Molecular characterization of Escherichia coli from dishwasher rubber seals

Authors

  • Marjanca Starčič Erjavec
  • Jerneja Ambrožič Avguštin

DOI:

https://doi.org/10.14720/abs.65.1.15942

Keywords:

E. coli, dishwasher, genes, One Health, plasmids, virulence

Abstract

In this study 35 Escherichia coli isolates obtained from sampled dishwashers rubber seals were analysed with polymerase chain reactions (PCR) using specific primers for phylogenetic group, multilocus sequence type (MLST) determination the presence of 43 virulence-associated genes (VAGs) linked with intestinal and extraintestinal E. coli infections and the presence of some typical E. coli virulence plasmids’ sequences in order to assess their virulence potential and/or specific genes, associated with the adaption to a specific environment. It was found that all of the 35 E. coli isolates belonged to the commensal non-pathogenic phylogenetic group A and that the diversity of these E. coli isolates, according to MLST analysis, was relatively low. Further, the prevalence of virulence-associated genes among the dishwasher rubber seal E. coli isolates was also low. Only the following VAGs were detected: fimH, crl, fluA, picU, irp, fyuA, sitA, aslA. Of the five plasmid replication regions tested only RepFIA and RepFIIA were detected. The two sequences associated with conjugative plasmids namely traJ and traT, were detected in only one isolate. Based on the obtained results the studied isolates can be designated as commensal E. coli with low pathogenic potential. Due to the low diversity of sequence types, even among isolates obtained from dishwashers from different locations, there is a possibility that strains from certain clonal groups are more adapted to specific habitats outside warm-blooded hosts than strains of other sequence types.

References

Abreu, A.G., Fraga, T.R., Granados Martínez, A.P., Kondo, M.Y., Juliano, M.A., Juliano, L., Navarro-Garcia, F., Isaac, L., Barbosa, A.S., Elias, W.P., 2015. The serine protease Pic from enteroaggregative Escherichia coli mediates immune evasion by the direct cleavage of complement. The Journal of Infectious Diseases, 212, 106-115. DOI: https://doi.org/10.1093/infdis/jiv013

Allocati, N., Masulli, M., Alexeyev, M.F., Di Ilio, C., 2013. Escherichia coli in Europe: an overview. International Journal of Environmental Research and Public Health, 10(12), 6235-6254. DOI: https://doi.org/10.3390/ijerph10126235

Bhullar, K., Zarepour, M., Yu, H., Yang, H., Croxen, M., Stahl, M., Finlay, B.B., Turvey, S.E., Vallance, B.A., 2015. The serine protease autotransporter Pic modulates Citrobacter rodentium pathogenesis and its innate recognition by the host. Infection and Immunity, 83, 2636-2650. DOI: https://doi.org/10.1128/IAI.00025-15

Carattoli, A., Bertini, A., Villa, L., Falbo, V., Hopkins, K.L., Threlfall, E.J., 2005. Identification of plasmids by PCR-based replicon typing. Journal of Microbiological Methods, 63, 219-228. DOI: https://doi.org/10.1016/j.mimet.2005.03.018

Chaudhuri, R.R., Henderson, I.R., 2012. The evolution of the Escherichia coli phylogeny. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 12(2), 214-226. DOI: https://doi.org/10.1016/j.meegid.2012.01.005

Clermont, O., Bonacorsi, S., Bingen, E., 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Applied and Environmental Microbiology, 66, 4555-4558. DOI: https://doi.org/10.1128/AEM.66.10.4555-4558.2000

Clermont, O., Christenson, J.K., Denamur, E., Gordon, D.M., 2013. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environmental Microbiology Reports, 5, 58-65. DOI: https://doi.org/10.1111/1758-2229.12019

Čurová, K., Slebodníková, R., Kmeťová, M., Hrabovský, V., Maruniak, M., Liptáková, E., Siegfried, L., 2020. Virulence, phylogenetic background and antimicrobial resistance in Escherichia coli associated with extraintestinal infections. Journal of Infection and Public Health, 13(10), 1537-1543. DOI: https://doi.org/10.1016/j.jiph.2020.06.032

Dozois, C.M., Fairbrother, J.M., Harel, J., Bossé, M., 1992. Pap-and pil-related DNA sequences and other virulence determinants associated with Escherichia coli isolated from septicemic chickens and turkeys. Infection and Immunity, 60, 2648-2656. DOI: https://doi.org/10.1128/iai.60.7.2648-2656.1992

Escobar-Páramo, P., Le Menac’h, A., Le Gall, T., Amorin, C., Gouriou, S., Picard, B., Skurnik, D., Denamur E., 2006. Identification of forces shaping the commensal Escherichia coli genetic structure by comparing animal and human isolates. Environmental Microbiology, 11, 1975-1984. DOI: https://doi.org/10.1111/j.1462-2920.2006.01077.x

Ewers, C., Li, G., Wilking, H., Kiessling, S., Alt, K., Antáo, E.M., Laturnus, C., Diehl, I., Glodde, S., Home- ier, T., Böhnke, U., Steinrück, H., Philipp, H.C., Wieler. L.H., 2007. Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they? International Journal of Medical Microbiology : IJMM, 297, 163-176. DOI: https://doi.org/10.1016/j.ijmm.2007.01.003

