Distribution and genomic characterization of tigecycline-resistant tet(X4)-positive Escherichia coli of swine farm origin

Li, Yan; Wang, Qian; Peng, Kai; Liu, Yuan; Xiao, Xia; Mohsin, Mashkoor; Li, Ruichao; Wang, Zhiqiang

doi:10.1099/mgen.0.000667

Cited by 23 publications

(32 citation statements)

References 61 publications

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“…Pigs have been found to be important vehicles of tet (X4)-producing E. coli isolates, which is consistent with the results from previous studies [ 4 , 5 , 8 , 16 ]. Furthermore, the pig tet (X4)-producing E. coli isolates from Shaanxi differed by only 119 SNPs from the human isolates in a previous study from China [ 8 ].…”

Section: Discussionsupporting

confidence: 91%

“…Currently, tet (X4)-producing E. coli isolates have been disseminated in meat products such as pork and chicken, food animals, animal feces, and farm soil [ 3 , 4 , 5 , 6 , 7 ]. In a previous study, tet (X4)-producing E. coli isolates in pigs and chickens accounted for 1.3% and 0.8%, respectively, which was disseminated in five provinces in southern and eastern China including Guangdong, Fujian, Jiangsu, Jiangxi, and Guangxi [ 4 ].…”

Section: Introductionmentioning

confidence: 99%

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International Spread of Tet(X4)-Producing Escherichia coli Isolates

Zhang

Zhan

Shi

2022

Foods

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Tigecycline resistance in bacteria has become a significant threat to food safety and public health, where the development of which is attributed to plasmid-mediated tet(X4) genes. In this study, the genomes of 613 tet(X4)-producing Escherichia coli (E. coli) isolates, available from public databases, are evaluated to determine their international prevalence and molecular characterization. These E. coli isolates have been disseminated in 12 countries across Asia and Europe. It was found that pigs and their products (n = 162) were the most common vehicle, followed by humans (n = 122), chickens (n = 60), and the environment (n = 49). Carbapenems-resistant genes blaNDM-5 (1.3%) and blaNDM-1 (0.2%) were identified, as well as colistin-resistant genes mcr-1.1 (12.6%) and mcr-3.1 (0.5%). It was noted that the tigecycline-resistant gene cluster tmexC-tmexD-toprJ1 was identified in seven (1.1%) isolates. Phylogenomic results indicated that tet(X4)-producing E. coli isolates fell into seven lineages (lineages I, II, III, IV, V, VI, and VII), and international spread mainly occurred in Asian countries, especially China, Pakistan, Singapore, and Malaysia. Four forms of tet(X4) transposon units were found, including the I-type (IS26-tet(X4)-ISCR2), II-type (ΔIS1R-tet(X4)-ISCR2), III-type (ISCR2-tet(X4)-ISCR2), and IV-type (ISCR2-tet(X4)-ΔISCR2). These findings underline further challenges for the spread of E. coli bearing tet(X4) gene.

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Section: Discussionsupporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

International Spread of Tet(X4)-Producing Escherichia coli Isolates

Zhang

Zhan

Shi

2022

Foods

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“…MW423609) from ST761 E. coli isolate SH19PTE6 collected from the same pig farm in 2019 ( Wang et al, 2021 ), and also showed high identity (> 99.7%) to multiple tet (X4)-carrying IncFIA18/IncFIB(K)/IncX1 plasmids from ST761 E. coli strains in China, such as pNT1W22-tetX4 (pig, CP075470), pRF108-2_97k_tetX (pig, MT219820), pSTB20-1T (pig, CP050174), p54-tetX (cow, CP041286), pYPE12-101k-tetX4 (pork, CP041443), and pYPE3-92k-tetX4 (pork, CP041453) ( Figure 2 ). Similar IncFIA18/IncFIB(K)/IncX1 plasmids harboring tet (X4) were also present among other E. coli lineages obtained from a pig farm in Jiangsu province, China ( Li Y. et al, 2021 ), e.g., pNT1N31-tetX4 (ST716, CP075481), pNT1F25-tetX4 (ST1421, CP075471), pNT1F31-tetX4 (ST206, CP045188), pNT1N25-tetX4 (ST641, CP075485), and pNT1F34-tetX (ST10115, CP075486) ( Figure 2 ), highlighting the importance role of horizontal transfer of plasmids in the tet (X4) dissemination between different bacteria.…”

Section: Resultsmentioning

confidence: 72%

“…Thus far, tet (X) and its variants [ tet (X1)∼ tet (X47)] have been identified in Gram-negative pathogens and encode flavin-dependent monooxygenase that modify tigecycline ( Aminov, 2021 ; Li R. et al, 2021 ; Umar et al, 2021 ; Zhang et al, 2021 ). Among them, the mobile tet (X4) gene has been increasingly identified in E. coli from various sources including food-producing animals, wild birds, food products, humans, and the environment, mainly in China ( He et al, 2019 ; Fang et al, 2020 ; Li et al, 2020 ; Li Y. et al, 2021 ; Dong et al, 2022 ; Liu et al, 2022 ). It has sporadically reported in countries outside of China, e.g., Singapore, Pakistan, Vietnam, United Kingdom, and Norway ( Ding et al, 2020 ; Marathe et al, 2021 ; Mohsin et al, 2021 ; Dao et al, 2022 ; Martelli et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

“…Although tigecycline is not applied in livestock, the tet (X4) gene and tigecycline resistance are frequently described in E. coli from food-producing animals (mainly pigs) in China ( He et al, 2019 ; Fang et al, 2020 ; Li Y. et al, 2021 ; Liu et al, 2022 ). The heavy use of tetracyclines in animal production might facilitate the emergence and spread of tet (X) in livestock ( He et al, 2019 ).…”

Section: Introductionmentioning

confidence: 99%

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Tigecycline-resistant Escherichia coli ST761 carrying tet(X4) in a pig farm, China

Wang

et al. 2022

Front. Microbiol.

