Genomic Analysis of <i>Enterococcus faecium</i> from Hospital Soil and Patients: Bridging Community and Hospital Strains

Background: Enterococcus faecium is an opportunistic pathogen classified into hospital-associated (HA), community-associated (CA), and Els (formerly clade B, later identified as E. lactis) clades. The HA E. faecium is linked to clinical infections and antibiotic resistance, with hospital soils serving as potential reservoirs for these resistant pathogens. Objectives: The present study aimed to investigate the phylogenetic relationships, clinical traits, and antibiotic resistance profiles of E. faecium strains isolated from hospital soils and patient feces. The goal was to assess the role of hospital soils as a reservoir for resistant E. faecium strains and identify similarities and differences between clinical and soil-derived isolates. Methods: A total of 25 E. faecium strains from hospital soil and 31 from patient feces were isolated and sequenced. Phylogenetic analysis was performed to categorize strains into HA, CA, and Els clades. Sequence categorization was further refined using HierBAPs. Antimicrobial susceptibility testing assessed resistance profiles. Whole-genome sequencing (WGS) data were analyzed to identify antimicrobial-resistance genes, virulence factors, and replicon distributions. An admixture-based population structure analysis was conducted to evaluate ancestral contributions. Results: Most strains were categorized into HA, CA, or Els clades, with five soil strains forming a distinct "clinical" group. This group shared resistance to ciprofloxacin, penicillin, levofloxacin, ampicillin, and erythromycin with clinical strains. Although the "clinical" group had fewer antibiotic resistance genes (ARGs) than clinical strains, it carried key resistance genes aac(6')-aph(2'') and erm(B), which were prevalent among clinical isolates. The virulence factor distribution and replicon numbers in the "clinical" group resembled those of HA and soil strains, respectively. Admixture analysis revealed equal contributions from HA and CA clades to the "clinical" group. Conclusions: The "clinical" group of E. faecium acts as a transitional group bridging HA and CA clades. Hospital soils serve as reservoirs for resistant E. faecium strains and potential dissemination points for HA E. faecium. These findings highlight the clinical risks posed by E. faecium in hospital soil environments.