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Genome-Based Analysis of Extended-Spectrum β-Lactamase-Producing Escherichia coli in the Aquatic Environment and Nile Perch (Lates niloticus) of Lake Victoria, Tanzania

Extended-spectrum β-lactamase (ESBL)-producing bacteria constitute an emerging global health issue with food products being vehicles of transmission and the aquatic environments serving as potential reservoirs. This study aimed to characterize ESBL-producing Escherichia coli in Nile perch and water...

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Autores principales: Baniga, Zebedayo, Hounmanou, Yaovi M. Gildas, Kudirkiene, Egle, Kusiluka, Lughano J. M., Mdegela, Robinson H., Dalsgaard, Anders
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7046833/
https://www.ncbi.nlm.nih.gov/pubmed/32153519
http://dx.doi.org/10.3389/fmicb.2020.00108
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author Baniga, Zebedayo
Hounmanou, Yaovi M. Gildas
Kudirkiene, Egle
Kusiluka, Lughano J. M.
Mdegela, Robinson H.
Dalsgaard, Anders
author_facet Baniga, Zebedayo
Hounmanou, Yaovi M. Gildas
Kudirkiene, Egle
Kusiluka, Lughano J. M.
Mdegela, Robinson H.
Dalsgaard, Anders
author_sort Baniga, Zebedayo
collection PubMed
description Extended-spectrum β-lactamase (ESBL)-producing bacteria constitute an emerging global health issue with food products being vehicles of transmission and the aquatic environments serving as potential reservoirs. This study aimed to characterize ESBL-producing Escherichia coli in Nile perch and water from Lake Victoria in Tanzania. A total of 180 samples of Nile perch and 60 water samples were screened for ESBL-producing E. coli on MacConkey agar supplemented with 2 μg/ml of cefotaxime and confirmed by bla(CTX–M) and bla(TEM) PCR. Antimicrobial resistance was determined by the disk diffusion method, and the ESBL-producing isolates were whole genome sequencing (WGS). ESBL-producing E. coli were detected in eight of the 180 analyzed Nile perch samples, and only one water sample was positive (1.7%, n = 60). Isolates were resistant to sulfamethoxazole–trimethoprim (100%), ampicillin/cloxacillin (100%), erythromycin 72.7% (8/11), tetracycline 90.9% (10/11), and nalidixic acid 63.6% (7/11). This mostly corroborates the resistance genes that they carried for sulfonamides (sul1 and sul2), trimethoprim (dfrA and dfrB), aminoglycosides [aac(3)-IId, strA, and strB], tetracycline [tet(B) and tet(D)], and fluoroquinolones (qepA4). They harbored plasmid replicon types IncF, IncX, IncQ, and Col and carried bla(CTX–M–)(15) and bla(TEM–)(1)(B) genes generally found on the same contigs as the IncF plasmid replicon. Although epidemiologically unrelated, the strains formed three separate sequence type–phylogroup–serotype-specific clusters: C1, C2, and C3. Cluster C1 included five strains (3 to 13 SNPs) belonging to ST167, phylogroup A, and serotype O9:H21; the two C2 strains (11 SNPs) belong to ST156, phylogroup B1, and serotype ONT:H28; and C3 was made up of four strains (SNPs ranged from 4 to 17) of ST636, phylogroup B2, and serotype O45:H7. The common virulence gene gad was reported in all strains. In addition, strains in C2 and C3 possessed iss, lpfA, and nfaE virulence genes, and the vat gene was found only in C3. The present study reports the occurrence of multidrug-resistant ESBL-producing E. coli carrying plasmid-mediated ESBL genes in offshore water and Nile perch in Lake Victoria. Strains formed three clonal clusters of unknown origin. This study reveals that the Lake may serve as reservoir for ESBL-producing bacteria that can be transmitted by fish as a food chain hazard of One-Health concern.
