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Article

Whole Genome Analysis of Proteus mirabilis in a Poultry Breeder Farm Reveals the Dissemination of blaNDM and blaCTX-M Mediated by Diverse Mobile Genetic Elements

by
Haibin Hu
1,†,
Ke Wu
1,†,
Tiejun Zhang
1,
Yuhuan Mou
1,
Luya Liu
1,
Xiaoqin Wang
1,
Wei Xu
1,
Wenping Chen
2,
Xiaojiao Chen
2,
Hongning Wang
1 and
Changwei Lei
1,*
1
Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, Animal Disease Prevention and Food Safety Key Laboratory of Sichuan Province, College of Life Sciences, Sichuan University, Chengdu 610065, China
2
Beijing Huadu Yukou Poultry Industry Co., Ltd., Beijing 101206, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agriculture 2025, 15(5), 555; https://doi.org/10.3390/agriculture15050555
Submission received: 27 December 2024 / Revised: 24 February 2025 / Accepted: 3 March 2025 / Published: 5 March 2025
(This article belongs to the Topic Animal Diseases in Agricultural Production Systems: Their Veterinary, Zoonotic, and One Health Importance, 2nd Edition)
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Abstract

:
Proteus mirabilis is a significant foodborne opportunistic pathogen associated with various nosocomial infections. Chicken farms may serve as an important reservoir for P. mirabilis. However, research on antibiotic resistance and genomic features of P. mirabilis in China’s poultry industry is limited. This study isolates P. mirabilis from a breeder farm in China and investigates the dissemination of P. mirabilis and clinically significant antibiotic resistance genes (ARGs), including blaNDM and blaCTX-M. From 510 samples, 69 isolates were obtained, classified into 11 sequence types (STs), with ST135 and ST175 predominating. A total of 39 ARGs were detected, including fosA3, floR, blaCTX-M-3, blaCTX-M-65, and blaNDM-1. Genetic analysis revealed that blaNDM-1 was exclusively located on Salmonella genomic island 1 (SGI1), while blaCTX-M was found in various mobile genetic elements (MGEs), including Tn7, SXT/R391 integrative conjugative elements (ICEs), Proteus mirabilis genomic resistance island 1 (PmGRI1), and SGI1. Notably, many isolates carried multiple MGEs, suggesting frequent horizontal transfer of ARGs in P. mirabilis. These findings underscore the role of P. mirabilis in carrying and spreading antibiotic resistance, posing significant risks to the poultry industry and public health.

1. Introduction

Proteus mirabilis is a Gram-negative bacillus known for its motility, urease production, and hydrogen sulfide production [1,2,3,4]. This bacterium is commonly found in various environments, including soil, sewage, and water sources, as well as in the gastrointestinal tracts of both humans and animals [5]. P. mirabilis is a significant opportunistic pathogen responsible for a wide range of nosocomial infections, including those affecting the respiratory tract, eyes, ears, nose, skin, burns, throat, and wounds [4].
Antimicrobial resistance (AMR) is a critical global public health issue. Antibiotic resistance in several pathogenic bacteria, including Escherichia coli and Clostridium perfringens, poses a huge threat to public health [6,7,8]. Projections estimate that antimicrobial-resistant bacteria could cause over 39 million deaths globally within the next 25 years [9]. Enterobacterales bacteria, such as P. mirabilis, that produce extended-spectrum β-lactamases (ESBLs) are considered one of the critical priority pathogens by the World Health Organization (WHO) [10]. ESBLs are a group of β-lactamases capable of hydrolyzing penicillin, and first-, second-, and third-generation cephalosporins, with blaCTX-M being one of the key genes encoding these enzymes [11]. Carbapenems are effective in treating infections caused by ESBL-producing bacteria [12]. According to the WHO 2024 Bacterial Priority Pathogens List, carbapenem-resistant Enterobacterales remain a critical threat to public health [10].
Farm animals are recognized as a critical reservoir of antibiotic resistance due to the widespread use of antimicrobial agents in domestic breeding. Previous studies have reported clinical P. mirabilis isolates carrying the blaNDM-1 gene in Brazil, Europe, and China [13,14,15]. Additionally, blaNDM-positive P. mirabilis isolates have also been found in wild animals in China [16,17]. However, data on the prevalence and genomic characteristics of P. mirabilis carrying blaNDM-1 and blaCTX-M within the poultry industry is still lacking. In this study, we investigated the prevalence and AMR profiles of P. mirabilis in a breeder farm in China and employed whole-genome sequencing (WGS) to analyze the genetic context of key ARGs. The findings highlight the significant role of P. mirabilis in the dissemination of antibiotic resistance within the poultry industry.