Hoffman, J., Badger, J.L., Zhang, Y., Huang, S., Kim, K.S., 2000. Escherichia coli K1 aslA contributes to invasion of brain microvascular endothelial cells in vitro and in vivo. Infection and Immunity, 68, 5062-5067. DOI: https://doi.org/10.1128/IAI.68.9.5062-5067.2000

Jang, J., Hur, H.G., Sadowsky, M.J., Byappanahalli, M.N., Yan, T., Ishii, S., 2017. Environmental Escherichia coli: ecology and public health implications-a review. Journal of Applied Microbiology, 123(3), 570-581. DOI: https://doi.org/10.1111/jam.13468

Janβen, T., Schwarz, C., Preikschat, P., Voss, M., Phillip, H.C., Wieler, L.H., 2001. Virulence associated genes in avian pathogenic Escherichia coli (APEC) isolated from internal organs of poultry having died from colibacillosis. International Journal of Medical Microbiology: IJMM, 291, 371-378. DOI: https://doi.org/10.1078/1438-4221-00143

Johnson, J.R., Stell, A.L., 2000. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. The Journal of Infectious Diseases, 181, 261-272. DOI: https://doi.org/10.1086/315217

Kaper, J.B., Nataro, J.P., Mobley, H.L., 2004. Pathogenic Escherichia coli. Nature reviews. Microbiology, 2(2), 123-140. DOI: https://doi.org/10.1038/nrmicro818

Maurer, J.J., Brown, T.P., Steffens, W.L., Thayer, S.G., 1998. The occurrence of ambient temperature-regulated adhesins, curli, and the temperature-sensitive hemagglutinin tsh among avian Escherichia coli. Avian Diseases, 42, 106-118. DOI: https://doi.org/10.2307/1592582

Miao, L., Li, H., Ding, W., Lu, S., Pan, S., Guo, X., Zhou, X., Wang, D., 2022. Research priorities on One Health: A bibliometric analysis. Frontiers in Public Health, 10, 889854. DOI: https://doi.org/10.3389/fpubh.2022.889854

Parham, N.J., Pollard, S.J., Chaudhuri, R.R., Beatson, S.A., Desvaux, M., Russell, M.A., Ruiz, J., Fivian, A., Vila, J., Henderson, I.R., 2005. Prevalence of pathogenicity island IICFT073 genes among extraintestinal clinical isolates of Escherichia coli. Journal of Clinical Microbiology, 43, 2425-2434. DOI: https://doi.org/10.1128/JCM.43.5.2425-2434.2005

Paton, A.W., Paton, J.C., 1998. Detection and characterization of Shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic E. coli hlyA, rfbO111, and rfbO157. Journal of Clinical Microbiology, 36, 598-602. DOI: https://doi.org/10.1128/JCM.36.2.598-602.1998

Pratt, L.A., Kolter, R., 1999. Genetic analyses of bacterial biofilm formation. Current Opinion in Microbiology, 2, 598-603. DOI: https://doi.org/10.1016/S1369-5274(99)00028-4

Restieri, C., Garriss, G., Locas, M.C., Dozois, C.M., 2007. Autotransporter-encoding sequences are phylogenetically distributed among Escherichia coli clinical isolates and reference strains. Applied and Environmental Microbiology, 73, 1553-1562. DOI: https://doi.org/10.1128/AEM.01542-06

Ruiz, J., Simon, K., Horcajada, J.P., Velasco, M., Barranco, M., Roig, G., Moreno-Martínez, A., Martínez,

J.A., Jiménez de Anta, T., Mensa, J., Vila, J., 2002. Differences in virulence factors among clinical isolates of Escherichia coli causing cystitis and pyelonephritis in women and prostatitis in men. Journal of Clinical Microbiology, 40, 4445-4449. DOI: https://doi.org/10.1128/JCM.40.12.4445-4449.2002

Runyen-Janecky, L.J., Reeves, S.A., Gonzales, E.G., Payne, S.M., 2003. Contribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells. Infection and Immunity, 71, 1919-1928. DOI: https://doi.org/10.1128/IAI.71.4.1919-1928.2003

Schubert, S., Rakin, A., Karch, H., Carniel, E., Heesemann, J., 1998. Prevalence of the „high-pathogenicity island“ of Yersinia species among Escherichia coli strains that are pathogenic to humans. Infection and Immunity, 66, 480-485. DOI: https://doi.org/10.1128/IAI.66.2.480-485.1998

Sobecky, P.A., Mincer, T.J., Chang, M.C., Helinski, D.R., 1997. Plasmids isolated from marine sediment microbial communities contain replication and incompatibility regions unrelated to those of known plasmid groups. Applied and Environmental Microbiology, 63, 888-895. DOI: https://doi.org/10.1128/aem.63.3.888-895.1997

