Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases · 2026
Global phylogeography, genomic characteristics and transmission of antibiotic resistance of multi-drug resistant ORN-1-producing Raoultella ornithinolytica B1645-1B.
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Yu Chunfang, Wang Zuhua, Wu Lingling, Meng Lixue, Liu Long, Sha Longhua, Tuo Juan, Wang Jinlei, Li Jinpeng, Peng ZiJing, Zhang Yunqi, Liu Zhixin, Jin Zhixiong
Аннотация
OBJECTIVE: To characterize the genomic phylogeny and antimicrobial resistance (AMR) genotypes of the ORN-1-producing R. ornithinolytica B16451B, and to elucidate the transfer mechanisms of resistance genes at the genomic level.
METHODS: The genome of R. ornithinolytica B16451B was sequenced using the Illumina HiSeq 4000 and PacBio RSII sequencing platforms. A global phylogenetic analysis of the genomic data was conducted by the Center for Genomic Epidemiology (CGE), incorporating information on geographical distribution, isolation sources, and host associations. A comparative phylogenomic analysis was performed using the BLAST Ring Image Generator (BRIG). Genome annotation was performed using Glimmer and the Rapid Annotation using Subsystem Technology (RAST) server. Mobile genetic elements were predicted using TnCentral, ISFinder, and PHASTER. The antibiotic resistance genes (ARGs) were analyzed using the Comprehensive Antibiotic Resistance Database (CARD), while the virulence factors genes (VFGs) were analyzed using the Virulence Factor Database (VFDB). Gene transfer experiments were conducted in the intestinal tract of mice. Transconjugants were identified using 16S rRNA metagenomic sequencing, and drug-resistance genes were amplified by PCR.
RESULTS: A chromosome (designated chromosome 01) was first identified in strain B16451B. A carrying IS4 insertion sequence distinct resistance region within this chromosome, designated B1645-1B-RG, harbors the β-lactamase gene blaORN-1. Three intact prophages, designated prophage YC1, YC2, and YC3, were also first identified. The blaORN-1 gene was successfully transferred from strain B16451B to Escherichia coli (designated B1645-1BLMY1) and Klebsiella pneumoniae (designated B1645-1BYCF2) in the intestines of mice. The strain B16451B harbored 25 antimicrobial resistance genes and 8 classes of virulence factor genes. Based on comparative genomic analysis of strains retrieved from the NCBI Genome Database, 98 antimicrobial resistance genes (ARGs) (e.g., sul1, blaKPC-2, blaNDM-1) among 234 R. ornithinolytica strains were identified to exhibit significantly higher prevalence in human isolates than in non-human host sources (e.g., water, animals, plants).
CONCLUSIONS: The chromosome 01 was identified in a multi-drug resistant ORN-1-producing the strain B16451B isolated from China. The genome of strain B16451B harbors three integrated prophages: YC1 (42.2 kb), YC2 (60.5 kb), and YC3 (23.8 kb) was identified. The IS4 insertion might promote blaORN-1 gene transfer within the intestinal flora of mice. Among these 234 R. ornithinolytica strains analyzed in this study, most virulence factor genes (e.g., ompa, yagx/ecpc) and resistance genes (e.g., blaKPC, blaNDM) exhibited higher prevalence in Homo sapiens isolates than in strains from non-human sources including water, animals and plants. These findings provide valuable references for clinicians optimize the management of R. ornithinolytica infections and guide clinical treatment.
METHODS: The genome of R. ornithinolytica B16451B was sequenced using the Illumina HiSeq 4000 and PacBio RSII sequencing platforms. A global phylogenetic analysis of the genomic data was conducted by the Center for Genomic Epidemiology (CGE), incorporating information on geographical distribution, isolation sources, and host associations. A comparative phylogenomic analysis was performed using the BLAST Ring Image Generator (BRIG). Genome annotation was performed using Glimmer and the Rapid Annotation using Subsystem Technology (RAST) server. Mobile genetic elements were predicted using TnCentral, ISFinder, and PHASTER. The antibiotic resistance genes (ARGs) were analyzed using the Comprehensive Antibiotic Resistance Database (CARD), while the virulence factors genes (VFGs) were analyzed using the Virulence Factor Database (VFDB). Gene transfer experiments were conducted in the intestinal tract of mice. Transconjugants were identified using 16S rRNA metagenomic sequencing, and drug-resistance genes were amplified by PCR.
RESULTS: A chromosome (designated chromosome 01) was first identified in strain B16451B. A carrying IS4 insertion sequence distinct resistance region within this chromosome, designated B1645-1B-RG, harbors the β-lactamase gene blaORN-1. Three intact prophages, designated prophage YC1, YC2, and YC3, were also first identified. The blaORN-1 gene was successfully transferred from strain B16451B to Escherichia coli (designated B1645-1BLMY1) and Klebsiella pneumoniae (designated B1645-1BYCF2) in the intestines of mice. The strain B16451B harbored 25 antimicrobial resistance genes and 8 classes of virulence factor genes. Based on comparative genomic analysis of strains retrieved from the NCBI Genome Database, 98 antimicrobial resistance genes (ARGs) (e.g., sul1, blaKPC-2, blaNDM-1) among 234 R. ornithinolytica strains were identified to exhibit significantly higher prevalence in human isolates than in non-human host sources (e.g., water, animals, plants).
CONCLUSIONS: The chromosome 01 was identified in a multi-drug resistant ORN-1-producing the strain B16451B isolated from China. The genome of strain B16451B harbors three integrated prophages: YC1 (42.2 kb), YC2 (60.5 kb), and YC3 (23.8 kb) was identified. The IS4 insertion might promote blaORN-1 gene transfer within the intestinal flora of mice. Among these 234 R. ornithinolytica strains analyzed in this study, most virulence factor genes (e.g., ompa, yagx/ecpc) and resistance genes (e.g., blaKPC, blaNDM) exhibited higher prevalence in Homo sapiens isolates than in strains from non-human sources including water, animals and plants. These findings provide valuable references for clinicians optimize the management of R. ornithinolytica infections and guide clinical treatment.