2. Materials and Methods

2.1. Sample Collection and Identification of P. mirabilis

From 1 March to 15 April 2023, a total of 510 samples were collected from a breeder farm in China, consisting of 300 cloacal swabs, 100 dead embryos, 50 liver tissues from deceased chickens, 30 feed samples, and 30 drinking water samples. The samples were pre-enriched in Luria–Bertani (LB) liquid medium at 37 °C for 16 h, then sub-cultured onto LB agar plates. Strains exhibiting migratory growth were selected and streaked onto Salmonella-Shigella agar plates and then incubated at 37 °C for 16 h to purify the isolates. Suspected strains were then identified using 16S rRNA gene sequencing.

2.2. Antimicrobial Susceptibility Testing

Antimicrobial susceptibility testing was performed using the Kirby–Bauer disk diffusion method according to the 2024 guidelines issued by the Clinical and Laboratory Standards Institute: https://clsi.org/standards/products/microbiology/documents/m100/ (accessed on 12 April 2024). Susceptibilities to 12 antimicrobial agents, including colistin sulfate (CST), azithromycin (AZM), trimethoprim-sulfamethoxazole (SXT), cefazolin (CFZ), cefazolin (CTX), florfenicol (FFC), chloramphenicol (CHL), ciprofloxacin (CIP), imipenem (IMP), tetracycline (TET), gentamicin (GEN), and Amikacin (AMK), were tested. Escherichia coli ATCC25922 is used as quality control. Multidrug resistance (MDR) is defined as resistance to more than three chemical classes of antimicrobials.

2.3. Whole Genome Sequencing and Bioinformatics Analysis

Genomic DNA of the isolates was extracted using a bacterial genomic DNA extraction kit (Tiangen, China). WGS was performed on the Illumina HiSeq platform, generating 150 bp paired-end reads. Clean reads were obtained using fastp v0.24: https://github.com/OpenGene/fastp (accessed on 23 April 2024). Clean reads were assembled into draft genomes using SPAdes v3.15.4: https://github.com/ablab/spades (accessed on 28 April 2024). ARGs were identified using ResFinder 4.1.1 [18], and single nucleotide polymorphisms (SNPs) were called from the P. mirabilis genomes using snippy 4.6.0, and phylogenetic trees based on concatenated alignments of high-quality SNPs were constructed using CSI Phylogeny 1.42: https://cge.food.dtu.dk/services/CSIPhylogeny/ (accessed on 1 May 2024). A threshold of 10 SNPs or less between isolates was considered indicative of a clonal relationship. The sequence types (STs) were identified using PubMLST [19]. The phylogenetic tree was visualized and modified in iTOL: https://itol.embl.de/ (accessed on 12 May 2024).

2.4. Genetic Environment Analysis of blaCTX-M and blaNDM

To determine the MGEs associated with the blaNDM-1 and blaCTX-M genes, the P. mirabilis isolates carrying the blaNDM-1 and blaCTX-M genes were further sequenced using the Nanopore MinION rapid sequencing kit (Oxford Nanopore Technologies, Oxford, United Kingdom). Nanopore sequencing data were combined with Illumina data and assembled into complete genomes using Unicycler v0.5.0:https://github.com/rrwick/Unicycler (accessed on 14 August 2024). Genomes were aligned using Snippy v4.6.0: https://github.com/tseemann/snippy (accessed on 3 September 2024). The genetic context of blaCTX-M and blaNDM-1 was examined using Easyfig v2.2.2.5: https://mjsull.github.io/Easyfig/ (accessed on 10 October 2024).

3. Results

3.1. Isolation and Antibiotic Resistance of P. mirabilis

From 510 samples, 69 P. mirabilis isolates were obtained (Table S1), with isolation rates varying by source: cloacal swabs (14.7%, 44/300), dead embryos (20%, 20/100), liver tissues (6%, 3/50), and feed samples (6.7%, 2/30). No isolates were detected in drinking water samples (0/30). The overall isolation rate was 13.53%.
The antimicrobial susceptibility testing revealed that all 69 P. mirabilis isolates were MDR, displaying high resistance rates to various antibiotics. Specifically, the isolates showed resistance to CST (100%), TET (100%), AZM (98.5%), SXT (81.5%), CFZ (69.2%), CTX (68.1%), FFC (49.2%), CHL (43.1%), CIP (43.1%), IMP (33.8%), GEN (26.2%), and AMK (20%). In contrast, resistance rates to antibiotics such as CAZ, IPM, and AMK were comparatively lower (Figure 1a).

