Shaohua Hu

The emerging infectious agent Elizabethkingia meningoseptica is associated with life-threatening infections in immunocompromised individuals. However, there are limited data on its geographic distribution, phylogenetic evolution, pathogenesis, and transmission. In this study, we comprehensively analyze and compare the genomic features, evolutionary history, emergence date, and transmission networks of global E. meningoseptica . Geographical distribution reveals the presence of the emerging bacteria in Asia, Europe, and North America, three continents with similar latitudes. Phylogenetic analyses show no relationship between the strain’s evolutionary history and its location, origin, or source, despite the presence of genetic diversity. Analysis of the emergence timeline suggests that America is the most likely source of E. meningoseptica with the common ancestor of this pathogen dating back 90 years. Putative transmission networks indicate that E. meningoseptica bacteria can spread within the same hospital and even across borders. Minor variations in resistance genotypes and virulence genes are observed, supporting existing evidence of inherent resistance and pathogenicity in E. meningoseptica . Additionally, minocycline and doxycycline demonstrate potent antimicrobial activity against this pathogen, making them promising candidates for treating E. meningoseptica infections. Our research highlights the potential for severe nosocomial outbreaks caused by E. meningoseptica with horizontal transmission occurring between countries worldwide. To prevent future outbreak infections, increased genomic surveillance of global E. meningoseptica populations is necessary. IMPORTANCE: Elizabethkingia meningoseptica is an emerging infectious agent associated with life-threatening infections in immunocompromised individuals. However, there are limited data available on the genomic features of E. meningoseptica . This study aims to characterize the geographical distribution, phylogenetic evolution, pathogenesis, and transmission of this bacterium. A systematic analysis of the E. meningoseptica genome revealed that a common ancestor of this bacterium existed 90 years ago. The evolutionary history showed no significant relationship with the sample source, origin, or region, despite the presence of genetic diversity. Whole genome sequencing data also demonstrated that E. meningoseptica bacteria possess inherent resistance and pathogenicity, enabling them to spread within the same hospital and even across borders. This study highlights the potential for E. meningoseptica to cause severe nosocomial outbreaks and horizontal transmission between countries worldwide. The available evidence is crucial for the development of evidence-based public health policies to prevent global outbreaks caused by emerging pathogens.

Elizabethkingia anophelis 12012‐2 PRCM was isolated from a patient with multiple organ dysfunction syndrome and lower respiratory tract infection in China. Minimum inhibitory concentration (MIC) analysis demonstrated that it was resistant to 20 antibiotics including trimethoprim/sulfamethoxazole and ciprofloxacin, which were effective for the elimination of other Elizabethkingia infections. To investigate multidrug resistance and pathogenicity mechanisms, we analyzed genome features of 12012‐2 PRCM and compared them to the other Elizabethkingia species. The draft genome size was 4.02 Mb with a GC content of 32%, comparable to that of other E. anophelis strains. Phylogenetic analysis showed that E. anophelis 12012‐2 PRCM formed a sister group with E. anophelis 502, distinct from clades formed by other clinical and environmental E. anophelis isolates. E. anophelis 12012‐2 PRCM contained multiple copies of β‐lactamase genes as well as genes predicted to function in antimicrobial efflux. It also contained 92 genes that were potentially involved in virulence, disease, and defense, and were associated with resistance and pathogenicity. Comparative genomic analysis showed high homology among three clinical and two environmental E. anophelis strains having a variety of similar antibiotic resistance and virulence factor genes, and similar genomic structure. Applications of this analysis will contribute to understanding the antibiotic resistance and pathogenic mechanisms of E. anophelis infections, which will assist in the management of infections as it increases in prevalence.