Strain belonging to an emerging, virulent sublineage of ST131 Escherichia coli isolated in fresh spinach, suggesting that ST131 may be transmissible through agricultural products

Food contamination with pathogenic Escherichia coli can cause severe disease. Here, we report the isolation of a multidrug resistant strain (A23EC) from fresh spinach. A23EC belongs to subclade C2 of ST131, a virulent clone of Extraintestinal Pathogenic E. coli (ExPEC). Most A23EC virulence factors...

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Main Authors: Maria G. Balbuena-Alonso, Manel Camps, Gerardo Cortés-Cortés, Eder A. Carreón-León, Patricia Lozano-Zarain, Rosa del Carmen Rocha-Gracia
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-10-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2023.1237725/full
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author Maria G. Balbuena-Alonso
Manel Camps
Gerardo Cortés-Cortés
Gerardo Cortés-Cortés
Eder A. Carreón-León
Patricia Lozano-Zarain
Rosa del Carmen Rocha-Gracia
author_facet Maria G. Balbuena-Alonso
Manel Camps
Gerardo Cortés-Cortés
Gerardo Cortés-Cortés
Eder A. Carreón-León
Patricia Lozano-Zarain
Rosa del Carmen Rocha-Gracia
author_sort Maria G. Balbuena-Alonso
collection DOAJ
description Food contamination with pathogenic Escherichia coli can cause severe disease. Here, we report the isolation of a multidrug resistant strain (A23EC) from fresh spinach. A23EC belongs to subclade C2 of ST131, a virulent clone of Extraintestinal Pathogenic E. coli (ExPEC). Most A23EC virulence factors are concentrated in three pathogenicity islands. These include PapGII, a fimbrial tip adhesin linked to increased virulence, and CsgA and CsgB, two adhesins known to facilitate spinach leaf colonization. A23EC also bears TnMB1860, a chromosomally-integrated transposon with the demonstrated potential to facilitate the evolution of carbapenem resistance among non-carbapenemase-producing enterobacterales. This transposon consists of two IS26-bound modular translocatable units (TUs). The first TU carries aac(6’)-lb-cr, blaOXA-1, ΔcatB3, aac(3)-lle, and tmrB, and the second one harbors blaCXT-M-15. A23EC also bears a self-transmissible plasmid that can mediate conjugation at 20°C and that has a mosaic IncF [F(31,36):A(4,20):B1] and Col156 origin of replication. Comparing A23EC to 86 additional complete ST131 sequences, A23EC forms a monophyletic cluster with 17 other strains that share the following four genomic traits: (1) virotype E (papGII+); (2) presence of a PAI II536-like pathogenicity island with an additional cnf1 gene; (3) presence of chromosomal TnMB1860; and (4) frequent presence of an F(31,36):A(4,20):B1 plasmid. Sequences belonging to this cluster (which we named “C2b sublineage”) are highly enriched in septicemia samples and their associated genetic markers align with recent reports of an emerging, virulent sublineage of the C2 subclade, suggesting significant pathogenic potential. This is the first report of a ST131 strain belonging to subclade C2 contaminating green leafy vegetables. The detection of this uropathogenic clone in fresh food is alarming. This work suggests that ST131 continues to evolve, gaining selective advantages and new routes of transmission. This highlights the pressing need for rigorous epidemiological surveillance of ExPEC in vegetables with One Health perspective.
