Abstract
Pseudomonas aeruginosa is a Gram-negative bacterium which can cause serious infections among immune-depressed people including cystic fibrosis patients where it can colonize the lungs causing chronic infections. Iron is essential for P. aeruginosa and can be provided via three sources under aerobic conditions: its own siderophores pyochelin (PCH) and pyoverdine (PVD), xenosiderophores, or heme, respectively. Pyoverdine is the high affinity siderophore and its synthesis and uptake involve more than 30 genes organized in different operons. Its synthesis and uptake are triggered by iron scarcity via the Fur regulator and involves two extra cytoplasmic sigma factors (ECF), PvdS for the biosynthesis of PVD and FpvI for the uptake via the TonB-dependent FpvA outer membrane transporter and other periplasmic and inner membrane proteins. It appeared recently that the regulation of PVD biosynthesis and uptake involves other regulators, including other ECF factors, and LysR regulators. This is the case especially for the genes coding for periplasmic and inner membrane proteins involved in the reduction of Fe3+ to Fe2+ and the transport of ferrous iron to the cytoplasm that appears to represent a crucial step in the uptake process.
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Introduction
Pseudomonas aeruginosa is an important opportunistic pathogen able to cause a variety of acute or chronic infections (Lyczak et al. 2000). Being mostly an aerobe microorganism, it must rely on different strategies to take up iron, which is mainly in the highly insoluble Fe3+ form (Cornelis and Dingemans 2013). Pyoverdine (PVD) is the high affinity siderophore produced by P. aeruginosa under conditions of iron scarcity and is important for the virulence of the pathogen since unlike pyochelin, the other P. aeruginosa siderophore, it is able to displace iron from Fe-transferrin complex (Meyer et al. 1996). Pyoverdines are produced by many Pseudomonas species and comprise a dihydroxyquinoline fluorescent chromophore joined to a peptide chain of variable length and composition (Ravel and Cornelis 2003). Production of siderophores and their uptake are triggered by iron limitation and are regulated by the master regulator Fur (Ferric Uptake Regulator) (Escolar et al. 1999). However, PVD biosynthesis and uptake is not directly regulated by Fur, but indirectly via two extra cytoplasmic function sigma factors (ECF) PvdS and FpvI for biosynthesis and uptake, respectively (Fig. 1) (Visca et al. 2007). These two ECF are sequestered by the cytoplasmic domain of the FpvR anti-sigma protein spanning the inner membrane and are released when the ferri-PVD interacts with the outer membrane FpvA TonB dependent transporter (TBDT), triggering a proteolytic degradation of FpvR in a process termed cell surface signaling (Llamas et al. 2014). PvdS not only controls the genes for PVD biosynthesis, but also the genes coding for the exotoxin A and the PrpL secreted protease virulence factors (Ochsner et al. 1995; Wilderman et al. 2001). The biosynthesis and uptake of PVD involves two clusters of genes in P. aeruginosa including non-ribosomal peptide synthetases PvdL (for the chromophore precursor) (Mossialos et al. 2002), PvdI, PvdJ and PvdD for the peptide chain of pyoverdine (Ravel and Cornelis 2003). The uptake of Fe-PVD involves the outer membrane FpvA transporter whereby the Fe-PVD enters the periplasm and binds the periplasmic proteins FpvF and FpvC followed by the reduction of Fe3+ to Fe2+ which remains attached to FpvC while FpvF stays bound to apo-pyoverdine before further recycling via the efflux system FpvRTOpmQ (Bonneau et al. 2020). Finally, Fe2+ is transported to the cytoplasm by the FpvDE ABC transporter (Fig. 2A) (Brillet et al. 2012; Ganne et al. 2017; Bonneau et al. 2020). This periplasmic iron reduction and transport represents the last step of Fe-PVD uptake and is therefore crucial since it represents a no-return mechanism allowing the entry of Fe2+ inside the cytoplasm.
