Background <p>The transferable resistance genes <i>optrA</i> and <i>poxtA</i> mediate cross-resistance to florfenicol and linezolid, posing serious challenges to both veterinary and human healthcare. Swine farms serve as critical ecological niches for the development and dissemination of multidrug-resistant (MDR) <i>Enterococcus faecium</i> (<i>E. faecium</i>) strains. However, the mechanisms by which <i>E. faecium</i> harboring <i>optrA</i> and <i>poxtA</i> disseminates and persists across the human-animal-environment interface remain unclear.</p> Results <p>In this study, 61 multidrug-resistant <i>E. faecium</i> isolates carrying <i>optrA</i> and/or <i>poxtA</i> were recovered from swine, farm workers, and surrounding environments. Antimicrobial susceptibility testing, conjugation assays, whole-genome sequencing, and phylogenomic analysis were performed. The predominant resistance genes were <i>optrA</i> (78.7%), <i>poxtA</i> (28.5%), and <i>fexA</i> (74.9%). Phylogenetic analysis of 18 representative isolates identified six distinct clades, including a novel sequence type (ST2514) shared across all three sources, suggesting potential inter-host transmission. One representative strain (RX23) harbored <i>optrA</i> and <i>poxtA</i> on two distinct multi-replicon plasmids. Experimental exposure to florfenicol increased plasmid stability (&gt; 90% retention) and resistance levels (2–4-fold MIC elevation), indicating adaptive persistence under antibiotic pressure. Although co-transfer imposed an initial fitness cost, this burden was mitigated over serial passages, enabling long-term plasmid retention.</p> Conclusions <p>Our findings provide evidence that both plasmid-mediated transfer and ecological selection contribute to the dissemination and persistence of <i>optrA</i>/<i>poxtA</i>-positive <i>E. faecium</i> in swine farms. The presence of shared lineages across humans, animals, and environmental niches highlights a potential public health threat. Integrated surveillance and antimicrobial stewardship under the One Health framework are essential to prevent further dissemination along the food production chain.</p>

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Genomic analysis of Enterococcus faecium co-carrying optrA and poxtA from a swine farm: dissemination across the human–animal–environment interface

  • Panpan Xia,
  • Huimin Wu,
  • Wanzhao Chen,
  • Rui Tian,
  • Mengqi Yang,
  • Shuqin Xu,
  • Chenhui Zhang,
  • Tianyuan Zeng,
  • Lining Xia

摘要

Background

The transferable resistance genes optrA and poxtA mediate cross-resistance to florfenicol and linezolid, posing serious challenges to both veterinary and human healthcare. Swine farms serve as critical ecological niches for the development and dissemination of multidrug-resistant (MDR) Enterococcus faecium (E. faecium) strains. However, the mechanisms by which E. faecium harboring optrA and poxtA disseminates and persists across the human-animal-environment interface remain unclear.

Results

In this study, 61 multidrug-resistant E. faecium isolates carrying optrA and/or poxtA were recovered from swine, farm workers, and surrounding environments. Antimicrobial susceptibility testing, conjugation assays, whole-genome sequencing, and phylogenomic analysis were performed. The predominant resistance genes were optrA (78.7%), poxtA (28.5%), and fexA (74.9%). Phylogenetic analysis of 18 representative isolates identified six distinct clades, including a novel sequence type (ST2514) shared across all three sources, suggesting potential inter-host transmission. One representative strain (RX23) harbored optrA and poxtA on two distinct multi-replicon plasmids. Experimental exposure to florfenicol increased plasmid stability (> 90% retention) and resistance levels (2–4-fold MIC elevation), indicating adaptive persistence under antibiotic pressure. Although co-transfer imposed an initial fitness cost, this burden was mitigated over serial passages, enabling long-term plasmid retention.

Conclusions

Our findings provide evidence that both plasmid-mediated transfer and ecological selection contribute to the dissemination and persistence of optrA/poxtA-positive E. faecium in swine farms. The presence of shared lineages across humans, animals, and environmental niches highlights a potential public health threat. Integrated surveillance and antimicrobial stewardship under the One Health framework are essential to prevent further dissemination along the food production chain.