escherichia coli? Int J Med Microbiol. 2011;301(8):642–647.
  • Lüthje P, Brauner A. Virulence factors of uropathogenic E. coli and their interaction with the host. Adv Microb Physiol. 2014;65:337–372.
  • Stork C, Kovács B, Rózsai B, et al. Characterization of asymptomatic bacteriuria Escherichia coli isolates in search of alternative strains for efficient bacterial interference against uropathogens. Front Microbiol. 2018;9:214.
  • Smajs D, Micenková L, Smarda J, et al. Bacteriocin synthesis in uropathogenic and commensal Escherichia coli: colicin E1 is a potential virulence factor. BMC Microbiol. 2010;10(1):288.
  • Villaseca JM, Navarro-García F, Mendoza-Hernández G, et al. Pet toxin from enteroaggregative Escherichia coli produces cellular damage associated with fodrin disruption. Infect Immun. 2000;68(10):5920–5927.
  • Ruiz-Perez F, Nataro JP. Bacterial serine proteases secreted by the autotransporter pathway: classification, specificity, and role in virulence. Cell Mol Life Sci. 2014;71(5):745–770.
  • Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol. 2004;2(2):123–140.
  • Girón JA, Ho AS, Schoolnik GK. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science. 1991;254(5032):710–713.