Keywords
Curli Fimbriae
Hemolytic Uremic Syndrome
Shiga Toxin-Producing Escherichia Coli
Sources
How to Cite
Abstract
Shiga toxin-producing Escherichia coli (STEC) O157:H7 is the most prevalent serotype associated with severe diseases worldwide. Biofilms by STEC O157:H7 constitute a high risk to public health and the food industry since they allow cross-contamination of surfaces and the consequent transmission to humans. This study aimed to detect the presence of adhesins genotypically and determine the ability to form biofilm and the curli expression in a collection of 30 O157:H7 strains from healthy cattle and human cases. The efa1, iha, fimCD, ehaA, lpfA1-3, and lpfA2-2 genes were detected in all strains; cah was frequently detected in strains isolated from humans (16/20), and agn43 was the least prevalent gene (3/30). All strains could form a biofilm, although those isolated from cattle were the most biofilm-formers. The curli-negative phenotype was the most prevalent phenotype observed at 37 °C and room temperature. The association between curli production and biofilm formation could not be determined, but the highest proportion of curli-positive strains at room temperature were strong biofilm-formers. These results highlight the possibility of the persistence of STEC O157:H7 in environmental conditions and food processing facilities, increasing the risk of contamination or infection.
References
Oderiz S, Leotta GA, Galli L. Detección y caracterización de Escherichia coli productor de toxina Shiga en niños atendidos en un hospital pediátrico interzonal de la ciudad de La Plata. Rev Argent Microbiol. 2018;50(4): 341-350. https://doi.org/10.1016/j.ram.2017.08.008
Freedman SB, Xie J, Neufeld MS, Hamilton WL, Hartling L, Tarr PI. Shiga toxin-producing Escherichia coli infection, antibiotics, and risk of developing hemolytic uremic syndrome: a meta-analysis. Clin Infect Dis. 2016; 62(10): 1251-1258. https://doi.org/10.1093/cid/ciw099
Kohansal M, Asad AG. Molecular analysis of Shiga toxin-producing Escherichia coli O157:H7 and non-O157 strains isolated from calves. Onderstepoort J Vet Res. 2018; 85(1):e1-e7. https://doi.org/10.4102/ojvr.v85i1.1621
Tayh G, Boubaker SM, Khedher RB, Jbeli M, Chehida FB, Mamlouk A, et al. Prevalence, virulence genes and antimicrobial profiles of Escherichia coli O157:H7 isolated from healthy cattle. Research Square (preprint). 2021. https://doi.org/10.21203/rs.3.rs-580804/v1
Luna S, Krishnasamy V, Saw L, Smith L, Wagner J, Weigand J, et al. Outbreak of E. coli O157:H7 infections associated with exposure to animal manure in a rural community -Arizona and Utah, June-July 2017. MMWR. 2018; 67(23): 659-662. http://dx.doi.org/10.15585/mmwr.mm6723a2
Ruiz MJ, Padola NL, Leotta G, Colello R, Passucci J, Rodríguez E, et al. Calidad microbiológica de la carne picada y detección de patógenos en muestras ambientales de carnicerías de la ciudad de Tandil, provincia de Buenos Aires, Argentina. Rev Argent Microbiol. (In press). 2021. https://doi.org/10.1016/j.ram.2021.04.003
Tanaro JD, Piaggio MC, Gasparovic AM, Badaracco VA, Tesouro R, Kesselman D, et al. Escherichia coli O157:H7 productor de toxina Shiga aisladas de muestras de agua relacionadas a establecimientos pecuarios de engorde a corral. Ciencia, Docencia y Tecnología Suplemento. 2016; 6 (6).
Zotta CM, Chinen I, Lavayén S, Cepeda M, Deza N, Morvay L, et al. Portación de Escherichia coli en convivientes de casos de síndrome urémico hemolítico. Salud (i) Ciencia. 2015; 21: 136-141.