3.2. ARGs of P. mirabilis Isolates

A total of 39 ARGs were identified among the isolates (Figure 1b). The sulfonamide resistance gene sul1 and fosfomycin resistance gene fosA3 were detected in 68 (98.6%) and 63 (91.3%) isolates, respectively. Notably, the ESBL gene blaCTX-M-65 was detected in 13 (18.84%) isolates, and the 3 P. mirabilis isolates from liver samples carried the carbapenem resistance gene blaNDM-1. The detection results of ARGs across isolates of different STs are presented in Figure 2.

3.3. Phylogeny Analysis of P. mirabilis Isolates

MLST indicated that the 69 strains were categorized into 11 sequence types (STs). Specifically, 16 strains were identified as ST135, predominantly originating from dead embryo samples, while two strains were obtained from cloacal swabs. Likewise, 16 strains were categorized as ST175, and nearly all of them were sourced from cloacal swabs. In addition, 14 strains were assigned to ST208 and 12 strains to ST508, both of which were solely derived from cloacal swabs. It is worth noting that the three strains of ST820 obtained from liver samples were the sole STs carrying the blaNDM-1 gene identified in the present study.
To investigate the potential transmission of P. mirabilis in the breeder farm, we performed phylogenetic analysis on the P. mirabilis isolates based on the core-genome SNPs (Figure 3). The isolates with the same STs gathered together in the maximum-likelihood tree. In addition, several clonal clusters (SNPs < 10) were identified (marked by Ⅰ to Ⅷ in the maximum-likelihood tree), suggesting the probable clonal dissemination of P. mirabilis within the breeder farm.

3.4. Genetic Environments of blaCTX-M and blaNDM

Genetic environments of clinically important antimicrobial resistance genes blaCTX-M and blaNDM were characterized by long/short read hybrid assemblies and BLAST analysis https://blast.ncbi.nlm.nih.gov/Blast.cgi, which showed that those genes were located on diverse MGEs including Tn7 transposon, SXT/R391 ICEs, PmGRI1, and SGI1 (Figure 4 and Figure 5).
It was found that the blaCTX-M-65 gene was located within the Tn7 region (58,504 bp) in isolate 3_1_YK_14, which harbored 20 ARGs (Figure 4a). This Tn7 region shared a 91% sequence identity with the Tn7 region of P. mirabilis MPE5139 (GenBank accession number CP053684) that was isolated from Guangdong, China. Notably, the Tn7 in P. mirabilis 3_1_YK_14 contained two additional ARGs, blaCTX-M-65, and fosA3, but lacked aph(4)-Ia and aac(3)-IV compared to MPE5139 Tn7 (Figure 4a).
The blaCTX-M-65 gene in isolates 3_1_YK_20, 4_15_YK_45-1 and 3_1_YK_11 was located on SXT/R391 ICEs (Figure 4b). ICEPmiChnYK_20 was 121,980 bp in size and harbored 16 ARGs, including fosA3, floR, and blaCTX-M-65. These ARGs are located in the HS4 hotspot, with no insertions observed in the VRIII region. Compared to ICEPmiChnYK_20, ICEPmiChnYK45_1 (127,149 bp) lacked hotspot HS1, and hotspot HS5 was replaced by chromosomal DNA. Additionally, ICEPmiChnYK45_1 contained a large region similar to ICEPmiChnYK_20 that was inserted in HS4. Another related ICE, ICEPmiChnYK_11 (129,189 bp), harbored blaCTX-M-65, floR, and fosA3, but it only showed similarity to ICEPmiChnYK45_1 at the ends and middle sections. The VRIII region was absent in ICEPmiChnYK_11, with the remaining sequence replaced by chromosomal DNA (Figure 4b).
Furthermore, blaCTX-M-65 was located on the PmGRI1 region in isolates 3_1_YK_19_2 and 3_1_YK_1 (Figure 4c). In 3_1_YK_19_2, the PmGRI1 region spanned 28,464 bp, containing nine ARGs. The blaCTX-M-65 was located between IS26 and IS903B elements, while fosA3 was flanked by two IS26 elements. Compared to PmGRI1 (GenBank accession number MW699444) in YN8 from Sichuan, China, PmGRI1 in 3_1_YK_19_2 lost a significant portion of its characteristic genes, including catA1. In contrast, the PmGRI1 region in 3_1_YK_1 spanned 140,504 bp and harbored 34 ARGs, making it the most complex PmGRI1 structure identified among these isolates. This complexity is likely a result of a double Tn21 transposition event, which subsequently led to the insertion of a 104,227 bp SXT/R391 ICE fragment into the PmGRI1 region (Figure 4c).
The blaNDM-1 gene in isolate 4_15_YK_Y2-1 was identified within the SGI1 element named SGI1-YK_2 (Figure 5). SGI1-YK_2 was 42,497 bp in size, harbored nine ARGs including blaNDM-1, and shared 99% sequence identity with SGI1-JZ109 (GenBank accession number ON553415) in P. mirabilis JZ109 from a market in Sichuan, China. Notably, blaCTX-M-3 was also found in the SGI1 variant (SGI1-YK12_1) in isolate 4_15_YK_12-1; SGI1-YK12_1 was 65,050 bp in size and carried 11 ARGs including floR. SGI1-YK12_1 shared the same SGI1 backbone with SGI1-YK_2. Compared to SGI1-YK_2, SGI1-YK12_1 displayed a more complex genetic structure, including seven copies of IS26 (Figure 5).

