Genomic Insights into Carbapenem-Resistant Organisms Producing New Delhi Metallo-β-Lactamase in Live Poultry Markets

New Delhi metallo-β-lactamase (NDM) is an enzyme that can degrade a wide range of β-lactam antibiotics. The widespread dissemination of the <i>bla</i><sub>NDM</sub> gene, which encodes NDM, in animal-derived settings poses a threat to public health security. Live poultry mark...

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Main Authors: Xueqiang Xin, Yi Yin, Jiayong Kong, Mianzhi Wang, Zhiqiang Wang, Ruichao Li
Format: Article
Language:English
Published: MDPI AG 2025-05-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/13/6/1195
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author Xueqiang Xin
Yi Yin
Jiayong Kong
Mianzhi Wang
Zhiqiang Wang
Ruichao Li
author_facet Xueqiang Xin
Yi Yin
Jiayong Kong
Mianzhi Wang
Zhiqiang Wang
Ruichao Li
author_sort Xueqiang Xin
collection DOAJ
description New Delhi metallo-β-lactamase (NDM) is an enzyme that can degrade a wide range of β-lactam antibiotics. The widespread dissemination of the <i>bla</i><sub>NDM</sub> gene, which encodes NDM, in animal-derived settings poses a threat to public health security. Live poultry markets represent critical nodes in public health surveillance. However, there is currently limited reporting on the spread of the <i>bla</i><sub>NDM</sub> gene within these markets under the One Health approach. This study investigated the prevalence of the <i>bla</i><sub>NDM</sub> gene in live poultry markets and, by integrating newly sequenced genomes with publicly available database entries, performed an in-depth analysis of its association networks with other genetic elements across species. A total of 233 <i>bla</i><sub>NDM</sub>-positive strains, comprising 218 <i>Escherichia coli</i> strains, 4 <i>Enterobacter cloacae</i> strains, 7 <i>Klebsiella pneumoniae</i>, 2 <i>Klebsiella aerogenes</i>, 1 <i>Providencia rettgeri</i>, and 1 <i>Proteus mirabilis</i> were isolated from two live poultry markets in Jiangsu, China. Among the <i>bla</i><sub>NDM</sub>-positive strains, multiple variants were identified, primarily <i>bla</i><sub>NDM-5</sub>, followed by <i>bla</i><sub>NDM-1</sub>, <i>bla</i><sub>NDM-13</sub>, <i>bla</i><sub>NDM-27</sub>, and <i>bla</i><sub>NDM-39</sub>. The coexistence of <i>bla</i><sub>NDM-5</sub> and <i>mcr-1</i> was detected in five <i>E. coli</i> strains. Additionally, we found one <i>E. coli</i> strain in which <i>bla</i><sub>NDM-5</sub> coexisted with <i>estT</i> and <i>tet</i>(X4), and another <i>E. coli</i> strain where <i>bla</i><sub>NDM-5</sub> coexisted with <i>estT</i>. Spearman correlation analysis of publicly available genomes revealed that the genetic element preferences of <i>bla</i><sub>NDM</sub> variants vary significantly across species (|R| > 0.3, <i>p</i> < 0.05). The element preferences of <i>E. coli</i> strains carrying <i>bla</i><sub>NDM-5</sub> are similar to those of <i>Klebsiella pneumoniae</i> harboring <i>bla</i><sub>NDM-1</sub>. In <i>Klebsiella aerogenes</i>, <i>Enterobacter cloacae</i>, and <i>Proteus mirabilis</i>, strains carrying <i>bla</i><sub>NDM-1</sub>, have opposite genetic element preferences when compared with strains harboring <i>bla</i><sub>NDM-5</sub> or <i>bla</i><sub>NDM-7</sub>. Notably, we report the first evidence of the <i>bla</i><sub>NDM-1</sub> gene transfer mediated by IS<i>Kpn13</i>, IS<i>Spu2</i>, and MITE<i>Kpn1</i>. The findings highlight that live poultry markets are important transmission hotspots of AMR and thus require continuous surveillance.