Uptake of ferri-PVD occurs via the binding to the FpvA outer membrane TBDT triggering a proteolytic cascade resulting in the degradation of the FpvR anti- factor and the release of the two ECF PvdS and FpvI (Llamas et al. 2014)
A Binding of Fe-PVD to FpvA is followed by association of the ferri-siderophore with the two periplasmic proteins FpvF and FpvC that interact with FpvG (Brillet et al. 2012; Ganne et al. 2017). After dissociation of the two proteins, FpvF stays associated with apo-PVD while FpvC is now bound with Fe2+ after Fe3+ reduction. Finally, Fe2+ is transported to the cytoplasm by the FpvDE ABC transporter. FpvF has been found to interact with the PvdRT-OpmQ efflux system involved in the recycling of apo-PVD out of the cell (see text for details). B The fpvGHJKCDEF cluster showing the direct regulation by PvdS, SigX and FpvI (Table 1). The involvement of the three ECF PA0149, PA2050 (Llamas et al. 2008) and HxuI (Cai et al. 2022) is maybe indirect but their overexpression results in increased transcription as indicated by the numbers above the different genes
Regulators beside Fur are involved in pvdS expression regulation
PvdS is one of the nineteen ECFσ factors encoded by the genome of P. aeruginosa PAO1 (21 in PA14) (Chevalier et al. 2019). PvdS expression was known to be controlled by the Fur regulator (Ochsner et al. 2002), but more recent data showed that three LysR regulators (LTTRs) also directly bind to the region upstream of the pvdS gene, OxyR, CysB, and PA2206 (Imperi et al. 2010; Wei et al. 2012; Reen et al. 2013) (Fig. 3). OxyR is the master regulator of the response of P. aeruginosa to oxidative stress and was previously known to activate the transcription of reactive oxygen response genes ahpCF, ahpB (alkyl hydroperoxidases) and katB which encodes a catalase (Ochsner et al. 2000). However, a global genome wide study based on Gene-Chip analysis revealed that the OxyR regulon is more extended and includes genes not known to be involved in oxidative stress resistance (Wei et al. 2012). Interestingly, the pvdS gene was one of the hits and the binding of OxyR to the promoter region of pvdS was confirmed by EMSA (electrophoretic mobility shift assay) (Wei et al. 2012). Vinckx and colleagues have confirmed the importance of OxyR for the PVD-mediated iron uptake in P. aeruginosa (Vinckx et al. 2008). A mutant with a deleted oxyR gene was found to be unable to grow under conditions of extreme iron limitation caused by the presence of the strong Fe3+ iron chelator ethylenediamine-N,N′-bis(2-hydroxyphenylacetic acid) (EDDHA) in the casamino acid medium (CAA) (Vinckx et al. 2008). However, this defect was not due to an impaired uptake of radioactive 59Fe PVD but was hypothesized to be a consequence of a defect in the import of iron to the cytoplasm suggesting an impaired process in the periplasm (Vinckx et al. 2008) as described above (Fig. 2). A second LTTR, PA2206, was found to bind to the promoter region of pvdS (Reen et al. 2013) (Fig. 3). PA2206 transcription was found to be up regulated by exposure to hydrogen peroxide (H2O2) and to be needed for a full response to oxidative stress generated by H2O2 independently of OxyR. PA2206 was shown by EMSA to bind to the pvdS promoter region (Reen et al. 2013). AlgR is a transcriptional regulator that regulates a variety of iron-associated genes and controls pyoverdine production through its phosphorylation state. P. aeruginosa PAO1 encoding a modified unphosphorylated AlgR variant, displayed a decreased PVD production, while another mutant producing constitutively phosphorylated AlgR showed an increased production of PVD. It was shown that AlgR-repressed pyoverdine production through the activation of PrrF2 small regulatory RNA expression and the direct repression of pvdS expression (Little et al. 2018). Unphosphorylated AlgR was found to bind the promoter region of pvdS by EMSA in a region before the OxyR and PA2206 binding sites (Little et al. 2018). A consensus binding site for AlgR has been derived from a Chip-seq study (Kong et al. 2015) and a 10 bp sequence corresponding to this predicted sequence could be found in the pvdS upstream region in the location predicted by Little et al. (Fig. 3). Another LTTR found to bind to the pvdS upstream region is CysB, the central regulator of sulfur metabolism in P. aeruginosa (Imperi et al. 2010). When cysB is deleted, growth is not affected in low iron medium, but the production of pyoverdine is decreased, as well as the PvdS-dependent PrpL protein (Imperi et al. 2010). Although not annotated as a transcriptional regulator, PpyR (Psl and Pyoverdine Operon Regulator), an inner membrane protein, is essential for the expression of all PVD genes since a ppyR mutant shows a dramatic decrease of all pyoverdine genes, including pvdS (Attila et al. 2008).