4. Discussion

P. mirabilis is an important opportunistic pathogen of humans and animals, posing threats to domestic breeding, food safety, and public health [20]. Recently, outbreaks of P. mirabilis infections have been reported in large-scale breeder farms, presenting substantial challenges to the poultry breeding industry [21,22]. Based on WGS, we investigated the prevalence, antibiotic resistance, and genomic characteristics of P. mirabilis in a breeder farm in China. Our study highlighted that P. mirabilis in breeder farms serves as a potential reservoir for clinically critical carbapenem and cephalosporin resistance genes (blaNDM and blaCTX-M), which are disseminated through diverse MGEs. The high prevalence of MDR P. mirabilis and the detection of blaNDM-1 and blaCTX-M across multiple sequence types (ST135 in dead embryos, ST175 in cloacal swabs, and ST820) suggest potential pathways for resistance gene dissemination within intensive farming systems.
Notably, the detection of blaNDM-1-carrying ST820 isolates in liver tissues highlights a potential zoonotic pathway, as resistant strains may enter the food chain through contaminated poultry products. The poultry industry’s reliance on prophylactic antibiotics, particularly β-lactams and tetracyclines, likely drives the selection and persistence of MDR strains carrying blaCTX-M and tet genes, as observed in our resistance profiles (high resistance to β-lactams and tetracyclines). These findings call for urgent reforms in antimicrobial stewardship, including stricter regulations on non-therapeutic antibiotic use and enhanced surveillance of resistance gene dynamics in farm environments.
All P. mirabilis isolates in this study were MDR and carried complex ARG profiles, including blaNDM-1 and blaCTX-M. The genetic linkage of blaNDM-1 and blaCTX-M to MGEs such as SGI1, Tn7, and SXT/R391 ICEs suggested that these elements might facilitate horizontal gene transfer (HGT) between P. mirabilis and other Enterobacteriaceae including Salmonella [23]. Several mediators, such as flies, eggs, and meat, can lead to the horizontal transfer of antibiotic resistance from animals to humans [17]. The detection of clinically significant ARGs in breeder farms highlights potential public health risks, particularly concerning the zoonotic transmission of resistant P. mirabilis strains from animals to humans, underscoring the urgent need for implementing effective antimicrobial resistance control measures.

5. Conclusions

Our study demonstrates that multidrug-resistant P. mirabilis is widespread in the breeder farm. These isolates harbor a range of clinically significant ARGs, including blaNDM and blaCTX-M, which pose a serious threat to public health. The ARGs are closely associated with various MGEs. Continuous monitoring and control measures are essential to mitigate this risk.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agriculture15050555/s1, Table S1: Information of the 69 strains.

