Prevalence and characterization of IncQ1α-mediated multi-drug resistance in Proteus mirabilis Isolated from pigs in Kunming, Yunnan, China

BackgroundProteus mirabilis is a conditionally pathogenic bacterium that is inherently resistant to polymyxin and tigecycline, largely due to antibiotic resistance genes (ARGs). These ARGs can be horizontally transferred to other bacteria, raising concerns about the Inc plasmid-mediated ARG transmis...

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Main Authors: Hongmei Liu, Na Xia, Fanan Suksawat, Bundit Tengjaroenkul, Yue Hu, Xiaofeng Zhou, Xiaojiang Li, Cuiqin Huang, Yinli Bao, Qiong Wu, Chunrong Zhang, Sunpetch Angkititrakul, Bin Xiang, Xin Wu
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Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1483633/full
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author Hongmei Liu
Hongmei Liu
Hongmei Liu
Na Xia
Fanan Suksawat
Bundit Tengjaroenkul
Yue Hu
Xiaofeng Zhou
Xiaojiang Li
Cuiqin Huang
Yinli Bao
Qiong Wu
Chunrong Zhang
Sunpetch Angkititrakul
Bin Xiang
Xin Wu
author_facet Hongmei Liu
Hongmei Liu
Hongmei Liu
Na Xia
Fanan Suksawat
Bundit Tengjaroenkul
Yue Hu
Xiaofeng Zhou
Xiaojiang Li
Cuiqin Huang
Yinli Bao
Qiong Wu
Chunrong Zhang
Sunpetch Angkititrakul
Bin Xiang
Xin Wu
author_sort Hongmei Liu
collection DOAJ
description BackgroundProteus mirabilis is a conditionally pathogenic bacterium that is inherently resistant to polymyxin and tigecycline, largely due to antibiotic resistance genes (ARGs). These ARGs can be horizontally transferred to other bacteria, raising concerns about the Inc plasmid-mediated ARG transmission from Proteus mirabilis, which poses a serious public health threat. This study aims to investigate the presence of Inc plasmid types in pig-derived Proteus mirabilis in Kunming, Yunnan, China.MethodsFecal samples were collected from pig farms across six districts of Kunming (Luquan, Jinning, Yiliang, Anning, Songming, and Xundian) from 2022 to 2023. Proteus mirabilis isolates were identified using IDS and 16S rRNA gene sequencing. Then, positive strains underwent antimicrobial susceptibility testing and incompatibility plasmid typing. Multi-drug-resistant isolates with positive incompatibility plasmid genes were selected for whole-genome sequencing. Resistance and Inc group data were then isolated and compared with 126 complete genome sequences from public databases. Whole-genome multi-locus sequence typing, resistance group analysis, genomic island prediction, and plasmid structural gene analysis were performed.ResultsA total of 30 isolates were obtained from 230 samples, yielding a prevalence of 13.04%. All isolates exhibited multi-drug resistance, with 100% resistance to cotrimoxazole, erythromycin, penicillin G, chloramphenicol, ampicillin, and streptomycin. Among these, 15 isolates tested positive for the IncQ1α plasmid repC gene. The two most multi-drug-resistant and repC-positive strains, NO. 15 and 21, were sequenced to compare genomic features on Inc groups and ARGs with public data. Genome analysis revealed that the repC gene was primarily associated with IncQ1α, with structural genes from other F-type plasmids (TraV, TraU, TraN, TraL, TraK, TraI, TraH, TraG, TraF, TraE/GumN, and TraA) also present. Strain NO. 15 carried 33 ARGs, and strain NO. 21 carried 38 ARGs, conferring resistance to tetracyclines, fluoroquinolones, aminoglycosides, sulfonamides, peptides, chloramphenicol, cephalosporins, lincomycins, macrolides, and 2-aminopyrimidines.ConclusionThe repC gene is primarily associated with IncQ1α, with structural genes from other F-type plasmids. A comparison with 126 public genome datasets confirmed this association.