The genomic context of the ECF pvdS gene (in red) showing tin the insert the intergenic sequence upstream of pvdS and the different binding sites for Fur (in red), PvdS (in blue), PA2206 LTTR (in yellow) (Reen et al. 2013), OxyR (in green) (Wei et al. 2012), and AlgR (brown) (Kong et al. 2015). The CysB regulator binding site (Imperi et al. 2010) has not been determined and is not indicated. See text for details
In addition to the regulators already mentioned, it was found very recently that three response regulators (RRs) from two-component systems, CzcR, AmgR, and PirR, bind to the upstream region of pvdS as well (Trouillon et al. 2021), further expanding the number of regulators involved in pvdS regulation. It is interesting to mention that PirR is the RR involved in the regulation of PirA, a second transporter of enterobactin and catecholates siderophores in P. aeruginosa (Ghysels et al. 2005).
ECF PvdS and FpvI regulons include other ECF
A recent comprehensive study of ten sigma factors extended regulons (“sigmulons”) in P. aeruginosa PA14 combining chromatin immunoprecipitation and high throughput sequencing (Chip-seq) revealed a network of interacting sigma factors among them seven ECFσ (Schulz et al. 2015). According to the results of this study, the SigX ECF interacts with fpvG and pvdI promoter regions (Schulz et al. 2015) (Table 1). SigX is an ECFσ involved in membrane fluidity homeostasis (Boechat et al. 2013; Blanka et al. 2014; Flechard et al. 2018; Chevalier et al. 2019; Bouffartigues et al. 2020) and its regulon is predicted to be quite large (610 genes) among two are under control of PvdS as well, including pvdI itself and fpvG (Schulz et al. 2015) (Table 1). Interestingly, the FpvI regulon which was supposed to comprise only the fpvA gene coding for the TonB-dependent ferri-pyoverdine TBDT (Beare et al. 2003), also now includes the fpvG, pvdI, and the pvdA genes, together with PvdS (Schulz et al. 2015). Noticeably, SigX is also involved in the regulation of fpvA and fpvR (Table 1).The probable inclusion of argA in the PvdS regulon is interesting because it is the first gene of the arginine/ornithine biosynthetic pathway and N-hydroxy ornithine is present in the peptide chain of pyoverdine involving the PvdA enzyme L-ornithine N(delta)-oxygenase (Ge and Seah 2006; Imperi et al. 2008).
The fpvGHJKCDEF genes cluster is multiply regulated
As already mentioned, this cluster comprises genes coding for membrane and periplasmic proteins involved in the reduction of iron from the Fe-PVD in the periplasm and the transport of Fe2+ to the cytoplasm by the ABC transporter FpvDE (Fig. 2A). As shown in Fig. 2B this cluster is under the direct control of the ECFσ PvdS, FpvI, and SigX (Schulz et al. 2015). Surprisingly, two other ECFσ are involved as well, PA0149, and PA2050 described as new cell surface signaling components (Llamas et al. 2008). PA0149 ECF overexpression activates the transcription of the PA0151 TBDT more than 30-fold, but also the fpvGHJKCDEF gene cluster (Fig. 2B). Likewise, overexpression of PA2050 ECFσ results in activation of the transcription of two TBDT, PA2057 (SppR) (Pletzer et al. 2016) and PA2070, but of fpvGHJKCDEF as well (Llamas et al. 2008) (Fig. 2B). The same authors suggest that this gene cluster is not only involved in Fe-PVD reduction and Fe transport from PVD, but also for similar steps involving other siderophore transport systems, explaining the multiple regulators involved in the control of expression of these genes. However, we do not know at this stage whether the action of both PA0149 and PA2050 ECF is direct or indirect via a second fur-like gene (fur2, PA2384), but no xenosiderophore has been identified for the TBDT involved (Llamas et al. 2008). Very recently, an article described the effect of the overexpression of the ECF HxuI on the expression of its cognate heme transporter gene, hxuA, but also on the fpvGHJKCDEF expression as well (Fig. 2) (Cai et al. 2022). The same authors identified a consensus DNA binding sequence for HxuI, upstream of hxuI, hxuA, fur2 and fpvG among other genes coding for virulence factors, including phzA2, the first gene of the second operon for pyocyanin biosynthesis (Cai et al. 2022). This interesting study further highlights the importance of the fpvGHJKCDEF cluster for the assimilation of Fe2+ from pyoverdine, but also from other iron sources.
