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In cystic fibrosis (CF) airways, the opportunistic pathogen  Pseudomonas aeruginosa  evolves from an acute to a chronic infection phenotype. Yet, the  in vivo  factors influencing the evolutionary trajectory of  P .  aeruginosa  are poorly understood. This study aimed at understanding the role of the CF lung microbiome in  P .  aeruginosa  evolution. Therefore, we investigated the  in vitro  biofilm evolution of an early CF  P .  aeruginosa  isolate, AA2, in the presence or absence of a synthetic CF lung microbiome. Whole genome sequencing of evolved populations revealed mutations in quorum sensing (QS) genes ( lasR ,  pqsR ) with and without the microbiome. Phenotypic assays confirmed decreased production of the QS molecule 3-O-C 12 -homoserine lactone, and QS-regulated virulence factors pyocyanin and protease. Furthermore, a mixture of  lasR  and  lasR pqsR  mutants was found, in which double mutants showed less pyocyanin and protease production than  lasR  mutants. While the microbial community did not influence the production of the tested  P .  aeruginosa  virulence factors, we observed a trend towards more mutations in the transcriptional regulators  gntR  and  mexL  when  P .  aeruginosa  was grown alone.  P .  aeruginosa  developed resistance to β-lactam antibiotics during evolution, when grown with and without the microbiome. In conclusion, in an experimental biofilm environment, the early  P .  aeruginosa  CF isolate AA2 evolves towards a CF-like genotype and phenotype, and most studied evolutionary adaptations are not impacted by CF microbiome members.

In vitro evolution of Pseudomonas aeruginosa AA2 biofilms in the presence of cystic fibrosis lung microbiome members