ESBL and AmpC β-lactamase encoding genes in E. coli from pig and pig farm workers in Vietnam and their association with mobile genetic elements

Animals are considered important sources of ESBL/AmpC-producing bacteria in humans. We analyzed indications of transfer of ESBL/AmpC genes between pigs and pig farmers in Vietnam by analyzing whole genome sequences of 114 ESBL/AmpC-producing E. coli isolated from the two hosts, and performed conjuga...

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Main Authors: Hounmanou, Yaovi Mahuton Gildas, Bortolaia, Valeria, Dang, Son Thi Thanh, Truong, Duong, Olsen, John E., Dalsgaard, Anders
Other Authors: School of Chemical and Biomedical Engineering
Format: Journal Article
Language:English
Published: 2021
Subjects:
Online Access:https://hdl.handle.net/10356/151775
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author Hounmanou, Yaovi Mahuton Gildas
Bortolaia, Valeria
Dang, Son Thi Thanh
Truong, Duong
Olsen, John E.
Dalsgaard, Anders
author2 School of Chemical and Biomedical Engineering
author_facet School of Chemical and Biomedical Engineering
Hounmanou, Yaovi Mahuton Gildas
Bortolaia, Valeria
Dang, Son Thi Thanh
Truong, Duong
Olsen, John E.
Dalsgaard, Anders
author_sort Hounmanou, Yaovi Mahuton Gildas
collection NTU
description Animals are considered important sources of ESBL/AmpC-producing bacteria in humans. We analyzed indications of transfer of ESBL/AmpC genes between pigs and pig farmers in Vietnam by analyzing whole genome sequences of 114 ESBL/AmpC-producing E. coli isolated from the two hosts, and performed conjugation experiments and plasmid profiling to confirm that such transfer could have happened. ESBL-encoding genes detected in pigs and pig farmers included bla CTX-M-55, bla CTX-M-27, bla CTX-M-65, bla CTX-M-15, bla CTX-M-14, bla CTX-M-3, bla CTX-M-24, and bla CARB-2, and AmpC β-lactamases included bla CMY-2, bla DHA-1, and bla CMY-42. The most frequent ESBL gene, bla CTX-M-55, was carried on plasmid with replicons types IncF, IncX, IncH, IncN, IncR, and IncP. The insertion transposases downstream of the bla CTX-M-55 gene were different in plasmids carried by different strains. The second most detected gene, bla CTX-M-27, is found in a stable genetic arrangement with the same flanking transposons seen across strains, and the gene was located on similar conjugal IncF plasmid types, suggesting a horizontal spread of these plasmids. In three strains, we observed a novel bla CTX-M-27 harboring IncF type of plasmid which had not been reported before. Its closest reference in NCBI was the non-ESBL Salmonella Typhimurium plasmid pB71 that might have experienced an insertion of bla CTX-M-27. Our data also point to an emergence of plasmids co-carrying ESBL genes, mcr genes, quinolones and other antimicrobials resistance determinants, and such plasmids require special attention. Plasmids phylogeny confirmed that the bla CTX-M-55 encoding plasmids varied considerably, while those encoding bla CTX-M-27 were closely related. Plasmids harboring both ESBL genes were confirmed to be conjugative and not to differ in transfer efficacy. The isolates carrying the plasmids, even those with plasmids of similar types, showed wide genetic variation with high number of SNPs, suggesting horizontal spread of plasmids into different clonal lines. Their virulence profiles did not confirm to known pathotypes, suggesting that unrelated commensals are a main reservoir for ESBL and AmpC β-lactamases in both humans and pigs. Overall, despite evidence of transferability of plasmids in the analyzed strains, our findings do not support that ESBL-producing E. coli from pigs or their ESBL/AmpC encoding plasmids are commonly spread to workers in close contact with the animals.