Starčič, M., Žgur-Bertok, D., Jordi, B.J., Wösten, M.M., Gaastra, W., van Putten, J.P., 2003. The cyclic AMP-cyclic AMP receptor protein complex regulates activity of the traJ promoter of the Escherichia coli conjugative plasmid pRK100. Journal of Bacteriology, 185, 1616-1623. DOI: https://doi.org/10.1128/JB.185.5.1616-1623.2003

Starčič Erjavec, M., Gaastra, W., van Putten, J., Žgur-Bertok, D., 2003. Identification of the origin of replications and partial characterization of plasmid pRK100. Plasmid, 50, 102-112. DOI: https://doi.org/10.1016/S0147-619X(03)00016-7

Starčič Erjavec, M., Žgur-Bertok, D., 2015. Virulence potential for extraintestinal infections among commensal Escherichia coli isolated from healthy humans-the Trojan horse within our gut. FEMS Microbiology Letters, 362(5), fnu061. DOI: https://doi.org/10.1093/femsle/fnu061

Stoppe, N.C., Silva, J.S., Carlos, C., Sato, M.I.Z., Saraiva, A.M., Ottoboni, L.M.M., Torres, T.T., 2017. Worldwide phylogenetic group patterns of Escherichia coli from commensal human and wastewater treatment plant isolates. Frontiers in Microbiology, 8, 2512. DOI: https://doi.org/10.3389/fmicb.2017.02512

Tenaillon, O., Skurnik, D., Picard, B., Denamur, E., 2010. The population genetics of commensal Escherichia coli. Nature Reviews. Microbiology, 8, 207-217. DOI: https://doi.org/10.1038/nrmicro2298

Tóth, I., Hérault, F., Beutin, L., Oswald E., 2003. Production of cytolethal distending toxins by pathogenic Escherichia coli strains isolated from human and animal sources: establishment of the existence of a new cdt variant (Type IV). Journal of Clinical Microbiology, 41, 4285-4291. DOI: https://doi.org/10.1128/JCM.41.9.4285-4291.2003

Vidal, M., Kruger, E., Durán, C., Lagos, R., Levine, M., Prado, V., Toro, C., Vidal, R., 2005. Single multiplex PCR assay to identify simultaneously the six categories of diarrheagenic Escherichia coli associated with enteric infections. Journal of Clinical Microbiology, 43, 5362-5365. DOI: https://doi.org/10.1128/JCM.43.10.5362-5365.2005

Vila, J., Vargas, M., Henderson, I.R., Gascón, J., Nataro, J.P., 2000. Enteroaggregative Escherichia coli virulence factors in traveler‘s diarrhea strains. The Journal of Infectious Diseases, 182, 1780-1783. DOI: https://doi.org/10.1086/317617

Watt, S., Lanotte, P., Mereghetti, L., Moulin-Schouleur, M., Picard, B., Quentin, R., 2003. Escherichia coli strains from pregnant women and neonates: intraspecies genetic distribution and prevalence of virulence factors. Journal of Clinical Microbiology, 41, 1929-1935. DOI: https://doi.org/10.1128/JCM.41.5.1929-1935.2003

Wirth, T., Falush, D., Lan, R., Colles, F., Mensa, P., Wieler, L.H., Karch, H., Reeves, P.R., Maiden, M.C., Ochman, H., Achtman, M., 2006. Sex and virulence in Escherichia coli: an evolutionary perspective. Molecular Microbiology, 60, 1136-1151. DOI: https://doi.org/10.1111/j.1365-2958.2006.05172.x

Yamamoto, S., Terai, A., Yuri, K., Kurazono, H., Takeda, Y., Yoshida, O., 1995. Detection of urovirulence factors in Escherichia coli by multiplex polymerase chain reaction. FEMS Immunology and Medical Microbiology, 12, 85-90. DOI: https://doi.org/10.1111/j.1574-695X.1995.tb00179.x

Yamamoto, T., Echeverria, P., 1996. Detection of the enteroaggregative Escherichia coli heat-stable enterotoxin 1 gene sequences in enterotoxigenic E. coli strains pathogenic for humans. Infection and Immunity, 64, 1441-1445. DOI: https://doi.org/10.1128/iai.64.4.1441-1445.1996

Zude, I., Leimbach, A., Dobrindt, U., 2013. Prevalence of autotransporters in Escherichia coli: what is the impact of phylogeny and pathotype? International Journal of Medical Microbiology: IJMM, 304, 243-256. Zupančič, J., Turk, M., Črnigoj, M., Ambrožič Avguštin, J., Gunde-Cimerman, N., 2019. The dishwasher E. coli from dishwasher rubber seals rubber seal acts as a reservoir of bacteria in the home environment. BMC Microbiology, 19(1), 300. DOI: https://doi.org/10.1186/s12866-019-1674-5

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Published

01.07.2022

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Original Research Paper

How to Cite

Starčič Erjavec, M., & Ambrožič Avguštin, J. (2022). Molecular characterization of Escherichia coli from dishwasher rubber seals. Acta Biologica Slovenica, 65(1), 18-27. https://doi.org/10.14720/abs.65.1.15942

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