Genomic and metabolic characterization of <i>Trueperella pyogenes</i> isolated from domestic and wild animals

<i>Trueperella pyogenes</i> is an important bacterial pathogen implicated in infections such as mastitis, metritis, pneumonia, and liver abscesses in both domestic and wild animals, as well as endocarditis and prosthetic joint infections in humans. Understanding the genomic and metabolic features that enable <i>T. pyogenes</i> to colonize different anatomical sites within a host and its inter-kingdom transmission and survival is important for the effective control of this pathogen. We employed whole-genome sequencing, phenotype microarrays, and antimicrobial susceptibility testing to identify genomic, metabolic and phenotypic features, and antimicrobial resistance (AMR) genes in <i>T. pyogenes</i> recovered from different livestock, companion, and wildlife animals. For comparative genomic analysis, 83 <i>T. pyogenes</i> genomes, including 60 isolated in the current study and 23 publicly available genomes were evaluated. These genomes represented <i>T. pyogenes</i> strains originating from 16 different body sites of 11 different animal hosts (e.g., cattle, swine, ovine, deer, bison, horse, chamois, and cat). Additionally, 49 <i>T. pyogenes</i> isolates (cattle, sheep, deer, swine, and cats) were evaluated for phenotypic AMR using disk diffusion, and for metabolic profiling using the Biology GENIII MicroPlates. The <i>T. pyogenes</i> strains were found not to be host- or body site-specific. The presence of conserved virulence genes (<i>plo</i> and <i>fimA</i>), as well as genotypic and phenotypic AMR may contribute to the ability of <i>T. pyogenes</i> to cause infections in livestock, wildlife, and pets. Most of the tested isolates metabolized diverse carbon sources and chemical compounds, suggesting that this metabolic versatility may enhance the survival, competitiveness, and pathogenic potential of <i>T. pyogenes</i>.IMPORTANCE<i>Trueperella pyogenes</i> is an important animal pathogen with zoonotic potential, posing a significant health concern to both animals and humans due to its ability to cause infections across different animal host species and tissues. Current understanding of this pathogen's adaptability and survival mechanisms is limited. Here, we evaluated the genomic, virulence, metabolic, and antimicrobial resistance (AMR) characteristics of <i>T. pyogenes</i> recovered from 16 different body sites of 11 different animal hosts (livestock, companion, and wild animals). We identified multiple AMR and virulence genes that may enable <i>T. pyogenes</i> for sustained infection and transmission. Additionally, <i>T. pyogenes</i> strains displayed metabolic versatility which could also contribute to its ability to thrive in diverse environments. Understanding the genomic and metabolic, and AMR characteristics that enable <i>T. pyogenes</i> to colonize different anatomical sites within a host and its transmission between different animal species is important for the effective control of this pathogen.