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spelling pubmed-70468332020-03-09 Genome-Based Analysis of Extended-Spectrum β-Lactamase-Producing Escherichia coli in the Aquatic Environment and Nile Perch (Lates niloticus) of Lake Victoria, Tanzania Baniga, Zebedayo Hounmanou, Yaovi M. Gildas Kudirkiene, Egle Kusiluka, Lughano J. M. Mdegela, Robinson H. Dalsgaard, Anders Front Microbiol Microbiology Extended-spectrum β-lactamase (ESBL)-producing bacteria constitute an emerging global health issue with food products being vehicles of transmission and the aquatic environments serving as potential reservoirs. This study aimed to characterize ESBL-producing Escherichia coli in Nile perch and water from Lake Victoria in Tanzania. A total of 180 samples of Nile perch and 60 water samples were screened for ESBL-producing E. coli on MacConkey agar supplemented with 2 μg/ml of cefotaxime and confirmed by bla(CTX–M) and bla(TEM) PCR. Antimicrobial resistance was determined by the disk diffusion method, and the ESBL-producing isolates were whole genome sequencing (WGS). ESBL-producing E. coli were detected in eight of the 180 analyzed Nile perch samples, and only one water sample was positive (1.7%, n = 60). Isolates were resistant to sulfamethoxazole–trimethoprim (100%), ampicillin/cloxacillin (100%), erythromycin 72.7% (8/11), tetracycline 90.9% (10/11), and nalidixic acid 63.6% (7/11). This mostly corroborates the resistance genes that they carried for sulfonamides (sul1 and sul2), trimethoprim (dfrA and dfrB), aminoglycosides [aac(3)-IId, strA, and strB], tetracycline [tet(B) and tet(D)], and fluoroquinolones (qepA4). They harbored plasmid replicon types IncF, IncX, IncQ, and Col and carried bla(CTX–M–)(15) and bla(TEM–)(1)(B) genes generally found on the same contigs as the IncF plasmid replicon. Although epidemiologically unrelated, the strains formed three separate sequence type–phylogroup–serotype-specific clusters: C1, C2, and C3. Cluster C1 included five strains (3 to 13 SNPs) belonging to ST167, phylogroup A, and serotype O9:H21; the two C2 strains (11 SNPs) belong to ST156, phylogroup B1, and serotype ONT:H28; and C3 was made up of four strains (SNPs ranged from 4 to 17) of ST636, phylogroup B2, and serotype O45:H7. The common virulence gene gad was reported in all strains. In addition, strains in C2 and C3 possessed iss, lpfA, and nfaE virulence genes, and the vat gene was found only in C3. The present study reports the occurrence of multidrug-resistant ESBL-producing E. coli carrying plasmid-mediated ESBL genes in offshore water and Nile perch in Lake Victoria. Strains formed three clonal clusters of unknown origin. This study reveals that the Lake may serve as reservoir for ESBL-producing bacteria that can be transmitted by fish as a food chain hazard of One-Health concern. Frontiers Media S.A. 2020-02-21 /pmc/articles/PMC7046833/ /pubmed/32153519 http://dx.doi.org/10.3389/fmicb.2020.00108 Text en Copyright © 2020 Baniga, Hounmanou, Kudirkiene, Kusiluka, Mdegela and Dalsgaard. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Baniga, Zebedayo
Hounmanou, Yaovi M. Gildas
Kudirkiene, Egle
Kusiluka, Lughano J. M.
Mdegela, Robinson H.
Dalsgaard, Anders
Genome-Based Analysis of Extended-Spectrum β-Lactamase-Producing Escherichia coli in the Aquatic Environment and Nile Perch (Lates niloticus) of Lake Victoria, Tanzania
title Genome-Based Analysis of Extended-Spectrum β-Lactamase-Producing Escherichia coli in the Aquatic Environment and Nile Perch (Lates niloticus) of Lake Victoria, Tanzania
title_full Genome-Based Analysis of Extended-Spectrum β-Lactamase-Producing Escherichia coli in the Aquatic Environment and Nile Perch (Lates niloticus) of Lake Victoria, Tanzania
title_fullStr Genome-Based Analysis of Extended-Spectrum β-Lactamase-Producing Escherichia coli in the Aquatic Environment and Nile Perch (Lates niloticus) of Lake Victoria, Tanzania
title_full_unstemmed Genome-Based Analysis of Extended-Spectrum β-Lactamase-Producing Escherichia coli in the Aquatic Environment and Nile Perch (Lates niloticus) of Lake Victoria, Tanzania
title_short Genome-Based Analysis of Extended-Spectrum β-Lactamase-Producing Escherichia coli in the Aquatic Environment and Nile Perch (Lates niloticus) of Lake Victoria, Tanzania
title_sort genome-based analysis of extended-spectrum β-lactamase-producing escherichia coli in the aquatic environment and nile perch (lates niloticus) of lake victoria, tanzania
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7046833/
https://www.ncbi.nlm.nih.gov/pubmed/32153519
http://dx.doi.org/10.3389/fmicb.2020.00108
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