High Affinity Iron Uptake by Pyoverdine in Pseudomonas Aeruginosa Involves Multiple Regulators Besides Fur, PvdS, and FpvI

Overview

Journal Biometals

Specialty Biochemistry

Date 2022 Feb 16

PMID 35171432

Authors

Pierre Cornelis

Ali Tahrioui

Olivier Lesouhaitier

Emeline Bouffartigues

Marc Feuilloley

Christine Baysse

Sylvie Chevalier

Affiliations

Soon will be listed here.

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 Fe to Fe and the transport of ferrous iron to the cytoplasm that appears to represent a crucial step in the uptake process.

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References

Attila C, Ueda A, Wood T . PA2663 (PpyR) increases biofilm formation in Pseudomonas aeruginosa PAO1 through the psl operon and stimulates virulence and quorum-sensing phenotypes. Appl Microbiol Biotechnol. 2007; 78(2):293-307. DOI: 10.1007/s00253-007-1308-y. View

Beare P, For R, Martin L, Lamont I . Siderophore-mediated cell signalling in Pseudomonas aeruginosa: divergent pathways regulate virulence factor production and siderophore receptor synthesis. Mol Microbiol. 2002; 47(1):195-207. DOI: 10.1046/j.1365-2958.2003.03288.x. View

Blanka A, Schulz S, Eckweiler D, Franke R, Bielecka A, Nicolai T . Identification of the alternative sigma factor SigX regulon and its implications for Pseudomonas aeruginosa pathogenicity. J Bacteriol. 2013; 196(2):345-56. PMC: 3911239. DOI: 10.1128/JB.01034-13. View

Boechat A, Kaihami G, Politi M, Lepine F, Baldini R . A novel role for an ECF sigma factor in fatty acid biosynthesis and membrane fluidity in Pseudomonas aeruginosa. PLoS One. 2014; 8(12):e84775. PMC: 3875570. DOI: 10.1371/journal.pone.0084775. View

Bonneau A, Roche B, Schalk I . Iron acquisition in Pseudomonas aeruginosa by the siderophore pyoverdine: an intricate interacting network including periplasmic and membrane proteins. Sci Rep. 2020; 10(1):120. PMC: 6954188. DOI: 10.1038/s41598-019-56913-x. View

Bouffartigues E, Si Hadj Mohand I, Maillot O, Tortuel D, Omnes J, David A . The Temperature-Regulation of Operon Reveals an Intriguing Molecular Network Involving the Sigma Factors AlgU and SigX. Front Microbiol. 2020; 11:579495. PMC: 7641640. DOI: 10.3389/fmicb.2020.579495. View

Brillet K, Ruffenach F, Adams H, Journet L, Gasser V, Hoegy F . An ABC transporter with two periplasmic binding proteins involved in iron acquisition in Pseudomonas aeruginosa. ACS Chem Biol. 2012; 7(12):2036-45. DOI: 10.1021/cb300330v. View

Ren A, Jia M, Liu J, Zhou T, Wu L, Dong T . Acquisition of T6SS Effector TseL Contributes to the Emerging of Novel Epidemic Strains of Pseudomonas aeruginosa. Microbiol Spectr. 2022; 11(1):e0330822. PMC: 9927574. DOI: 10.1128/spectrum.03308-22. View

Chevalier S, Bouffartigues E, Bazire A, Tahrioui A, Duchesne R, Tortuel D . Extracytoplasmic function sigma factors in Pseudomonas aeruginosa. Biochim Biophys Acta Gene Regul Mech. 2018; 1862(7):706-721. DOI: 10.1016/j.bbagrm.2018.04.008. View

10.

Cornelis P, Dingemans J . Pseudomonas aeruginosa adapts its iron uptake strategies in function of the type of infections. Front Cell Infect Microbiol. 2013; 3:75. PMC: 3827675. DOI: 10.3389/fcimb.2013.00075. View

11.

Escolar L, Perez-Martin J, de Lorenzo V . Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol. 1999; 181(20):6223-9. PMC: 103753. DOI: 10.1128/JB.181.20.6223-6229.1999. View

12.

Flechard M, Duchesne R, Tahrioui A, Bouffartigues E, Depayras S, Hardouin J . The absence of SigX results in impaired carbon metabolism and membrane fluidity in Pseudomonas aeruginosa. Sci Rep. 2018; 8(1):17212. PMC: 6249292. DOI: 10.1038/s41598-018-35503-3. View

13.

Frangipani E, Visaggio D, Heeb S, Kaever V, Camara M, Visca P . The Gac/Rsm and cyclic-di-GMP signalling networks coordinately regulate iron uptake in Pseudomonas aeruginosa. Environ Microbiol. 2013; 16(3):676-88. DOI: 10.1111/1462-2920.12164. View

14.

Ganne G, Brillet K, Basta B, Roche B, Hoegy F, Gasser V . Iron Release from the Siderophore Pyoverdine in Pseudomonas aeruginosa Involves Three New Actors: FpvC, FpvG, and FpvH. ACS Chem Biol. 2017; 12(4):1056-1065. DOI: 10.1021/acschembio.6b01077. View

15.

Ge L, Seah S . Heterologous expression, purification, and characterization of an l-ornithine N(5)-hydroxylase involved in pyoverdine siderophore biosynthesis in Pseudomonas aeruginosa. J Bacteriol. 2006; 188(20):7205-10. PMC: 1636248. DOI: 10.1128/JB.00949-06. View

16.

Ghysels B, Ochsner U, Mollman U, Heinisch L, Vasil M, Cornelis P . The Pseudomonas aeruginosa pirA gene encodes a second receptor for ferrienterobactin and synthetic catecholate analogues. FEMS Microbiol Lett. 2005; 246(2):167-74. DOI: 10.1016/j.femsle.2005.04.010. View

17.

Imperi F, Tiburzi F, Fimia G, Visca P . Transcriptional control of the pvdS iron starvation sigma factor gene by the master regulator of sulfur metabolism CysB in Pseudomonas aeruginosa. Environ Microbiol. 2010; 12(6):1630-42. DOI: 10.1111/j.1462-2920.2010.02210.x. View

18.

Kong W, Zhao J, Kang H, Zhu M, Zhou T, Deng X . ChIP-seq reveals the global regulator AlgR mediating cyclic di-GMP synthesis in Pseudomonas aeruginosa. Nucleic Acids Res. 2015; 43(17):8268-82. PMC: 4787818. DOI: 10.1093/nar/gkv747. View

19.

Little A, Okkotsu Y, Reinhart A, Damron F, Barbier M, Barrett B . AlgR Phosphorylation Status Differentially Regulates Pyocyanin and Pyoverdine Production. mBio. 2018; 9(1). PMC: 5790918. DOI: 10.1128/mBio.02318-17. View

20.

Llamas M, Mooij M, Sparrius M, Vandenbroucke-Grauls C, Ratledge C, Bitter W . Characterization of five novel Pseudomonas aeruginosa cell-surface signalling systems. Mol Microbiol. 2007; 67(2):458-72. DOI: 10.1111/j.1365-2958.2007.06061.x. View