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spelling ntu-10356/1517752023-12-29T06:53:02Z ESBL and AmpC β-lactamase encoding genes in E. coli from pig and pig farm workers in Vietnam and their association with mobile genetic elements Hounmanou, Yaovi Mahuton Gildas Bortolaia, Valeria Dang, Son Thi Thanh Truong, Duong Olsen, John E. Dalsgaard, Anders School of Chemical and Biomedical Engineering Science::Biological sciences Extended-spectrum β-lactamase Mobile Genetic Element Animals are considered important sources of ESBL/AmpC-producing bacteria in humans. We analyzed indications of transfer of ESBL/AmpC genes between pigs and pig farmers in Vietnam by analyzing whole genome sequences of 114 ESBL/AmpC-producing E. coli isolated from the two hosts, and performed conjugation experiments and plasmid profiling to confirm that such transfer could have happened. ESBL-encoding genes detected in pigs and pig farmers included bla CTX-M-55, bla CTX-M-27, bla CTX-M-65, bla CTX-M-15, bla CTX-M-14, bla CTX-M-3, bla CTX-M-24, and bla CARB-2, and AmpC β-lactamases included bla CMY-2, bla DHA-1, and bla CMY-42. The most frequent ESBL gene, bla CTX-M-55, was carried on plasmid with replicons types IncF, IncX, IncH, IncN, IncR, and IncP. The insertion transposases downstream of the bla CTX-M-55 gene were different in plasmids carried by different strains. The second most detected gene, bla CTX-M-27, is found in a stable genetic arrangement with the same flanking transposons seen across strains, and the gene was located on similar conjugal IncF plasmid types, suggesting a horizontal spread of these plasmids. In three strains, we observed a novel bla CTX-M-27 harboring IncF type of plasmid which had not been reported before. Its closest reference in NCBI was the non-ESBL Salmonella Typhimurium plasmid pB71 that might have experienced an insertion of bla CTX-M-27. Our data also point to an emergence of plasmids co-carrying ESBL genes, mcr genes, quinolones and other antimicrobials resistance determinants, and such plasmids require special attention. Plasmids phylogeny confirmed that the bla CTX-M-55 encoding plasmids varied considerably, while those encoding bla CTX-M-27 were closely related. Plasmids harboring both ESBL genes were confirmed to be conjugative and not to differ in transfer efficacy. The isolates carrying the plasmids, even those with plasmids of similar types, showed wide genetic variation with high number of SNPs, suggesting horizontal spread of plasmids into different clonal lines. Their virulence profiles did not confirm to known pathotypes, suggesting that unrelated commensals are a main reservoir for ESBL and AmpC β-lactamases in both humans and pigs. Overall, despite evidence of transferability of plasmids in the analyzed strains, our findings do not support that ESBL-producing E. coli from pigs or their ESBL/AmpC encoding plasmids are commonly spread to workers in close contact with the animals. Published version We acknowledged the financial support from the Danish International Development Assistance (Danida) to the project “Health and Antibiotics in Vietnamese Pig Production” (grant DFC File No. 17-M06-KU). 2021-07-16T09:48:22Z 2021-07-16T09:48:22Z 2021 Journal Article Hounmanou, Y. M. G., Bortolaia, V., Dang, S. T. T., Truong, D., Olsen, J. E. & Dalsgaard, A. (2021). ESBL and AmpC β-lactamase encoding genes in E. coli from pig and pig farm workers in Vietnam and their association with mobile genetic elements. Frontiers in Microbiology, 12, 629139-. https://dx.doi.org/10.3389/fmicb.2021.629139 1664-302X https://hdl.handle.net/10356/151775 10.3389/fmicb.2021.629139 33776959 2-s2.0-85103138923 12 629139 en Frontiers in Microbiology © 2021 Hounmanou, Bortolaia, Dang, Truong, Olsen and Dalsgaard. 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. application/pdf
spellingShingle Science::Biological sciences
Extended-spectrum β-lactamase
Mobile Genetic Element
Hounmanou, Yaovi Mahuton Gildas
Bortolaia, Valeria
Dang, Son Thi Thanh
Truong, Duong
Olsen, John E.
Dalsgaard, Anders
ESBL and AmpC β-lactamase encoding genes in E. coli from pig and pig farm workers in Vietnam and their association with mobile genetic elements
title ESBL and AmpC β-lactamase encoding genes in E. coli from pig and pig farm workers in Vietnam and their association with mobile genetic elements
title_full ESBL and AmpC β-lactamase encoding genes in E. coli from pig and pig farm workers in Vietnam and their association with mobile genetic elements
title_fullStr ESBL and AmpC β-lactamase encoding genes in E. coli from pig and pig farm workers in Vietnam and their association with mobile genetic elements
title_full_unstemmed ESBL and AmpC β-lactamase encoding genes in E. coli from pig and pig farm workers in Vietnam and their association with mobile genetic elements
title_short ESBL and AmpC β-lactamase encoding genes in E. coli from pig and pig farm workers in Vietnam and their association with mobile genetic elements
title_sort esbl and ampc β lactamase encoding genes in e coli from pig and pig farm workers in vietnam and their association with mobile genetic elements
topic Science::Biological sciences
Extended-spectrum β-lactamase
Mobile Genetic Element
url https://hdl.handle.net/10356/151775
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