Author Contributions

Conceptualization, H.H., H.W. and C.L.; data curation, H.W. and C.L.; formal analysis, T.Z., Y.M., L.L. and W.X.; funding acquisition, C.L.; investigation, W.C. and X.C.; methodology, H.H., K.W., Y.M., L.L. and X.W.; resources, W.C. and X.C.; software, K.W., T.Z., X.W. and W.X.; writing—original draft, H.H., K.W. and C.L.; writing—review and editing, K.W., H.W. and C.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (32100147), the Natural Science Foundation of Sichuan Province (grant number 2025ZNSFSC0209), and the earmarked fund for China Agriculture Research System (CARS-40-K14).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The WGS data of 69 P. mirabilis strains have been deposited in National Center for Biotechnology Information under BioProject number PRJNA1198800. The nucleotide sequences of the eight genetic elements have been deposited in GenBank under accession numbers PQ682447 and PQ768528-PQ768534.

Conflicts of Interest

Authors Wenping Chen and Xiaojiao Chen were employed by the company Beijing Huadu Yukou Poultry Industry Co., Ltd. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The authors declare no conflicts of interest.

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Agriculture 15 00555 g001
Figure 1. Antibiotic resistance and antibiotic resistance genes (ARGs) of the P. mirabilis isolates. (a) Antibiotic resistance against the selected antimicrobial agents. (b) ARGs in the isolates, including aminoglycoside resistance genes aac(3)-IV, aac(3)-lld, aadA1, aadA2, aadA2b, aadA3, aadA5, aph(3″)-Ⅰb, aph(3′)-Ia, aph(3′)-VIa, aph(4)-Ⅰa, and aph(6)-Id; aminoglycoside and quinolone resistance genes aac(6′)-Ib-cr; rifampin resistance gene ARR-3; cephalosporin resistance genes blaCTX-M-3 and blaCTX-M-65; carbapenem resistance gene blaNDM-1; beta-lactam resistance genes blaOXA-1 and blaTEM-1B; bleomycin resistance gene bleO; chloramphenicol resistance genes catB3, cmlA1, and floR; trimethoprim resistance genes dfrA1, dfrA12, dfrA17, and dfrA32; macrolide resistance genes erm(42), ere(A), mph(E), and msr(E); fosfomycin resistance gene fosA3; lincosamide resistance gene lnu(F); quinolone resistance gene qnrD1; sulfonamide resistance genes sul1, sul2, and sul3; and tetracycline resistance genes tet(A) and tet(C).
Figure 1. Antibiotic resistance and antibiotic resistance genes (ARGs) of the P. mirabilis isolates. (a) Antibiotic resistance against the selected antimicrobial agents. (b) ARGs in the isolates, including aminoglycoside resistance genes aac(3)-IV, aac(3)-lld, aadA1, aadA2, aadA2b, aadA3, aadA5, aph(3″)-Ⅰb, aph(3′)-Ia, aph(3′)-VIa, aph(4)-Ⅰa, and aph(6)-Id; aminoglycoside and quinolone resistance genes aac(6′)-Ib-cr; rifampin resistance gene ARR-3; cephalosporin resistance genes blaCTX-M-3 and blaCTX-M-65; carbapenem resistance gene blaNDM-1; beta-lactam resistance genes blaOXA-1 and blaTEM-1B; bleomycin resistance gene bleO; chloramphenicol resistance genes catB3, cmlA1, and floR; trimethoprim resistance genes dfrA1, dfrA12, dfrA17, and dfrA32; macrolide resistance genes erm(42), ere(A), mph(E), and msr(E); fosfomycin resistance gene fosA3; lincosamide resistance gene lnu(F); quinolone resistance gene qnrD1; sulfonamide resistance genes sul1, sul2, and sul3; and tetracycline resistance genes tet(A) and tet(C).
Agriculture 15 00555 g001
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Figure 2. Detection results of ARGs in the P. mirabilis isolates of different STs and isolation sources. The black squares indicate the presence of ARGs. The dendrograms on the left and top sides of the heatmap show hierarchical clustering of the isolates and ARGs, respectively.
Figure 2. Detection results of ARGs in the P. mirabilis isolates of different STs and isolation sources. The black squares indicate the presence of ARGs. The dendrograms on the left and top sides of the heatmap show hierarchical clustering of the isolates and ARGs, respectively.
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Figure 3. Phylogenetic analysis of 69 P. mirabilis strains: the origin, ST, and presence of key ARGs are represented using different colors. The clonal clusters (SNPs ≤ 10) are designated as I–VIII.
Figure 3. Phylogenetic analysis of 69 P. mirabilis strains: the origin, ST, and presence of key ARGs are represented using different colors. The clonal clusters (SNPs ≤ 10) are designated as I–VIII.
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Figure 4. Genetic environments of blaCTX-M-65, including its association with Tn7 transposons (a), SXT/R391 ICEs (b), and PmGRI1 (c) in P. mirabilis isolates. ORFs are depicted as arrows, with arrowheads indicating the direction of transcription. Integrase genes, resistance genes, and transposase genes are highlighted in yellow, red, and blue, respectively. Regions with >85% nucleotide sequence identity are shaded in gray. HS1 to HS5 denote hotspots 1 to 5, and VRIII represents variable region III within the SXT/R391 integrative conjugative element (ICE). Direct repeats at the ends of genetic elements are labeled as DR-L and DR-R.
Figure 4. Genetic environments of blaCTX-M-65, including its association with Tn7 transposons (a), SXT/R391 ICEs (b), and PmGRI1 (c) in P. mirabilis isolates. ORFs are depicted as arrows, with arrowheads indicating the direction of transcription. Integrase genes, resistance genes, and transposase genes are highlighted in yellow, red, and blue, respectively. Regions with >85% nucleotide sequence identity are shaded in gray. HS1 to HS5 denote hotspots 1 to 5, and VRIII represents variable region III within the SXT/R391 integrative conjugative element (ICE). Direct repeats at the ends of genetic elements are labeled as DR-L and DR-R.
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Figure 5. Genetic environments of clinically important ARGs blaNDM-1 and blaCTX-M-3 associated with SGI1 variants in P. mirabilis isolates. Genes and ORFs are depicted as arrows, with arrowheads indicating the direction of transcription. Integrase genes, resistance genes, and transposase genes are highlighted in yellow, red, and blue, respectively. Regions with >85% nucleotide sequence identity are shaded in gray. Direct repeats at the ends of genetic elements are labeled as DR-L and DR-R.
Figure 5. Genetic environments of clinically important ARGs blaNDM-1 and blaCTX-M-3 associated with SGI1 variants in P. mirabilis isolates. Genes and ORFs are depicted as arrows, with arrowheads indicating the direction of transcription. Integrase genes, resistance genes, and transposase genes are highlighted in yellow, red, and blue, respectively. Regions with >85% nucleotide sequence identity are shaded in gray. Direct repeats at the ends of genetic elements are labeled as DR-L and DR-R.
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MDPI and ACS Style

