Genomic epidemiology and antimicrobial resistance of <i>Corynebacterium macclintockiae</i> , the predominant species of human pathogens within the <i>Corynebacterium jeikeium</i> complex

Genomic characteristics and optimal treatment of <i>Corynebacterium jeikeium</i> remain largely unknown. We collected clinical information and performed whole-genome sequencing analysis of the causative strains of six cases of <i>C. jeikeium</i> infection at a single hospital over a 9-year period. Additionally, whole-genome sequencing analysis was performed on 33 <i>C</i>. <i>jeikeium</i> strains from cases of bloodstream infection at eight hospitals. Antimicrobial susceptibility testing was performed, and the results were compared to the resistance genes identified. Publicly available genome data of strains of <i>C. jeikeium</i> complex, consisting of <i>C. jeikeium sensu stricto</i>, <i>Corynebacterium macclintockiae</i>, and <i>Corynebacterium evansiae</i>, worldwide, were combined with the data from this study to determine the distribution of genomic species. In the single-center study, cases of prosthetic osteoarticular infection, postoperative intra-abdominal infection, and catheter-related bloodstream infection were identified, and the causative strains were genomically identified as <i>C. macclintockiae</i>. All but one isolate (32/33, 97.0%) in the eight-center study identified as <i>C. jeikeium</i> by matrix-assisted laser desorption ionization-time of flight mass spectrometry were also genomically identified as <i>C. macclintockiae</i>. Nosocomial transmission was suggested in three strain pairs by core-genome single nucleotide polymorphism analysis. <i>C. macclintockiae</i> strains were generally multidrug-resistant, but all anti-methicillin-resistant <i>Staphylococcus aureus</i> agents, including teicoplanin, had favorable activity, and the strains without the <i>tet</i>(W) gene (22/38, 57.9%) were susceptible to tetracyclines. Genome analysis of 66 <i>C</i>. <i>jeikeium</i> complex strains collected worldwide, consisting mainly of clinical strains, re-identified 51 strains (77.3%) as <i>C. macclintockiae</i>. This study demonstrates that <i>C. macclintockiae</i> is the major genomic species of the <i>C. jeikeium</i> complex causing human infections.IMPORTANCERecent widespread use of matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) has facilitated the identification of <i>Corynebacterium</i> spp. in microbiology laboratories, thereby raising awareness of the clinical importance of these organisms. Nevertheless, the accumulation of information on genomic characteristics of <i>Corynebacterium jeikeium</i> has been significantly limited compared to other pathogenic organisms thus far. In this study, we analyzed causative strains of infections identified as <i>C. jeikeium</i> by MALDI-TOF MS, collected from multiple institutions throughout Japan, and found that most of these strains were genomically identified as <i>Corynebacterium macclintockiae</i>, a species that has been newly described recently. Collection of clinical information on selected cases showed that <i>C. macclintockiae</i> indeed caused invasive infections that required intravenous or long-term oral antimicrobial therapy. Additional analyses using genomic data of <i>C. jeikeium</i> complex strains registered in public databases suggest that <i>C. macclintockiae</i> is of global clinical importance.