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              <p>The role of polyamines in pathogen virulence remains relatively understudied, but it has been demonstrated for Streptococcus pneumoniae and Legionella pneumophila, and is currently being investigated for Candida albicans (data presented at GDR Polyamines 2023), with diverse mechanisms of action.In our laboratory, using an untargeted metabolomics approach on Pseudomonas aeruginosa (Pa) isolates (n=66) collected from a cohort of cystic fibrosis (CF) patients, we identified a correlation between the production levels of several molecules from the polyamine pathway—including spermidine—and both the virulence of the strains and the decline in respiratory function (FEV1) in CF patients over time (Moyne et al. 2021). Our objective is to decipher the role of polyamines in P. aeruginosa virulence.To achieve this, we sequenced clinical Pa isolates from our cohort and performed a transcriptomic study on 6 isolates with high polyamine production (PH) and 5 isolates with low production (PB). Genomic and transcriptomic analyses allowed us to identify the genes involved in this differential polyamine production. We generated knockout (KO), allelic exchange, and complemented mutants of these genes in the PH strain of a strain pair derived from the same patient (patient 14). These mutants were characterized for cytotoxicity phenotypes, and we initiated competition assays between these mutants and Staphylococcus aureus.Genomic analysis revealed the presence of both the “classical” spermidine biosynthesis pathway (speE and speD) and an “alternative” biosynthesis pathway (speE2, speD2, PA4775, pmrA, and pmrB), organized as an operon and regulated by the two-component system PmrAB. This alternative pathway has been previously described, but the final reaction product remains debated: spermidine according to Johnson et al. (2012) or norspermidine according to Bolard et al. (2019).Through transcriptomic analysis, we validated that the alternative pathway is the predominant one, as it is strongly upregulated in PH isolates, which are high polyamine producers. The construction of KO and allelic exchange mutants allowed us to assess cytotoxicity phenotypes on A549 pulmonary epithelial cells and J774 macrophages, confirming the importance of this pathway in P. aeruginosa cytotoxicity.PerspectivesIdentifying the alternative polyamine biosynthesis pathway is particularly intriguing. First, we aim to characterize the final product of this pathway—spermidine or norspermidine—using high-resolution mass spectrometry combined with GNPS molecular networking (Nothias et al. 2022). Second, we intend to evaluate the role of this pathway in P. aeruginosa evolution over time. Finally, we plan to investigate whether exogenous polyamines produced by the host can modulate P. aeruginosa virulence.A better understanding of the evolutionary trajectory of these strains in the context of cystic fibrosis patients will provide critical insights into predicting and managing potential infectious exacerbations linked to shifts in the environmental conditions in which these strains have been adapting over many years.</p>
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              <p>Le rôle des polyamines dans la virulence de pathogène est relativement peu étudié, mais a été démontré pour Streptococcus pneumoniae, Legionella pneumophila et est en cours pour Candida albicans (données présentées au GDR Polyamines 2023) avec des mécanismes d’action variés. Au laboratoire, en utilisant une approche de métabolomique non ciblée sur des isolats de Pseudomonas aeruginosa  (n=66) provenant d’une cohorte de patients atteints de mucoviscidose, nous avons trouvé une corrélation entre le niveau de production de plusieurs molécules de la voie des polyamines, entre autre la spermidine, et le niveau de virulence des souches et l’instabilité de de la fonction respiratoire (VEMS) des patients CF au cours du temps (Moyne et al. 2021). Notre objectif est de déchiffrer le rôle des polyamines dans la virulence de Pseudomonas aeruginosa (Pa). Pour cela, nous avons réalisé le séquençage des isolats cliniques de Pa de notre cohorte et réalisé une étude transcriptomique pour 6 isolats présentant un niveau élevé de production de polyamines (PH) et 5, un niveau bas PB. L’analyse de ces génomes et transcriptomes a permis d’identifier les gènes impliqués dans cette différence de production de polyamines. Nous avons construits les mutants KO, d’échanges alléliques et complémentés de ces gènes dans la souche PH d’un couple de souches provenant d’un même patient (patient 14). Nous avons caractérisé les phénotypes de cytotoxicité, et débuté des expériences de compétition entre ces mutants et S. aureus. Grâce à l’étude des génomes, nous avons pu mettre en évidence la présence chez ces isolats de Pa d’une voie de synthèse de la spermidine dite « classique » (speE et speD), mais également la présence d’une voie dite « alternative » de biosynthèse de spermidine (speE2, speD2, PA4775, pmrA et pmrB), voie en opéron et sous le contrôle d’un système à 2 composants PmrAB. Cette voie alternative est connue mais le produit final de la réaction diverge selon les sources, spermidine pour Johnson et al. 2012, ou norspermidine pour Bolard et al. 2019. Grâce à l’étude transcriptomique, nous avons validé que la voie alternative est bien la voie la plus importante, fortement up-régulée chez les isolats PH, haut producteur de polyamines. La construction des mutants KO et d’échanges alléliques, nous a permis de mesurer les phénotypes de cytotoxicité sur des cellules épithéliales pulmonaires A549 et macrophagique J774, et validé l’importance de cette voie dans la cytotoxicité de Pa. En perspective, l’identification de la voies alternative de production des polyamines est intéressante. Nous souhaiterions dans un premier temps caractérisé le produit de cette voie alternative, spermidine ou norspermidine, par spectrométrie de masse haute résolution à l’aide de réseau moléculaire GNPS (Nothias et al. 2022). Dans un deuxième temps, nous aimerions évaluer l’importance de cette voie dans l’évolution de Pa au cours du temps. Enfin, nous aimerions regarder si la présence de polyamines exogènes, produite par l’hôte pourrait moduler la virulence de Pa. Mieux comprendre la trajectoire évolutive de ces souches en matière d’adaptation chez le patient mucoviscidosique permettra de mieux anticiper la prise en charge des potentielles exacerbations infectieuses dues au changement des conditions dans lesquelles ces souches évoluaient depuis de nombreuses années.</p>
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