Scheutz F, Teel LD, Beutin L, Pierard D, Buvens G, Karch H, et al. Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J Clin Microbiol. 2012 ; 50(9) : 2951-63. https://doi.org/10.1128/jcm.00860-12
Szalo IM, Goffaux F, Pirson V, Piérard D, Ball H, Mainil J. Presence in bovine enteropathogenic (EPEC) and enterohaemorrhagic (EHEC) Escherichia coli of genes encoding for putative adhesins of human EHEC strains. Res Microbiol. 2002 Dec; 153(10):653-8. https://doi.org/10.1016/s0923-2508(02)01379-7
Torres AG, Blanco M, Valenzuela P, Slater TM, Patel SD, Dahbi G, et al. Genes related to long polar fimbriae of pathogenic Escherichia coli strains as reliable markers to identify virulent isolates. J Clin Microbiol. 2009; 47(8): 2442-51. https://doi.org/10.1128/jcm.00566-09
Montero D, Orellana P, Gutiérrez D, Araya D, Salazar JC, Prado V, et al. Immunoproteomic analysis to identify Shiga toxin-producing Escherichia coli outer membrane proteins expressed during human infection. Infect Immun. 2014; 82: 476777. https://doi.org/10.1128/iai.02030-14
Wu Y, Hinenoya A, Taguchi T, Nagita A, Shima K, Tsukamoto T, et al. Distribution of virulence genes related to adhesins and toxins in Shiga toxin-producing Escherichia coli strains isolated from healthy cattle and diarrheal patients in Japan. J Vet Med Sci. 2010; 72: 589-597. https://doi.org/10.1292/jvms.09-0557
Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002; 15(2): 167-93. https://doi.org/10.1128/cmr.15.2.167-193.2002
Bae YM, Baek SY, Lee SY. Resistance of pathogenic bacteria on the surface of stainless steel depending on attachment form and efficacy of chemical sanitizers. Int J Food Microbiol. 2012; 153(3): 465-473. https://doi.org/10.1016/j.ijfoodmicro.2011.12.017
Di Domenico EG, Farulla I, Prignano G, Gallo MT, Vespaziani M, Cavallo I, et al. Biofilm is a major virulence determinant in bacterial colonization of chronic skin ulcers independently from the multidrug resistant phenotype. Int J Mol Sci. 2017; 18(5): 1077. https://doi.org/10.3390/ijms18051077
Nesse LL, Sekse C, Berg K, Johannesen KC, Solheim H, Vestby LK, et al. Potentially pathogenic Escherichia coli can form a biofilm under conditions relevant to the food production chain. Appl Environ Microbiol. 2014 Apr; 80(7): 2042-9. https://doi.org/10.1128/aem.03331-13
Padola NL, Sanz ME, Blanco JE, Blanco M, Blanco J, Etcheverría AI, et al. Serotypes and virulence genes of bovine Shigatoxigenic Escherichia coli (STEC) isolated from a feedlot in Argentina. Vet Microbiol. 2004; 100(1-2): 3-9. https://doi.org/10.1016/s0378-1135(03)00127-5
Leotta GA, Chinen I, Epszteyn S, Miliwebsky E, Melamed I, Motter M, et al. Validación de una técnica de PCR múltiple para la detección de Escherichia coli productor de toxina Shiga. Rev Argent Microbiol. 2005; 37(1):1-10.
Vidal M, Escobar P, Prado V, Hormazábal JC, Vidal R. Distribution of putative adhesins in Shiga toxin-producing Escherichia coli (STEC) strains isolated from different sources in Chile. Epidemiol Infect. 2007; 135(4): 688-694. https://doi.org/10.1017/s0950268806007102
Prado V, Cavagnaro SM. Síndrome hemolítico urémico asociado a infección intestinal por Escherichia coli productora de Shigatoxina (STEC) en pacientes chilenos: aspectos clínicos y epidemiológicos. Rev Chilena Infectol. 2008; 25(6): 435-444. https://doi.org/10.4067/S0716-10182008000600003
Fernández D, Rodriguez EM, Arroyo GH, Padola NL, Parma AE (2009). Seasonal variation of Shiga toxin-encoding genes (stx) and detection of E. coli O157 in dairy cattle from Argentina. J Appl Microbiol. 106 (4): 1260-7. https://doi.org/10.1111/j.1365-2672.2008.04088.x
Fernández D, Sanz ME, Parma AE, Padola NL. Characterization of Shiga toxin-producing Escherichia coli isolated from newborn, milk-fed, and growing calves in Argentina. J Dairy Sci. 2012; 95: 5340-5343. https://doi.org/10.3168/jds.2011-5140
Nicholls L, Grant TH, Robins-Browne RM. Identification of a novel genetic locus that is required for in vitro adhesion of a clinical isolate of enterohaemorrhagic Escherichia coli to epithelial cells. Mol Microbiol. 2000; 35(2): 275-288. https://doi.org/10.1046/j.1365-2958.2000.01690.x
Cookson AL, Cooley WA, Woodward MJ. The role of type 1 and curli fimbriae of Shiga toxin-producing Escherichia coli in adherence in abiotic surfaces. Int J Med Microbiol. 2002; 292(3-4): 195-205. https://doi.org/10.1078/1438-4221-00203
Montero DA, Velasco J, Del Canto F, Puente JL, Padola NL, Rasko DA. Locus of Adhesion and Autoaggregation (LAA), a pathogenicity island presents in emerging Shiga Toxin-producing Escherichia coli strains. Sci Rep. 2017; 7(1):7011. https://doi.org/10.1038/s41598-017-06999-y
Cáceres ME, Etcheverría AI, Padola NL. Effects of the culture medium and the methodology applied on the biofilm formation of 2 diarrheagenic Escherichia coli strains. Rev Argent Microbiol. 2019; 51(3): 208-2013. https://doi.org/10.1016/j.ram.2018.04.007
Gómez J, Gómez-Lus ML, Bas P, Ramos C, Caini F, Maestre JR, et al. [Biofilm score: is it a differential element within gram negative bacilli?] Rev Esp Quimioter. 2013; 26: 97-102.
