Phenotypic Adaption of Pseudomonas aeruginosa by Hacking Siderophores Produced by Other Microorganisms

Using proteomic and RT-qPCR approaches, we investigated how Pseudomonas aeruginosa adapts the level of expression of its various iron-uptake pathways in response to different growth conditions (planktonic growth in different media and an epithelial cells infection assay) in the presence and absence of four different exosiderophores. The results show a complex phenotypic plasticity in the expression of the various iron-uptake pathways indicating a high potential of adaptation of P. aeruginosa to a large variety of biotopes. [Display omitted] Highlights •P. aeruginosa grown with exosiderophores and analyzed by proteomic and RT-qPCR.•Catechol-type exosiderophores strongly induce the expression of their transporters.•Repression of the endogenous iron uptake pathways.•Complex phenotypic plasticity in the expression of the various iron-uptake pathways. Bacteria secrete siderophores to access iron, a key nutrient poorly bioavailable and the source of strong competition between microorganisms in most biotopes. Many bacteria also use siderophores produced by other microorganisms (exosiderophores) in a piracy strategy. Pseudomonas aeruginosa, an opportunistic pathogen, produces two siderophores, pyoverdine and pyochelin, and is also able to use a panel of exosiderophores. We first investigated expression of the various iron-uptake pathways of P. aeruginosa in three different growth media using proteomic and RT-qPCR approaches and observed three different phenotypic patterns, indicating complex phenotypic plasticity in the expression of the various iron-uptake pathways. We then investigated the phenotypic plasticity of iron-uptake pathway expression in the presence of various exosiderophores (present individually or as a mixture) under planktonic growth conditions, as well as in an epithelial cell infection assay. In all growth conditions tested, catechol-type exosiderophores were clearly more efficient in inducing the expression of their corresponding transporters than the others, showing that bacteria opt for the use of catechol siderophores to access iron when they are present in the environment. In parallel, expression of the proteins of the pyochelin pathway was significantly repressed under most conditions tested, as well as that of proteins of the pyoverdine pathway, but to a lesser extent. There was no effect on the expression of the heme and ferrous uptake pathways. Overall, these data provide precise insights on how P. aeruginosa adjusts the expression of i