Conclusions
This short review presents evidence that the regulation of PVD production and uptake involves different regulators, either by acting at the level of the master ECF pvdS gene (OxyR, PA2206, AlgR, CysB, PirR, CzcR, AmgR) or other genes, although their contribution might not be as essential compared to PvdS but might contribute to fine tuning of pyoverdine production in function of environmental cues, which have not yet been defined. Particularly interesting is the participation of several ECF, including the recently described HxuI involvement, in the regulation of genes coding for periplasmic and inner membrane proteins involved in the reduction of Fe-PVD and the import of Fe2+ to the cytoplasm, suggesting that this process might contribute to the reduction of Fe3+ from other iron sources. There is also some evidence that the PvdS and FpvI regulons are larger than previously anticipated, including other genes outside the PVD cluster. However, several other regulators are likely to be involved, directly or indirectly into the regulation of siderophore-mediated iron uptake in P. aeruginosa, as described for the Gac-Rsm pathway, probably via the production of the internal c-di-GMP signal molecule (Frangipani et al. 2014).
References
Attila C, Ueda A, Wood TK (2008) PA2663 (PpyR) increases biofilm formation in Pseudomonas aeruginosa PAO1 through the psl operon and stimulates virulence and quorum-sensing phenotypes. Appl Microbiol Biotechnol 78(2):293–307. https://doi.org/10.1007/s00253-007-1308-y
Beare PA, For RJ, Martin LW, Lamont IL (2003) Siderophore-mediated cell signalling in Pseudomonas aeruginosa: divergent pathways regulate virulence factor production and siderophore receptor synthesis. Mol Microbiol 47(1):195–207. https://doi.org/10.1046/j.1365-2958.2003.03288.x
Blanka A, Schulz S, Eckweiler D, Franke R, Bielecka A, Nicolai T et al (2014) Identification of the alternative sigma factor SigX regulon and its implications for Pseudomonas aeruginosa pathogenicity. J Bacteriol 196(2):345–356. https://doi.org/10.1128/JB.01034-13
Boechat AL, Kaihami GH, Politi MJ, Lepine F, Baldini RL (2013) A novel role for an ECF sigma factor in fatty acid biosynthesis and membrane fluidity in Pseudomonas aeruginosa. PLoS ONE 8(12):e84775. https://doi.org/10.1371/journal.pone.0084775
Bonneau A, Roche B, Schalk IJ (2020) Iron acquisition in Pseudomonas aeruginosa by the siderophore pyoverdine: an intricate interacting network including periplasmic and membrane proteins. Sci Rep 10(1):120. https://doi.org/10.1038/s41598-019-56913-x
Bouffartigues E, Si Hadj Mohand I, Maillot O, Tortuel D, Omnes J, David A et al (2020) The temperature-regulation of Pseudomonas aeruginosa cmaX-cfrX-cmpX operon reveals an intriguing molecular network involving the sigma factors AlgU and SigX. Front Microbiol 11:579495. https://doi.org/10.3389/fmicb.2020.579495
Brillet K, Ruffenach F, Adams H, Journet L, Gasser V, Hoegy F et al (2012) An ABC transporter with two periplasmic binding proteins involved in iron acquisition in Pseudomonas aeruginosa. ACS Chem Biol 7(12):2036–2045. https://doi.org/10.1021/cb300330v
Cai Z, Yang F, Shao X, Yue Z, Li Z, Song Y et al (2022) ECF sigma factor HxuI is critical for in vivo fitness of Pseudomonas aeruginosa during infection. Microbiol Spectr. https://doi.org/10.1128/spectrum.01620-21
Chevalier S, Bouffartigues E, Bazire A, Tahrioui A, Duchesne R, Tortuel D et al (2019) Extracytoplasmic function sigma factors in Pseudomonas aeruginosa. Biochim Biophys Acta Gene Regul Mech 1862(7):706–721. https://doi.org/10.1016/j.bbagrm.2018.04.008