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spelling doaj.art-f2e69608b1f24dc3992437355b818a202023-10-09T11:13:09ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-10-011310.3389/fcimb.2023.12377251237725Strain belonging to an emerging, virulent sublineage of ST131 Escherichia coli isolated in fresh spinach, suggesting that ST131 may be transmissible through agricultural productsMaria G. Balbuena-Alonso0Manel Camps1Gerardo Cortés-Cortés2Gerardo Cortés-Cortés3Eder A. Carreón-León4Patricia Lozano-Zarain5Rosa del Carmen Rocha-Gracia6Posgrado en Microbiología, Centro de Investigaciones Microbiológicas, Instituto de Ciencias, Benemérita Universidad Autónoma de Puebla, Puebla, MexicoDepartament of Microbiology and Environmental Toxicology, University of California at Santa Cruz, Santa Cruz, CA, United StatesPosgrado en Microbiología, Centro de Investigaciones Microbiológicas, Instituto de Ciencias, Benemérita Universidad Autónoma de Puebla, Puebla, MexicoDepartament of Microbiology and Environmental Toxicology, University of California at Santa Cruz, Santa Cruz, CA, United StatesFacultad de Ciencias Químicas, Universidad Autónoma de Chihuahua, Chihuahua, MexicoPosgrado en Microbiología, Centro de Investigaciones Microbiológicas, Instituto de Ciencias, Benemérita Universidad Autónoma de Puebla, Puebla, MexicoPosgrado en Microbiología, Centro de Investigaciones Microbiológicas, Instituto de Ciencias, Benemérita Universidad Autónoma de Puebla, Puebla, MexicoFood contamination with pathogenic Escherichia coli can cause severe disease. Here, we report the isolation of a multidrug resistant strain (A23EC) from fresh spinach. A23EC belongs to subclade C2 of ST131, a virulent clone of Extraintestinal Pathogenic E. coli (ExPEC). Most A23EC virulence factors are concentrated in three pathogenicity islands. These include PapGII, a fimbrial tip adhesin linked to increased virulence, and CsgA and CsgB, two adhesins known to facilitate spinach leaf colonization. A23EC also bears TnMB1860, a chromosomally-integrated transposon with the demonstrated potential to facilitate the evolution of carbapenem resistance among non-carbapenemase-producing enterobacterales. This transposon consists of two IS26-bound modular translocatable units (TUs). The first TU carries aac(6’)-lb-cr, blaOXA-1, ΔcatB3, aac(3)-lle, and tmrB, and the second one harbors blaCXT-M-15. A23EC also bears a self-transmissible plasmid that can mediate conjugation at 20°C and that has a mosaic IncF [F(31,36):A(4,20):B1] and Col156 origin of replication. Comparing A23EC to 86 additional complete ST131 sequences, A23EC forms a monophyletic cluster with 17 other strains that share the following four genomic traits: (1) virotype E (papGII+); (2) presence of a PAI II536-like pathogenicity island with an additional cnf1 gene; (3) presence of chromosomal TnMB1860; and (4) frequent presence of an F(31,36):A(4,20):B1 plasmid. Sequences belonging to this cluster (which we named “C2b sublineage”) are highly enriched in septicemia samples and their associated genetic markers align with recent reports of an emerging, virulent sublineage of the C2 subclade, suggesting significant pathogenic potential. This is the first report of a ST131 strain belonging to subclade C2 contaminating green leafy vegetables. The detection of this uropathogenic clone in fresh food is alarming. This work suggests that ST131 continues to evolve, gaining selective advantages and new routes of transmission. This highlights the pressing need for rigorous epidemiological surveillance of ExPEC in vegetables with One Health perspective.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1237725/fullExPECST131food safetyvirulencemobile genetic elementsconjugative transfer
spellingShingle Maria G. Balbuena-Alonso
Manel Camps
Gerardo Cortés-Cortés
Gerardo Cortés-Cortés
Eder A. Carreón-León
Patricia Lozano-Zarain
Rosa del Carmen Rocha-Gracia
Strain belonging to an emerging, virulent sublineage of ST131 Escherichia coli isolated in fresh spinach, suggesting that ST131 may be transmissible through agricultural products
Frontiers in Cellular and Infection Microbiology
ExPEC
ST131
food safety
virulence
mobile genetic elements
conjugative transfer
title Strain belonging to an emerging, virulent sublineage of ST131 Escherichia coli isolated in fresh spinach, suggesting that ST131 may be transmissible through agricultural products
title_full Strain belonging to an emerging, virulent sublineage of ST131 Escherichia coli isolated in fresh spinach, suggesting that ST131 may be transmissible through agricultural products
title_fullStr Strain belonging to an emerging, virulent sublineage of ST131 Escherichia coli isolated in fresh spinach, suggesting that ST131 may be transmissible through agricultural products
title_full_unstemmed Strain belonging to an emerging, virulent sublineage of ST131 Escherichia coli isolated in fresh spinach, suggesting that ST131 may be transmissible through agricultural products
title_short Strain belonging to an emerging, virulent sublineage of ST131 Escherichia coli isolated in fresh spinach, suggesting that ST131 may be transmissible through agricultural products
title_sort strain belonging to an emerging virulent sublineage of st131 escherichia coli isolated in fresh spinach suggesting that st131 may be transmissible through agricultural products
topic ExPEC
ST131
food safety
virulence
mobile genetic elements
conjugative transfer
url https://www.frontiersin.org/articles/10.3389/fcimb.2023.1237725/full
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