Genomic diversity of Pseudomonas aeruginosa causing bacteremic pneumonia in an intensive care unit, with emergence of an OXA-796-producing NDM-1 ST773 isolate.

Abstract

Pseudomonas aeruginosa bacteremic pneumonia carries exceptionally high mortality, yet there is a paucity of genomic characterization of the strains causing this infection. We performed hybrid sequencing (Illumina and Oxford Nanopore) of 12 non-redundant P. aeruginosa isolates from patients with severe bacteremic pneumonia admitted to the intensive care unit of a tertiary hospital between 2015 and 2023. The 12 isolates were assigned to nine distinct sequence types, suggesting that severe bacteremic pneumonia can arise from diverse P. aeruginosa lineages rather than being dominated by a single specialized or high-risk clone. In the combined dataset of our isolates and publicly available Korean P. aeruginosa genomes, type III secretion system exotoxin genotypes exoU and exoS showed a mutually exclusive and phylogenetically segregated distribution, as previously reported, with both genotypes represented among bacteremic pneumonia isolates. Carbapenemase genes were detected in only one isolate, PA22 (ST773), which harboured bla _NDM-1 together with bla _OXA-796 and was the only isolate displaying phenotypic carbapenem resistance and multidrug resistance. To assess the clonal relationship between bla _NDM-1-positive PA22 and the carbapenemase-negative ST773 isolate PA20 and to track the evolution of PA22 resistome within a broader epidemiological context, we investigated the population structure of a global ST773 dataset. Core genome MLST-based minimum spanning trees revealed a deep bifurcation within ST773, separating bla _NDM-1-positive and carbapenemase-negative lineages. Korean ST773 isolates formed two distinct clusters within the NDM-1-positive lineage, with the PA22-containing cluster phylogenetically proximal to isolates from the United States. Within the NDM-1-positive Korean cluster, bla _OXA-796 was located in conserved class 1 integron gene cassette arrays that exhibit ongoing structural diversification among closely related isolates, evidenced by variable integration of IS110 elements. Our findings demonstrate that severe bacteremic pneumonia arises from phylogenetically diverse P. aeruginosa lineages and provide genomic context for the NDM-1-producing ST773 clone that is rapidly emerging in Korea.