Bokranz W, Wang X, Tschäpe H, Römling U. Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. J Med Microbiol. 2005; 54(12): 1171-1182. https://doi.org/10.1099/jmm.0.46064-0
Vogeleer P, Tremblay YD, Mafu AA, Jacques M, Harel J. Life on the outside: role of biofilms in environmental persistence of Shiga-toxin producing Escherichia coli. Front Microbiol. 2014; 5:317. https://doi.org/10.3389/fmicb.2014.00317
Cáceres ME, Etcheverría AI, Fernández D, Rodríguez EM, Padola NL. Variation in the distribution of putative virulence and colonization factors in Shiga toxin-producing Escherichia coli isolated from different categories of cattle. Front Cell Infect Microbiol. 2017; 7:147. https://doi.org/10.3389/fcimb.2017.00147
Biscola FT, Abe CM, Guth BEC. Determination of adhesin gene sequences in and biofilm formation by O157 and non-O157 Shiga toxin-producing Escherichia coli strains isolated from different sources. Appl Environ Microbiol. 2011; 77(7): 2201-2208. https://doi.org/10.1128/aem.01920-10
Torres AG, Perna NT, Burland V, Ruknudin A, Blattner FR, Kaper JB. Characterization of Cah, a calcium-binding and heat-extractable autotransporter protein of enterohaemorrhagic Escherichia coli. Mol Microbiol. 2002; 45(4):951-66. https://doi.org/10.1046/j.1365-2958.2002.03094.x
Schiebel J, Böhm A, Nitschke J, Burdukiewicz M, Weinreich J, Ali A, et al. Genotypic and phenotypic characteristics associated with biofilm formation by human clinical Escherichia coli isolates of different pathotypes. Appl Environ Microbiol 2017; 83(24):e01660-17. https://doi.org/10.1128/aem.01660-17
Picozzi C, Antoniani D, Vigentini I, Foschino R, Kneifel W. Genotypic characterization and biofilm formation of Shiga toxin-producing Escherichia coli. FEMS Microbiol Lett. 2017; 364(2). https://doi.org/10.1093/femsle/fnw291
Vogeleer P, Tremblay YD, Jubelin G, Jacques M, Harel J. Biofilm-forming abilities of Shiga toxin-producing Escherichia coli isolates associated with human infections. Appl Environ Microbiol. 2015:82(5):1448-1458. https://doi.org/10.1128/aem.02983-15
Segura A, Auffret P, Bibbal D, Bertoni M, Durand A, Jubelin G, et al. Factors involved in the persistence of a Shiga toxin-producing Escherichia coli O157:H7 strain in bovine feces and gastro-intestinal content. Front microbiol. 2018; 9:375. https://doi.org/10.3389/fmicb.2018.00375
Blankenship HM, Carbonell S, Mosci R, McWilliams K, Pietrzen K, Benko S, et al. Genetic and phenotypic factors associated with persistent Shiga toxin-producing Escherichia coli shedding in beef cattle. Appl Environ Microbiol. 2020; 86 (20):e01292-20. https://doi.org/10.1128/AEM.01292-20
Gualdi L, Tagliabue L, Bertagnoli S, Ierano T, De Castro C, Landini P. Cellulose modulates biofilm formation by counteracting curli-mediated colonization of solid surfaces in Escherichia coli. Microbiology. 2008; 154: 2017-2024. https://doi.org/10.1099/mic.0.2008/018093-0
Pawar DM, Rossman ML, Chen J. Role of curli fimbriae in mediating the cells of enterohaemorrhagic Escherichia coli to attach to abiotic surfaces. J Appl Microbiol. 2005; 99(2):418-25. https://doi.org/10.1111/j.1365-2672.2005.02499.x
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