Frontiers in cellular and infection microbiology · 2026
Genomic convergence of mobilome-associated multidrug resistance and host-adaptation determinants in a postoperative Raoultella ornithinolytica isolate carrying bla KPC-2, bla NDM-5, and a truncated mcr-10-like element.
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Wang Ziheng, Xu Guangping, Li Ruodan, Qin Jiaxu, Bao Ruiming, Chen Zihao, Li Jie, Zhang Peng
Аннотация
OBJECTIVE: To characterize the convergence of resistance determinants, plasmid-mediated dissemination, and host adaptation in the postoperative Raoultella ornithinolytica isolate RO0725 through integrated genomic analyses and phenotypic validation. We further sought to evaluate its clinical and One Health risks.
METHODS: Long-read sequencing was used to generate a complete genome. Subsequent analyses assessed phylogeny, average nucleotide identity, resistance genes, and plasmid comparisons. Phenotypic validation included conjugation assays, bile salt tolerance, biofilm formation, and a Galleria mellonella infection model.
RESULTS: The RO0725 genome comprised one chromosome and five circular plasmids. RO0725 carried 14 antimicrobial-resistance genes distributed across the chromosome and three resistance-associated plasmids. Chromosomal determinants included intrinsic resistance-associated genes such as bla ORN-1, oqxA10, oqxB9, and fosA9. The plasmid pRO0725-1 carried a truncated mcr - 10-like element, whereas pRO0725-2 harbored bla KPC-2, bla CTX-M-3, bla TEM-1, qnrS1, dfrA14, arr-3, and aac(6')-Ib-AKT. The IncX3-like plasmid pRO0725-3 carried bla NDM-5 and ble-MBL. Both pRO0725-2 and pRO0725-3 exhibited transferable potential in conjugation assays. RO0725 did not form a near-clonal cluster (defined as ≤10 core-genome SNPs) with any public isolates. RO0725 contained host-adaptation-associated determinants involved in adhesion (ecp, fim, and mrk), iron acquisition (ent, fep, ybt, irp, fyuA, and iutA), stress response (phoP, rcsB, rpoS, acrAB, and ompA), and cellulose biosynthesis (bcs). Phenotypically, RO0725 exhibited enhanced bile salt tolerance, weak biofilm formation, and moderate lethality in the G. mellonella model.
CONCLUSION: RO0725 represents a convergence of transferable multidrug-resistance plasmids and host-adaptation determinants. These findings indicate that R. ornithinolytica may act as both an opportunistic pathogen and a potential reservoir for the interspecies dissemination of resistance genes. They support its inclusion in hospital and One Health antimicrobial-resistance surveillance.
METHODS: Long-read sequencing was used to generate a complete genome. Subsequent analyses assessed phylogeny, average nucleotide identity, resistance genes, and plasmid comparisons. Phenotypic validation included conjugation assays, bile salt tolerance, biofilm formation, and a Galleria mellonella infection model.
RESULTS: The RO0725 genome comprised one chromosome and five circular plasmids. RO0725 carried 14 antimicrobial-resistance genes distributed across the chromosome and three resistance-associated plasmids. Chromosomal determinants included intrinsic resistance-associated genes such as bla ORN-1, oqxA10, oqxB9, and fosA9. The plasmid pRO0725-1 carried a truncated mcr - 10-like element, whereas pRO0725-2 harbored bla KPC-2, bla CTX-M-3, bla TEM-1, qnrS1, dfrA14, arr-3, and aac(6')-Ib-AKT. The IncX3-like plasmid pRO0725-3 carried bla NDM-5 and ble-MBL. Both pRO0725-2 and pRO0725-3 exhibited transferable potential in conjugation assays. RO0725 did not form a near-clonal cluster (defined as ≤10 core-genome SNPs) with any public isolates. RO0725 contained host-adaptation-associated determinants involved in adhesion (ecp, fim, and mrk), iron acquisition (ent, fep, ybt, irp, fyuA, and iutA), stress response (phoP, rcsB, rpoS, acrAB, and ompA), and cellulose biosynthesis (bcs). Phenotypically, RO0725 exhibited enhanced bile salt tolerance, weak biofilm formation, and moderate lethality in the G. mellonella model.
CONCLUSION: RO0725 represents a convergence of transferable multidrug-resistance plasmids and host-adaptation determinants. These findings indicate that R. ornithinolytica may act as both an opportunistic pathogen and a potential reservoir for the interspecies dissemination of resistance genes. They support its inclusion in hospital and One Health antimicrobial-resistance surveillance.