Characterization of six Shiga toxin-producing Escherichia coli (STEC) strains carrying Stx2-phages from Colombia
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Sep 6, 2022
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Brayan Stiven Arango
https://orcid.org/0000-0003-0311-3433
Sebastián Peña Buitrago
https://orcid.org/0000-0002-4657-4232
Jhon Carlos Castaño Osorio
https://orcid.org/0000-0002-7639-3053
Claudia Viviana Granobles Velandia
https://orcid.org/0000-0002-0742-6181
https://orcid.org/0000-0003-0311-3433
Sebastián Peña Buitrago
https://orcid.org/0000-0002-4657-4232
Jhon Carlos Castaño Osorio
https://orcid.org/0000-0002-7639-3053
Claudia Viviana Granobles Velandia
https://orcid.org/0000-0002-0742-6181
##plugins.themes.bootstrap3.article.details##
Abstract
Shiga toxin producing Escherichia coli (STEC) is a bacterial pathogen that causes diarrhea and severe human diseases like HUS; its main virulence factor are the Shiga toxins (Stx1 and Stx2). Some Stx2 subtypes have been identified and associated with the risk of developing severe illness. Stx toxins are encoded in temperate bacteriophages which control their expression through the lytic cycle that is regulated by the late genes and Q anti-terminator protein. The aim of this work was to characterize six STEC strains carrying Stx2-phages to provide preliminary information and understanding about Stx2 strains from Colombia regarding the Stx production, lytic cycle induction and subtyping of Stx2. Two highlighted strains with higher levels of Stx production and lytic cycle’s induction were observed. All the evaluated strains carried either the Stx2a, Stx2c, or Stx2d subtypes. In addition, most of the strains carried the qO111 allele, and only one strain showed differences in the ninG region. Differences in the evaluated characteristics of the strains were observed, which could indicate the variability of these six STEC strains carrying Stx2-phages.
Keywords
STEC, Bacteriophage, Shiga toxin, Cattle, HUS
References
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doi: 10.1099/mic.0.2007/009704-0
[22]Ogura Y, Mondal S.I, Islam MR, Mako T, Arisawa K, Katsura K, Ooka T, Gotoh Y, Murase K, Ohnishi M, Hayashi T. The Shiga toxin 2 production level in enterohemorrhagic Escherichia coli O157: H7 is correlated with the subtypes of toxin encoding phage, Scientific reports, 5(1): 1–11, 2015.
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[23] Canchaya C, Fournous G, Chibani-Chennoufi S, Dillmann ML, Brüssow H. Phage as agents of lateral gene transfer, Current opinion in microbiology, 6(4): 417–424, 2003.
doi: 10.1016/s1369-5274(03)00086-
[24] Bobay L, Touchon M, Rocha E. Pervasive domestication of defective prophages by bacteria, Proceedings of the National Academy of Sciences, 111(33): 12127–12132, 2014.
doi: 10.1073/pnas.1405336111
[25] Johansen B, Wasteson Y, Granum P, Brynestad S. Mosaic structure of Shiga-toxin-2-encoding phages isolated from Escherichia coli O157:H7 indicates frequent gene exchange between lambdoid phage genomes, Microbiology, 147(7): 1929–1936, 2001.
doi: 10.1099/00221287-147-7-1929
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doi: 10.1128/IAI.72.12.7131
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doi: 10.1128/IAI.00060-09
[28] Karch H, Bielaszewska M. Sorbitol-fermenting Shiga toxin-producing Escherichia coli O157: H− strains: epidemiology, phenotypic and molecular characteristics, and microbiological diagnosis, Journal of Clinical Microbiology, 39(6): 2043–2049, 2001.
doi: 10.1128/JCM.39.6.2043-2049.2001
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doi: 10.2807/esw.06.44.01955-en
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doi: 10.1128/IAI.01180-08
[31] Koitabashi T, Vuddhakul V, Radu S, Morigaki T, Asai N, Nakaguchi Y, Nishibuchi M.