Cornelis P, Dingemans J (2013) Pseudomonas aeruginosa adapts its iron uptake strategies in function of the type of infections. Front Cell Infect Microbiol 3:75. https://doi.org/10.3389/fcimb.2013.00075
Escolar L, Perez-Martin J, de Lorenzo V (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181(20):6223–6229. doi: https://doi.org/10.1128/JB.181.20.6223-6229.1999
Flechard M, Duchesne R, Tahrioui A, Bouffartigues E, Depayras S, Hardouin J et al (2018) The absence of SigX results in impaired carbon metabolism and membrane fluidity in Pseudomonas aeruginosa. Sci Rep 8(1):17212. https://doi.org/10.1038/s41598-018-35503-3
Frangipani E, Visaggio D, Heeb S, Kaever V, Camara M, Visca P et al (2014) The Gac/Rsm and cyclic-di-GMP signalling networks coordinately regulate iron uptake in Pseudomonas aeruginosa. Environ Microbiol 16(3):676–688. https://doi.org/10.1111/1462-2920.12164
Ganne G, Brillet K, Basta B, Roche B, Hoegy F, Gasser V et al (2017) Iron release from the siderophore pyoverdine in Pseudomonas aeruginosa involves three new actors: FpvC, FpvG, and FpvH. ACS Chem Biol 12(4):1056–1065. https://doi.org/10.1021/acschembio.6b01077
Ge L, Seah SY (2006) Heterologous expression, purification, and characterization of an l-ornithine N(5)-hydroxylase involved in pyoverdine siderophore biosynthesis in Pseudomonas aeruginosa. J Bacteriol 188(20):7205–7210. https://doi.org/10.1128/JB.00949-06
Ghysels B, Ochsner U, Mollman U, Heinisch L, Vasil M, Cornelis P et al (2005) The Pseudomonas aeruginosa pirA gene encodes a second receptor for ferrienterobactin and synthetic catecholate analogues. FEMS Microbiol Lett 246(2):167–174. https://doi.org/10.1016/j.femsle.2005.04.010
Imperi F, Putignani L, Tiburzi F, Ambrosi C, Cipollone R, Ascenzi P et al (2008) Membrane-association determinants of the omega-amino acid monooxygenase PvdA, a pyoverdine biosynthetic enzyme from Pseudomonas aeruginosa. Microbiol (Reading) 154(Pt 9):2804–2813. https://doi.org/10.1099/mic.0.2008/018804-0
Imperi F, Tiburzi F, Fimia GM, Visca P (2010) Transcriptional control of the pvdS iron starvation sigma factor gene by the master regulator of sulfur metabolism CysB in Pseudomonas aeruginosa. Environ Microbiol 12(6):1630–1642. https://doi.org/10.1111/j.1462-2920.2010.02210.x
Kong W, Zhao J, Kang H, Zhu M, Zhou T, Deng X et al (2015) ChIP-seq reveals the global regulator AlgR mediating cyclic di-GMP synthesis in Pseudomonas aeruginosa. Nucleic Acids Res 43(17):8268–8282. https://doi.org/10.1093/nar/gkv747
Little AS, Okkotsu Y, Reinhart AA, Damron FH, Barbier M, Barrett B et al (2018) Pseudomonas aeruginosa AlgR phosphorylation status differentially regulates pyocyanin and pyoverdine production. MBio. https://doi.org/10.1128/mBio.02318-17
Llamas MA, Mooij MJ, Sparrius M, Vandenbroucke-Grauls CM, Ratledge C, Bitter W (2008) Characterization of five novel Pseudomonas aeruginosa cell-surface signalling systems. Mol Microbiol 67(2):458–472. https://doi.org/10.1111/j.1365-2958.2007.06061.x
Llamas MA, Imperi F, Visca P, Lamont IL (2014) Cell-surface signaling in Pseudomonas: stress responses, iron transport, and pathogenicity. FEMS Microbiol Rev 38(4):569–597. doi: https://doi.org/10.1111/1574-6976.12078
Lyczak JB, Cannon CL, Pier GB (2000) Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2(9):1051–1060. https://doi.org/10.1016/s1286-4579(00)01259-4
Meyer JM, Neely A, Stintzi A, Georges C, Holder IA (1996) Pyoverdin is essential for virulence of Pseudomonas aeruginosa. Infect Immun 64(2):518–523. https://doi.org/10.1128/iai.64.2.518-523.1996
