ThePseudomonas aeruginosa pirAgene encodes a second receptor for ferrienterobactin and synthetic catecholate analogues

Abstract

Actively secreted iron chelating agents termed siderophores play an important role in the virulence and rhizosphere competence of fluorescent pseudomonads, including Pseudomonas aeruginosa which secretes a high affinity siderophore, pyoverdine, and the low affinity siderophore, pyochelin. Uptake of the iron-siderophore complexes is an active process that requires specific outer membrane located receptors, which are dependent of the inner membrane-associated protein TonB and two other inner membrane proteins, ExbB and ExbC. P. aeruginosa is also capable of using a remarkable variety of heterologous siderophores as sources of iron, apparently by expressing their cognate receptors. Illustrative of this feature are the 32 (of which 28 putative) siderophore receptor genes observed in the P. aeruginosa PAO1 genome. However, except for a few (pyoverdine, pyochelin, enterobactin), the vast majority of P. aeruginosa siderophore receptor genes still remain to be characterized. Ten synthetic iron chelators of catecholate type stimulated growth of a pyoverdine/pyochelin deficient P. aeruginosa PAO1 mutant under condition of severe iron limitation. Null mutants of the 32 putative TonB-dependent siderophore receptor encoding genes engineered in the same genetic background were screened for obvious deficiencies in uptake of the synthetic siderophores, but none showed decreased growth stimulation in the presence of the different siderophores. However, a double knock-out mutant of ferrienterobactin receptor encoding gene pfeA (PA 2688) and pirA (PA0931) failed to be stimulated by 4 of the tested synthetic catecholate siderophores whose chemical structures resemble enterobactin. Ferric-enterobactin also failed to stimulate growth of the double pfeA-pirA mutant although, like its synthetic analogues, it stimulated growth of the corresponding single mutants. Hence, we confirmed that pirA represents a second P. aeruginosa ferric-enterobactin receptor. The example of these two enterobactin receptors probably illustrates a more general phenomenon of siderophore receptor redundancy in P. aeruginosa.

Structure and Function of the PiuA and PirA Siderophore-Drug Receptors from Pseudomonas aeruginosa and Acinetobacter baumannii

“…S1 in the supplemental material). This is consistent with a previous report identifying PirA of P. aeruginosa as a secondary transporter of ferric enterobactin (36).…”

“…The pirA gene in A. baumannii is preceded by nfuA, coding for an Fe-S-containing protein involved in intracellular iron utilization and oxidative-stress response (35). In P. aeruginosa, the gene for the secondary enterobactin transporter PirA is located next to a two-component system comprising the transcriptional regulator PirR (PA0929) and the sensor kinase PirS (PA0930) (36). The closest orthologue of PirA in E. coli is the ferric enterobactin transporter FepA, whose gene is embedded within the enterobactin biosynthesis region (not shown in Fig.…”

Comparative genomics reveals a deep-sea sediment-adapted life style of Pseudoalteromonas sp. SM9913

“…GI-2 contains one TonB-dependent siderophore receptor gene (PSM_A0556) that may be responsible for adsorbing iron ions from the environment (Moeck and Coulton, 1998;Ghysels et al, 2005). There are a total of three TonB-dependent siderophore receptor genes in the SM9913 genome.…”

“…There are a total of three TonB-dependent siderophore receptor genes in the SM9913 genome. Other genes of the siderophore uptake system, such as TonB2 and the TonB system transport proteins, ExbB2 and ExbD2 (Ghysels et al, 2005), are all present in SM9913. Iron is always a growth-limiting factor for marine bacteria (Qin et al, 2007a).…”

Citrate-mediated iron uptake in Pseudomonas aeruginosa: involvement of the citrate-inducible FecA receptor and the FeoB ferrous iron transporter

“…citrate (Cox, 1980b;Harding & Royt, 1990)]. While outer-membrane receptors for most of these heterologous siderophores have been identified (Banin et al, 2005;Cuiv et al, 2006;Ghysels et al, 2005;Llamas et al, 2006Llamas et al, , 2008Poole et al, 1990), additional (e.g. periplasmic or inner-membrane) transport components are generally not evident from the genome sequence.…”