Genetic Characterization of Escherichia coli O157: H7/–Strains Carrying the stx2 Gene but Not Producing Shiga Toxin 2, Microbiology and immunology, 50(2): 135–148, 2006.
doi: 10.1111/j.1348-0421.2006.tb03779.x
[32] Rahman M, Nabi A, Asadulghani M, Faruque SM, Islam MA. Toxigenic properties and stx phage characterization of Escherichia coli O157 isolated from animal sources in a developing country setting, BMC Microbiology, 18(1): 98, 2018.
doi: 10.1186/s12866-018-1235-3
[33] Koitabashi T, Cui S, Kamruzzaman M, Nishibuchi M. Isolation and characterization of the Shiga toxin gene (stx)–bearing Escherichia coli O157 and non-O157 from retail meats in Shandong Province, China, and characterization of the O157-derived stx 2 phages, Journal of food protection, 71(4): 706–713, 2008.
doi: 10.4315/0362-028x-71.4.706
[34] Fierz L, Cernela N, Hauser E, Nüesch-Inderbinen M, Stephan R. Human infections with Shiga toxin-producing Escherichia coli, Switzerland, 2010-2014, Frontiers in Microbiology, 8: 1471, 2017.
doi: 10.3389/fmicb.2017.01471
[35] Melton-Celsa A, O’Brien A, Feng P. Virulence Potential of Activatable Shiga Toxin 2d–Producing Escherichia coli Isolates from Fresh Produce, Journal of food protection, 78(11): 2085–2088, 2015.
doi: 10.4315/0362-028X.JFP-15-180
[36] Schmidt H, Scheef J, Morabito S, Caprioli A, Wieler LH, Karch H. A new Shiga toxin 2
variant (Stx2f) from Escherichia coli isolated from pigeons, Applied and Environmental Microbiology, 66(3): 1205–1208, 2000.
doi: 10.1128/aem.66.3.1205-1208.2000
[37] Meng Q, Bai X, Zhao A, Lan R, Du H, Wang T, Shi C, Yuan X, Bai X, Ji S, Jin D, Yu B, Wang Y, Sun H, Liu K, Xu J, Xiong Y. Characterization of Shiga toxin-producing Escherichia coli isolated from healthy pigs in China, BMC Microbiology, 14: 5, 2014.
doi: 10.1186/1471-2180-14-5
doi: 10.3390/toxins2122769
[2] Persad A, Lejeune J. Animal Reservoirs of Shiga Toxin-Producing Escherichia coli. In: Sperandio V, Hovde C editors, Enterohemorrhagic Escherichia Coli and Other Shiga Toxin-Producing E. Coli, 211–230, 2015.
doi: 10.1128/microbiolspec.EHEC-0027-2014
[3] Bergan J, Lingelem A, Simm R, Skotland T, Sandvig K. Shiga toxins, Toxicon, 60(6):1085–1107, 2012.
doi: 10.1016/j.toxicon.2012.07.016
[4] Bauwens A, Bielaszewska M, Kemper B, Langehanenberg P, Bally G, Reichelt R, Mulac D, Humpf HU, Friedrich AW, Kim KS, Karch H, Müthing J. Differential cytotoxic actions of Shiga toxin 1 and Shiga toxin 2 on microvascular and macrovascular endothelial cells, Thrombosis and haemostasis, 105(3): 515–528, 2011.
doi: 10.1160/TH10-02-0140
[5] Kawano K, Okada M, Haga T, Maeda K, Goto Y. Relationship between pathogenicity for humans and stx genotype in Shiga toxin-producing Escherichia coli serotype O157, European Journal of Clinical Microbiology and Infectious Diseases, 27(3): 227–232, 2008.
doi: 10.1007/s10096-007-0420-3
[6] Fuller CA, Pellino CA, Flagler MJ, Strasser JE, Weiss AA. Shiga toxin subtypes display dramatic differences in potency, Infection and immunity, 79(3): 1329–1337, 2011.
doi: 10.1007/s10096-007-0420-3
[7] Scheutz F, Teel L, Beutin L, Piérard D, Buvens G, Karch H, Mellmann A, Caprioli A, Tozzoli R, Morabito S, Strockbine N, Melton-Celsa A, Sanchez M, Persson S, O’Brienb A. Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature, Journal of clinical microbiology, 50(9): 2951–2963, 2012.
doi: 10.1128/JCM.00860-12
[8] Muhldorfer I, Hacker J, Keusch GT, Acheson DW, Tschape H, Kane AV, Ritter A, Olschlager T, Donohue-Rolfe A. Regulation of the Shiga-like toxin II operon in Escherichia coli, Infection and immunity, 64: 495–502, 1996.
doi: 10.1128/iai.64.2.495-502.1996
[9] Plunkett G, Rose D, Durfee T, Blattner F. Sequence of Shiga Toxin 2 Phage 933W from Escherichia coli O157: H7: Shiga Toxin as a Phage Late-Gene Product, Journal of bacteriology, 181(6): 1767–1778, 1999.
doi: 10.1128/JB.181.6.1767-1778.1999
[10] Matsumoto M, Suzuki M, Takahashi M, Hirose K, Minagawa H, Ohta M. Identification and epidemiological description of enterohemorrhagic Escherichia coli O157 strains producing low amounts of Shiga toxin 2 in Aichi Prefecture, Japan, Japanese Journal of Infectious Diseases, 61(6): 442–445, 2008.
