Recurring acquisition of carbapenemase genes and global emergence of Pseudomonas aeruginosa ST-1047, a lineage shaped by geopolitical conflicts.

UNLABELLED: Pseudomonas aeruginosa sequence type (ST)-1047 is emerging globally as a carbapenemase-rich lineage, yet its evolutionary history and population structure are not known. Here, we performed a comprehensive genomic and epidemiological investigation of 141 ST-1047 isolates from 15 countries, integrating short- and long-read sequencing data with Bayesian phylogenetics and mobile genetic element analyses. Two clonal subpopulations were identified. Subclone 1, defined by blaVIM-11 carriage and loss of exoU, is proposed to have been imported to the United States following the medical evacuation of wounded service members from Afghanistan in 2005 and later seeded a nosocomial outbreak in Washington state. Subclone 2, carrying blaIMP-1, is undergoing rapid clonal expansion due to nosocomial outbreaks in Ukraine hospitals where infection control is impaired by the war with Russia. Genomic islands resembling P. aeruginosa genomic island-97B mediated blaIMP-1 duplication and integration at multiple chromosomal sites, including between iron-regulated small RNAs PrrF1 and PrrF2. Outside these subclones, independent acquisitions of blaNDM-1 and/or blaDIM-1 occurred via diverse resistance islands. While plasmids were detected in some ST-1047 isolates, chromosomal integration of carbapenemase genes has promoted stability and driven the population structure. This global study reveals that, since its emergence in the late 19th century, the ST-1047 lineage showed an exceptional ability to acquire diverse carbapenemases, and that geopolitical conflicts influenced its global spread on at least two occasions. These findings underscore the need for sustained global surveillance and high-resolution genomic analyses to prevent further spread of this high-risk pathogen.

IMPORTANCE: Carbapenemase-producing Pseudomonas aeruginosa is a major cause of healthcare-associated infections worldwide and is associated with high mortality due to limited treatment options. In this study, we characterize the emergence and international spread of a previously underrecognized lineage of P. aeruginosa that has independently acquired and stabilized multiple resistance genes, including those encoding VIM, IMP, NDM, and Dutch imipenemase carbapenemases. Using genomic sequencing and evolutionary analyses, we show how this lineage emerged in the late 19th century and has since adapted by integrating resistance genes directly into its chromosome, promoting long-term stability and outbreak potential. Strikingly, we link its global expansion to population movements, soldier evacuations, and healthcare disruptions during armed conflicts in Afghanistan and Ukraine. This work reveals how political instability can drive the spread of multidrug-resistant bacteria and underscores the value of high-resolution surveillance to detect and contain emerging threats before they become dominant in clinical settings.