Mossialos D, Ochsner U, Baysse C, Chablain P, Pirnay JP, Koedam N et al (2002) Identification of new, conserved, non-ribosomal peptide synthetases from fluorescent pseudomonads involved in the biosynthesis of the siderophore pyoverdine. Mol Microbiol 45(6):1673–1685. doi: https://doi.org/10.1046/j.1365-2958.2002.03120.x
Ochsner UA, Vasil AI, Vasil ML (1995) Role of the ferric uptake regulator of Pseudomonas aeruginosa in the regulation of siderophores and exotoxin A expression: purification and activity on iron-regulated promoters. J Bacteriol 177(24):7194–7201. https://doi.org/10.1128/jb.177.24.7194-7201.1995
Ochsner UA, Vasil ML, Alsabbagh E, Parvatiyar K, Hassett DJ (2000) Role of the Pseudomonas aeruginosa oxyR-recG operon in oxidative stress defense and DNA repair: OxyR-dependent regulation of katB-ankB, ahpB, and ahpC-ahpF. J Bacteriol 182(16):4533–4544. https://doi.org/10.1128/JB.182.16.4533-4544.2000
Ochsner UA, Wilderman PJ, Vasil AI, Vasil ML (2002) GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol Microbiol 45(5):1277–1287. https://doi.org/10.1046/j.1365-2958.2002.03084.x
Pletzer D, Braun Y, Weingart H (2016) Swarming motility is modulated by expression of the putative xenosiderophore transporter SppR-SppABCD in Pseudomonas aeruginosa PA14. Antonie Van Leeuwenhoek 109(6):737–753. https://doi.org/10.1007/s10482-016-0675-8
Ravel J, Cornelis P (2003) Genomics of pyoverdine-mediated iron uptake in pseudomonads. Trends Microbiol 11(5):195–200
Reen FJ, Haynes JM, Mooij MJ, O’Gara F (2013) A non-classical LysR-type transcriptional regulator PA2206 is required for an effective oxidative stress response in Pseudomonas aeruginosa. PLoS ONE 8(1):e54479. https://doi.org/10.1371/journal.pone.0054479
Schulz S, Eckweiler D, Bielecka A, Nicolai T, Franke R, Dotsch A et al (2015) Elucidation of sigma factor-associated networks in Pseudomonas aeruginosa reveals a modular architecture with limited and function-specific crosstalk. PLoS Pathog 11(3):e1004744. https://doi.org/10.1371/journal.ppat.1004744
Trouillon J, Imbert L, Villard AM, Vernet T, Attree I, Elsen S (2021) Determination of the two-component systems regulatory network reveals core and accessory regulations across Pseudomonas aeruginosa lineages. Nucleic Acids Res. https://doi.org/10.1093/nar/gkab928
Vinckx T, Matthijs S, Cornelis P (2008) Loss of the oxidative stress regulator OxyR in Pseudomonas aeruginosa PAO1 impairs growth under iron-limited conditions. FEMS Microbiol Lett 288(2):258–265. https://doi.org/10.1111/j.1574-6968.2008.01360.x
Visca P, Imperi F, Lamont IL (2007) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15(1):22–30. doi: https://doi.org/10.1016/j.tim.2006.11.004
Wei Q, Minh PN, Dotsch A, Hildebrand F, Panmanee W, Elfarash A et al (2012) Global regulation of gene expression by OxyR in an important human opportunistic pathogen. Nucleic Acids Res 40(10):4320–4333. doi: https://doi.org/10.1093/nar/gks017
Wilderman PJ, Vasil AI, Johnson Z, Wilson MJ, Cunliffe HE, Lamont IL et al (2001) Characterization of an endoprotease (PrpL) encoded by a PvdS-regulated gene in Pseudomonas aeruginosa. Infect Immun 69(9):5385–5394. https://doi.org/10.1128/IAI.69.9.5385-5394.2001
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Cornelis, P., Tahrioui, A., Lesouhaitier, O. et al. High affinity iron uptake by pyoverdine in Pseudomonas aeruginosa involves multiple regulators besides Fur, PvdS, and FpvI. Biometals 36, 255–261 (2023). https://doi.org/10.1007/s10534-022-00369-6
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DOI: https://doi.org/10.1007/s10534-022-00369-6