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spelling doaj-art-e572dff884464f8da72ec0512a8d8e982025-01-09T06:11:00ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-01-011510.3389/fmicb.2024.14836331483633Prevalence and characterization of IncQ1α-mediated multi-drug resistance in Proteus mirabilis Isolated from pigs in Kunming, Yunnan, ChinaHongmei Liu0Hongmei Liu1Hongmei Liu2Na Xia3Fanan Suksawat4Bundit Tengjaroenkul5Yue Hu6Xiaofeng Zhou7Xiaojiang Li8Cuiqin Huang9Yinli Bao10Qiong Wu11Chunrong Zhang12Sunpetch Angkititrakul13Bin Xiang14Xin Wu15Yunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University, Kunming, ChinaEngineering Research Center for the Prevention and Control of Animal Original Zoonosis of Fujian Province University, College of Life Science, Longyan University, Fujian, ChinaFaculty of Veterinary Medicine, Khon Kaen University, Khon Kaen, ThailandYunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University, Kunming, ChinaFaculty of Veterinary Medicine, Khon Kaen University, Khon Kaen, ThailandFaculty of Veterinary Medicine, Khon Kaen University, Khon Kaen, ThailandYunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University, Kunming, ChinaYunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University, Kunming, ChinaYunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University, Kunming, ChinaEngineering Research Center for the Prevention and Control of Animal Original Zoonosis of Fujian Province University, College of Life Science, Longyan University, Fujian, ChinaEngineering Research Center for the Prevention and Control of Animal Original Zoonosis of Fujian Province University, College of Life Science, Longyan University, Fujian, ChinaEngineering Research Center for the Prevention and Control of Animal Original Zoonosis of Fujian Province University, College of Life Science, Longyan University, Fujian, ChinaEngineering Research Center for the Prevention and Control of Animal Original Zoonosis of Fujian Province University, College of Life Science, Longyan University, Fujian, ChinaFaculty of Veterinary Medicine, Khon Kaen University, Khon Kaen, ThailandYunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University, Kunming, ChinaYunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University, Kunming, ChinaBackgroundProteus mirabilis is a conditionally pathogenic bacterium that is inherently resistant to polymyxin and tigecycline, largely due to antibiotic resistance genes (ARGs). These ARGs can be horizontally transferred to other bacteria, raising concerns about the Inc plasmid-mediated ARG transmission from Proteus mirabilis, which poses a serious public health threat. This study aims to investigate the presence of Inc plasmid types in pig-derived Proteus mirabilis in Kunming, Yunnan, China.MethodsFecal samples were collected from pig farms across six districts of Kunming (Luquan, Jinning, Yiliang, Anning, Songming, and Xundian) from 2022 to 2023. Proteus mirabilis isolates were identified using IDS and 16S rRNA gene sequencing. Then, positive strains underwent antimicrobial susceptibility testing and incompatibility plasmid typing. Multi-drug-resistant isolates with positive incompatibility plasmid genes were selected for whole-genome sequencing. Resistance and Inc group data were then isolated and compared with 126 complete genome sequences from public databases. Whole-genome multi-locus sequence typing, resistance group analysis, genomic island prediction, and plasmid structural gene analysis were performed.ResultsA total of 30 isolates were obtained from 230 samples, yielding a prevalence of 13.04%. All isolates exhibited multi-drug resistance, with 100% resistance to cotrimoxazole, erythromycin, penicillin G, chloramphenicol, ampicillin, and streptomycin. Among these, 15 isolates tested positive for the IncQ1α plasmid repC gene. The two most multi-drug-resistant and repC-positive strains, NO. 15 and 21, were sequenced to compare genomic features on Inc groups and ARGs with public data. Genome analysis revealed that the repC gene was primarily associated with IncQ1α, with structural genes from other F-type plasmids (TraV, TraU, TraN, TraL, TraK, TraI, TraH, TraG, TraF, TraE/GumN, and TraA) also present. Strain NO. 15 carried 33 ARGs, and strain NO. 21 carried 38 ARGs, conferring resistance to tetracyclines, fluoroquinolones, aminoglycosides, sulfonamides, peptides, chloramphenicol, cephalosporins, lincomycins, macrolides, and 2-aminopyrimidines.ConclusionThe repC gene is primarily associated with IncQ1α, with structural genes from other F-type plasmids. A comparison with 126 public genome datasets confirmed this association.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1483633/fullProteus mirabilisantimicrobial resistanceInc plasmidrepC genewhole genome sequence
spellingShingle Hongmei Liu
Hongmei Liu
Hongmei Liu
Na Xia
Fanan Suksawat
Bundit Tengjaroenkul
Yue Hu
Xiaofeng Zhou
Xiaojiang Li
Cuiqin Huang
Yinli Bao
Qiong Wu
Chunrong Zhang
Sunpetch Angkititrakul
Bin Xiang
Xin Wu
Prevalence and characterization of IncQ1α-mediated multi-drug resistance in Proteus mirabilis Isolated from pigs in Kunming, Yunnan, China
Frontiers in Microbiology
Proteus mirabilis
antimicrobial resistance
Inc plasmid
repC gene
whole genome sequence
title Prevalence and characterization of IncQ1α-mediated multi-drug resistance in Proteus mirabilis Isolated from pigs in Kunming, Yunnan, China
title_full Prevalence and characterization of IncQ1α-mediated multi-drug resistance in Proteus mirabilis Isolated from pigs in Kunming, Yunnan, China
title_fullStr Prevalence and characterization of IncQ1α-mediated multi-drug resistance in Proteus mirabilis Isolated from pigs in Kunming, Yunnan, China
title_full_unstemmed Prevalence and characterization of IncQ1α-mediated multi-drug resistance in Proteus mirabilis Isolated from pigs in Kunming, Yunnan, China
title_short Prevalence and characterization of IncQ1α-mediated multi-drug resistance in Proteus mirabilis Isolated from pigs in Kunming, Yunnan, China
title_sort prevalence and characterization of incq1α mediated multi drug resistance in proteus mirabilis isolated from pigs in kunming yunnan china
topic Proteus mirabilis
antimicrobial resistance
Inc plasmid
repC gene
whole genome sequence
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1483633/full
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