Heterogeneity in recombination rates and accessory gene co-occurrence distinguish Pseudomonas aeruginosa phylogroups

Pseudomonas aeruginosa (class Gammaproteobacteria) is a ubiquitous, ecologically widespread, and metabolically versatile species. It is also an opportunistic pathogen that causes a variety of chronic and acute infections in humans. Its ability to thrive in diverse environments and exhibit a wide range of phenotypes lies in part on its large gene pool, but the processes that govern inter-strain genomic variation remain unclear. Here, we aim to characterize the recombination features and accessory genome structure of P. aeruginosa using 840 globally distributed genome sequences. The species can be subdivided into five phylogenetic sequence clusters (corresponding to known phylogroups), two of which are most prominent. Notable epidemic clones are found in the two phylogroups: ST17, ST111, ST146, ST274, and ST395 in phylogroup 1, and ST235 and ST253 in phylogroup 2. The two phylogroups differ in the frequency and characteristics of homologous recombination in their core genomes, including the specific genes that most frequently recombine and the impact of recombination on sequence diversity. Each phylogroup's accessory genome is characterized by a unique gene pool, co-occurrence networks of shared genes, and anti-phage defense systems. Different pools of antimicrobial resistance and virulence genes exist in the two phylogroups and display dissimilar patterns of co-occurrence. Altogether, our results indicate that each phylogroup displays distinct histories and patterns of acquiring exogenous DNA, which may contribute in part to their predominance in the global population. Our study has important implications for understanding the genome dynamics, within-species heterogeneity, and clinically relevant traits of P. aeruginosa.

The consummate opportunist Pseudomonas aeruginosa inhabits many nosocomial and non-clinical environments, posing a major health burden worldwide. Our study reveals phylogroup-specific differences in recombination features and co-occurrence networks of accessory genes within the species. This genomic variation partly explains its remarkable ability to exhibit diverse ecological and phenotypic traits, and thus contribute to circumventing clinical and public health intervention strategies to contain it. Our results may help inform efforts to control and prevent P. aeruginosa diseases, including managing transmission, therapeutic efforts, and pathogen circulation in non-clinical environmental reservoirs.