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This study aimed to investigate the prevalence and characterization of tet(X4) in Escherichia coli isolates from a pig farm in Shanghai, China, and to elucidate tet(X4) dissemination mechanism in this swine farm. Forty-nine (80.33%) E. coli strains were isolated from 61 samples from a pig farm and were screened for the presence of tet(X). Among them, six (12.24%) strains were positive for tet(X4) and exhibited resistance to tigecycline (MIC ≥ 16 mg/L). They were further sequenced by Illumina Hiseq. Six tet(X4)-positive strains belonged to ST761 with identical resistance genes, resistance profiles, plasmid replicons, and cgMLST type except that additional ColE10 plasmid was present in isolate SH21PTE35. Isolate SH21PTE31, as a representative ST761 E. coli strain, was further sequenced using Nanopore MinION. The tet(X4) in SH21PTE31 was located on IncFIA18/IncFIB(K)/IncX1 hybrid plasmid pYUSHP31-1, highly similar to other tet(X4)-carrying IncFIA18/IncFIB(K)/IncX1 plasmids from ST761 E. coli and other E. coli lineages in China. These IncFIA18/IncFIB(K)/IncX1 plasmids shared closely related multidrug resistance regions, and could reorganize, acquire or lose resistance modules mediated by mobile elements such as ISCR2 and IS26. Phylogenetic analysis were performed including all tet(X4)-positive isolates obtained in this pig farm combined with 43 tet(X4)-positive E. coli from pigs, cow, pork, wastewater, and patients with the same ST from NCBI. The 50 tet(X4)-carrying E. coli ST761 isolates from different areas in China shared a close phylogenetic relationship (0-49 SNPs). In conclusion, clonal transmission of tet(X4)-positive E. coli ST761 has occurred in this swine farm. E. coli ST761 has the potential to become a high-risk clone for tet(X4) dissemination in China.

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Development and evaluation of rapid and accurate one-tube RPA-CRISPR-Cas12b-based detection of mcr-1 and tet(X4)

Wang,

Chen,

Pan

et al. 2024

Appl Microbiol Biotechnol

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The emergence and quick spread of the plasmid-mediated tigecycline resistance gene tet(X4) and colistin resistance gene mcr-1 have posed a great threat to public health and raised global concerns. It is imperative to develop rapid and accurate detection systems for the onsite surveillance of mcr-1 and tet(X4). In this study, we developed one-tube recombinase polymerase amplification (RPA) and CRISPR-Cas12b integrated mcr-1 and tet(X4) detection systems. We identified mcr-1- and tet(X4)-conserved and -specific protospacers through a comprehensive BLAST search based on the NCBI nt database and used them for assembling the detection systems. Our developed one-tube RPA-CRISPR-Cas12b-based detection systems enabled the specific detection of mcr-1 and tet(X4) with a sensitivity of 6.25 and 9 copies within a detection time of ~ 55 and ~ 40 min, respectively. The detection results using pork and associated environmental samples collected from retail markets demonstrated that our developed mcr-1 and tet(X4) detection systems could successfully monitor mcr-1 and tet(X4), respectively. Notably, mcr-1- and tet(X4)-positive strains were isolated from the positive samples, as revealed using the developed detection systems. Whole-genome sequencing of representative strains identified an mcr-1-carrying IncI2 plasmid and a tet(X4)-carrying IncFII plasmid, which are known as important vectors for mcr-1 and tet(X4) transmission, respectively. Taken together, our developed one-tube RPA-CRISPR-Cas12b-based mcr-1 and tet(X4) detection systems show promising potential for the onsite detection of mcr-1 and tet(X4). Key points • One-tube RPA-CRISPR-Cas12b-based mcr-1 and tet(X4) detection systems were developed based on identified novel protospacers. • Both detection systems exhibited high sensitivity and specification with a sample-to-answer time of less than 1 h. • The detection systems show promising potential for onsite detection of mcr-1 and tet(X4).

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Distribution and genomic characterization of tigecycline-resistant tet(X4)-positive Escherichia coli of swine farm origin

Cited by 23 publications

References 61 publications

International Spread of Tet(X4)-Producing Escherichia coli Isolates

International Spread of Tet(X4)-Producing Escherichia coli Isolates

Tigecycline-resistant Escherichia coli ST761 carrying tet(X4) in a pig farm, China

Development and evaluation of rapid and accurate one-tube RPA-CRISPR-Cas12b-based detection of mcr-1 and tet(X4)

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