[11] Haugum K, Lindstedt B, Løbersli I, Kapperud G, Brandal T. Identification of the antiterminator qO111: H− gene in Norwegian sorbitol-fermenting Escherichia coli O157: NM, FEMS microbiology letters, 329(2): 102–110, 2012.
doi: 10.1111/j.1574-6968.2012.02505.x
[12] Piedrahita D, Márquez T, Máttar S. Detección de Escherichia coli 0157: H7 en poblaciones porcinas, canal bovina y productos cárnicos en el departamento de Córdoba, Revista MVZ Córdoba, 6: 119–126, 2001.
doi: 10.21897/rmvz.532
[13] Franco P, Orozco M, Ramírez L, López L. Determinación de Escherichia coli e identificación del serotipo O157: H7 en carne de cerdo comercializada en los principales supermercados de la ciudad de Cartagena, Revista Lasallista de investigación, 10: 91–100, 2013.
[14] Quiguanás-Guarín E, Granobles-Velandia C, Arango-Gil B, Giraldo-Rubio V, Castaño- Osorio J. Aislamiento de Escherichia coli productora de toxina Shiga (STEC) en heces de ganado y detección de factores de virulencia asociados con su patogénesis, Infectio, 25(1): 33–38, 2021.
doi: 10.22354/in.v25i1.906
[15] Muniesa M, Simon M, Prats G, Ferrer D, Panella H, Jofre J. Shiga toxin 2-converting bacteriophages associated with clonal variability in Escherichia coli O157: H7 strains of human origin isolated from a single outbreak, Infect Immun, 71(8): 4554–4562, 2003.
doi: 10.1128/iai.71.8.4554-4562.2003
[16] Unkmeir A, Schmidt H. Structural analysis of phage-borne stx genes and their flanking sequences in Shiga toxin-producing Escherichia coli and Shigella dysenteriae type 1 strains, Infect Immun, 68(9): 4856–4864, 2000.
doi: 10.1128/IAI.68.9.4856-4864.2000
[17] Smith D, Wareing B, Fogg P, Riley L, Spencer M, Cox M, Saunders J, McCarthy A, Allison H. Multilocus characterization scheme for Shiga toxin-encoding bacteriophages, Applied and environmental microbiology, 73(24): 8032–8040, 2007.
doi: 10.1128/AEM.01278-07
[18] LeJeune J, Abedon S, Takemura K, Christie NP, Sreevatsan S. Human Escherichia coli O157:H7 genetic marker in isolates of bovine origin, Emerging infectious diseases, 10(8): 1482–1485, 2004.
doi: 10.3201/eid1008.030784
[19] Persson S, Olsen K, Ethelberg S, Scheutz F. Subtyping method for Escherichia coli Shiga toxin (verocytotoxin) 2 variants and correlations to clinical manifestations, Journal of clinical microbiology, 45(6): 2020–2024, 2007.
doi: 10.1128/JCM.02591-06
[20] Granobles C, Krüger A, Parma Y, Parma AE, Lucchesi PM. Differences in Shiga toxin and phage production among stx2g-positive STEC strains, Frontiers in Cellular and Infection Microbiology, 2: 1–5, 2012.
doi: 10.3389/fcimb.2012.00082
[21] De Sablet T, Bertin Y, Vareille M, Girardeau JP, Garrivier A, Gobert AP, Martin C. Differential expression of stx2 variants in Shiga toxin-producing Escherichia coli belonging to seropathotypes A and C, Microbiology, 154(1): 176–186, 2008.
doi: 10.1099/mic.0.2007/009704-0
[22]Ogura Y, Mondal S.I, Islam MR, Mako T, Arisawa K, Katsura K, Ooka T, Gotoh Y, Murase K, Ohnishi M, Hayashi T. The Shiga toxin 2 production level in enterohemorrhagic Escherichia coli O157: H7 is correlated with the subtypes of toxin encoding phage, Scientific reports, 5(1): 1–11, 2015.
doi: 10.1038/srep16663
[23] Canchaya C, Fournous G, Chibani-Chennoufi S, Dillmann ML, Brüssow H. Phage as agents of lateral gene transfer, Current opinion in microbiology, 6(4): 417–424, 2003.
doi: 10.1016/s1369-5274(03)00086-
[24] Bobay L, Touchon M, Rocha E. Pervasive domestication of defective prophages by bacteria, Proceedings of the National Academy of Sciences, 111(33): 12127–12132, 2014.