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spelling doaj-art-c10d8c11af04457980b058ff92f74f522025-08-20T03:29:35ZengMDPI AGMicroorganisms2076-26072025-05-01136119510.3390/microorganisms13061195Genomic Insights into Carbapenem-Resistant Organisms Producing New Delhi Metallo-β-Lactamase in Live Poultry MarketsXueqiang Xin0Yi Yin1Jiayong Kong2Mianzhi Wang3Zhiqiang Wang4Ruichao Li5Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaNew Delhi metallo-β-lactamase (NDM) is an enzyme that can degrade a wide range of β-lactam antibiotics. The widespread dissemination of the <i>bla</i><sub>NDM</sub> gene, which encodes NDM, in animal-derived settings poses a threat to public health security. Live poultry markets represent critical nodes in public health surveillance. However, there is currently limited reporting on the spread of the <i>bla</i><sub>NDM</sub> gene within these markets under the One Health approach. This study investigated the prevalence of the <i>bla</i><sub>NDM</sub> gene in live poultry markets and, by integrating newly sequenced genomes with publicly available database entries, performed an in-depth analysis of its association networks with other genetic elements across species. A total of 233 <i>bla</i><sub>NDM</sub>-positive strains, comprising 218 <i>Escherichia coli</i> strains, 4 <i>Enterobacter cloacae</i> strains, 7 <i>Klebsiella pneumoniae</i>, 2 <i>Klebsiella aerogenes</i>, 1 <i>Providencia rettgeri</i>, and 1 <i>Proteus mirabilis</i> were isolated from two live poultry markets in Jiangsu, China. Among the <i>bla</i><sub>NDM</sub>-positive strains, multiple variants were identified, primarily <i>bla</i><sub>NDM-5</sub>, followed by <i>bla</i><sub>NDM-1</sub>, <i>bla</i><sub>NDM-13</sub>, <i>bla</i><sub>NDM-27</sub>, and <i>bla</i><sub>NDM-39</sub>. The coexistence of <i>bla</i><sub>NDM-5</sub> and <i>mcr-1</i> was detected in five <i>E. coli</i> strains. Additionally, we found one <i>E. coli</i> strain in which <i>bla</i><sub>NDM-5</sub> coexisted with <i>estT</i> and <i>tet</i>(X4), and another <i>E. coli</i> strain where <i>bla</i><sub>NDM-5</sub> coexisted with <i>estT</i>. Spearman correlation analysis of publicly available genomes revealed that the genetic element preferences of <i>bla</i><sub>NDM</sub> variants vary significantly across species (|R| > 0.3, <i>p</i> < 0.05). The element preferences of <i>E. coli</i> strains carrying <i>bla</i><sub>NDM-5</sub> are similar to those of <i>Klebsiella pneumoniae</i> harboring <i>bla</i><sub>NDM-1</sub>. In <i>Klebsiella aerogenes</i>, <i>Enterobacter cloacae</i>, and <i>Proteus mirabilis</i>, strains carrying <i>bla</i><sub>NDM-1</sub>, have opposite genetic element preferences when compared with strains harboring <i>bla</i><sub>NDM-5</sub> or <i>bla</i><sub>NDM-7</sub>. Notably, we report the first evidence of the <i>bla</i><sub>NDM-1</sub> gene transfer mediated by IS<i>Kpn13</i>, IS<i>Spu2</i>, and MITE<i>Kpn1</i>. The findings highlight that live poultry markets are important transmission hotspots of AMR and thus require continuous surveillance.https://www.mdpi.com/2076-2607/13/6/1195live poultrycarbapenem resistance<i>bla</i><sub>NDM</sub>genomic analysistransmission
spellingShingle Xueqiang Xin
Yi Yin
Jiayong Kong
Mianzhi Wang
Zhiqiang Wang
Ruichao Li
Genomic Insights into Carbapenem-Resistant Organisms Producing New Delhi Metallo-β-Lactamase in Live Poultry Markets
Microorganisms
live poultry
carbapenem resistance
<i>bla</i><sub>NDM</sub>
genomic analysis
transmission
title Genomic Insights into Carbapenem-Resistant Organisms Producing New Delhi Metallo-β-Lactamase in Live Poultry Markets
title_full Genomic Insights into Carbapenem-Resistant Organisms Producing New Delhi Metallo-β-Lactamase in Live Poultry Markets
title_fullStr Genomic Insights into Carbapenem-Resistant Organisms Producing New Delhi Metallo-β-Lactamase in Live Poultry Markets
title_full_unstemmed Genomic Insights into Carbapenem-Resistant Organisms Producing New Delhi Metallo-β-Lactamase in Live Poultry Markets
title_short Genomic Insights into Carbapenem-Resistant Organisms Producing New Delhi Metallo-β-Lactamase in Live Poultry Markets
title_sort genomic insights into carbapenem resistant organisms producing new delhi metallo β lactamase in live poultry markets
topic live poultry
carbapenem resistance
<i>bla</i><sub>NDM</sub>
genomic analysis
transmission
url https://www.mdpi.com/2076-2607/13/6/1195
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