Evolutionary adaptations in iron capture via type II pyoverdine in XDR pseudomonas aeruginosa ST235

Abstract

Pseudomonas aeruginosa ST235 is a globally disseminated, high-risk clone associated with multidrug resistance and increased virulence. This study explores structural and functional modifications in the pyoverdine synthesis system of the ST235 clone. We analysed extensively drug-resistant (XDR) P. aeruginosa isolates derived from invasive infections and identified a modified type II pyoverdine system unique to ST235. This system is characterized by a truncated pvdS gene and the presence of a novel GNAT-family N-acetyltransferase. Genomic analysis revealed significant rearrangements within the pyoverdine loci, including the replacement of the pvdD–pvdJ–pvdI gene cluster with two large non-ribosomal peptide synthetases and an alpha/beta-hydrolase. Additionally, multiple non-synonymous variations were identified in the pvdA and pvdF genes of ST235. Despite structural modifications within the pyoverdine biosynthetic locus, ST235 isolates exhibited higher overall pyoverdine production than non-ST235 strains. Moreover, iron titration assays confirmed the exceptionally strong Fe(III)-chelating activity of pyoverdine produced by ST235. Nuclear magnetic resonance (NMR) spectroscopy presented distinct chemical shifts in the pyoverdine molecule produced by ST235, particularly in the chromophore and ornithine regions. These findings indicate that the modified type II pyoverdine system of ST235 provides an evolutionary advantage by optimizing iron acquisition without additional metabolic costs, potentially contributing to the persistence and spread of the clone.