Hu, H.; Wu, K.; Zhang, T.; Mou, Y.; Liu, L.; Wang, X.; Xu, W.; Chen, W.; Chen, X.; Wang, H.; et al. Whole Genome Analysis of Proteus mirabilis in a Poultry Breeder Farm Reveals the Dissemination of blaNDM and blaCTX-M Mediated by Diverse Mobile Genetic Elements. Agriculture 2025, 15, 555. https://doi.org/10.3390/agriculture15050555

AMA Style

Hu H, Wu K, Zhang T, Mou Y, Liu L, Wang X, Xu W, Chen W, Chen X, Wang H, et al. Whole Genome Analysis of Proteus mirabilis in a Poultry Breeder Farm Reveals the Dissemination of blaNDM and blaCTX-M Mediated by Diverse Mobile Genetic Elements. Agriculture. 2025; 15(5):555. https://doi.org/10.3390/agriculture15050555

Chicago/Turabian Style

Hu, Haibin, Ke Wu, Tiejun Zhang, Yuhuan Mou, Luya Liu, Xiaoqin Wang, Wei Xu, Wenping Chen, Xiaojiao Chen, Hongning Wang, and et al. 2025. "Whole Genome Analysis of Proteus mirabilis in a Poultry Breeder Farm Reveals the Dissemination of blaNDM and blaCTX-M Mediated by Diverse Mobile Genetic Elements" Agriculture 15, no. 5: 555. https://doi.org/10.3390/agriculture15050555

APA Style

Hu, H., Wu, K., Zhang, T., Mou, Y., Liu, L., Wang, X., Xu, W., Chen, W., Chen, X., Wang, H., & Lei, C. (2025). Whole Genome Analysis of Proteus mirabilis in a Poultry Breeder Farm Reveals the Dissemination of blaNDM and blaCTX-M Mediated by Diverse Mobile Genetic Elements. Agriculture, 15(5), 555. https://doi.org/10.3390/agriculture15050555

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