doi: 10.1073/pnas.1405336111
[25] Johansen B, Wasteson Y, Granum P, Brynestad S. Mosaic structure of Shiga-toxin-2-encoding phages isolated from Escherichia coli O157:H7 indicates frequent gene exchange between lambdoid phage genomes, Microbiology, 147(7): 1929–1936, 2001.
doi: 10.1099/00221287-147-7-1929
[26] Gamage S, Patton A, Hanson J, Weiss AA. Diversity and host range of Shiga toxin encoding phage, Infection and Immunity, 72(12): 7131–7139, 2004.
doi: 10.1128/IAI.72.12.7131
[27] Shimizu T, Ohta Y, Noda M. Shiga Toxin 2 is specifically released from bacterial cells by Two different mechanisms, Infection and immunity, 77(7): 2813–2823, 2009.
doi: 10.1128/IAI.00060-09
[28] Karch H, Bielaszewska M. Sorbitol-fermenting Shiga toxin-producing Escherichia coli O157: H− strains: epidemiology, phenotypic and molecular characteristics, and microbiological diagnosis, Journal of Clinical Microbiology, 39(6): 2043–2049, 2001.
doi: 10.1128/JCM.39.6.2043-2049.2001
[29] Allison L. HUS due to a sorbitol-fermenting verotoxigenic E. coli O157 in Scotland, Eurosurveillance, 6(44), 1955.
doi: 10.2807/esw.06.44.01955-en
[30] Rosser T, Dransfield T, Allison L, Hanson M, Holden N, Evans J, Naylor S, La Ragione R, Low C, Gally D. Pathogenic potential of emergent sorbitol-fermenting Escherichia coli O157: NM, Infection and immunity, 76(12): 5598–5607, 2008.
doi: 10.1128/IAI.01180-08
[31] Koitabashi T, Vuddhakul V, Radu S, Morigaki T, Asai N, Nakaguchi Y, Nishibuchi M.
Genetic Characterization of Escherichia coli O157: H7/–Strains Carrying the stx2 Gene but Not Producing Shiga Toxin 2, Microbiology and immunology, 50(2): 135–148, 2006.
doi: 10.1111/j.1348-0421.2006.tb03779.x
[32] Rahman M, Nabi A, Asadulghani M, Faruque SM, Islam MA. Toxigenic properties and stx phage characterization of Escherichia coli O157 isolated from animal sources in a developing country setting, BMC Microbiology, 18(1): 98, 2018.
doi: 10.1186/s12866-018-1235-3
[33] Koitabashi T, Cui S, Kamruzzaman M, Nishibuchi M. Isolation and characterization of the Shiga toxin gene (stx)–bearing Escherichia coli O157 and non-O157 from retail meats in Shandong Province, China, and characterization of the O157-derived stx 2 phages, Journal of food protection, 71(4): 706–713, 2008.
doi: 10.4315/0362-028x-71.4.706
[34] Fierz L, Cernela N, Hauser E, Nüesch-Inderbinen M, Stephan R. Human infections with Shiga toxin-producing Escherichia coli, Switzerland, 2010-2014, Frontiers in Microbiology, 8: 1471, 2017.
doi: 10.3389/fmicb.2017.01471
[35] Melton-Celsa A, O’Brien A, Feng P. Virulence Potential of Activatable Shiga Toxin 2d–Producing Escherichia coli Isolates from Fresh Produce, Journal of food protection, 78(11): 2085–2088, 2015.
doi: 10.4315/0362-028X.JFP-15-180
[36] Schmidt H, Scheef J, Morabito S, Caprioli A, Wieler LH, Karch H. A new Shiga toxin 2
variant (Stx2f) from Escherichia coli isolated from pigeons, Applied and Environmental Microbiology, 66(3): 1205–1208, 2000.
doi: 10.1128/aem.66.3.1205-1208.2000
[37] Meng Q, Bai X, Zhao A, Lan R, Du H, Wang T, Shi C, Yuan X, Bai X, Ji S, Jin D, Yu B, Wang Y, Sun H, Liu K, Xu J, Xiong Y. Characterization of Shiga toxin-producing Escherichia coli isolated from healthy pigs in China, BMC Microbiology, 14: 5, 2014.
doi: 10.1186/1471-2180-14-5
How to Cite
Arango, B. S., Peña Buitrago, S., Castaño Osorio, J. C., & Granobles Velandia, C. V. (2022). Characterization of six Shiga toxin-producing Escherichia coli (STEC) strains carrying Stx2-phages from Colombia. Universitas Scientiarum, 27(2), 187–202. https://doi.org/10.11144/Javeriana.SC272.coss
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Microbiología / Microbiology / Microbiologia
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