The Two-component Regulators GacS and GacA Positively Regulate a Nonfluorescent Siderophore Through the Gac/Rsm Signaling Cascade in High-siderophore-yielding Pseudomonas Sp. Strain HYS

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 2014 Jul 2

PMID 24982309

Citations 14

Authors

Xinyan Yu

Min Chen

Zhen Jiang

Yi Hu

Zhixiong Xie

Affiliations

Soon will be listed here.

Abstract

Siderophores, which are produced to overcome iron deficiency, are believed to be closely related to the adaptability of bacteria. The high-siderophore-yielding Pseudomonas sp. strain HYS simultaneously secretes the fluorescent siderophore pyoverdine and another nonfluorescent siderophore that is a major contributor to the high siderophore yield. Transposon mutagenesis revealed siderophore-related genes, including the two-component regulators GacS/GacA and a special cluster containing four open reading frames (the nfs cluster). Deletion mutations of these genes abolished nonfluorescent-siderophore production, and expression of the nfs cluster depended on gacA, indicating that gacS-gacA may control the nonfluorescent siderophore through regulation of the nfs cluster. Furthermore, regulation of the nonfluorescent siderophore by GacS/GacA involved the Gac/Rsm pathway. In contrast, inactivation of GacS/GacA led to upregulation of the fluorescent pyoverdine. The two siderophores were secreted under different iron conditions, probably because of differential effects of GacS/GacA. The global GacS/GacA regulatory system may control iron uptake by modulating siderophore production and may enable bacteria to adapt to changing iron environments.

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References

Cornelis P . Iron uptake and metabolism in pseudomonads. Appl Microbiol Biotechnol. 2010; 86(6):1637-45. DOI: 10.1007/s00253-010-2550-2. View

Yang L, Nilsson M, Gjermansen M, Givskov M, Tolker-Nielsen T . Pyoverdine and PQS mediated subpopulation interactions involved in Pseudomonas aeruginosa biofilm formation. Mol Microbiol. 2009; 74(6):1380-92. DOI: 10.1111/j.1365-2958.2009.06934.x. View

Reimmann C, Valverde C, Kay E, Haas D . Posttranscriptional repression of GacS/GacA-controlled genes by the RNA-binding protein RsmE acting together with RsmA in the biocontrol strain Pseudomonas fluorescens CHA0. J Bacteriol. 2004; 187(1):276-85. PMC: 538806. DOI: 10.1128/JB.187.1.276-285.2005. View

Cassat J, Skaar E . Iron in infection and immunity. Cell Host Microbe. 2013; 13(5):509-519. PMC: 3676888. DOI: 10.1016/j.chom.2013.04.010. View

Pernestig A, Melefors O, Georgellis D . Identification of UvrY as the cognate response regulator for the BarA sensor kinase in Escherichia coli. J Biol Chem. 2000; 276(1):225-31. DOI: 10.1074/jbc.M001550200. View

Schwyn B, NEILANDS J . Universal chemical assay for the detection and determination of siderophores. Anal Biochem. 1987; 160(1):47-56. DOI: 10.1016/0003-2697(87)90612-9. View

Andrews S, Robinson A, Rodriguez-Quinones F . Bacterial iron homeostasis. FEMS Microbiol Rev. 2003; 27(2-3):215-37. DOI: 10.1016/S0168-6445(03)00055-X. View

Ratledge C, Dover L . Iron metabolism in pathogenic bacteria. Annu Rev Microbiol. 2000; 54:881-941. DOI: 10.1146/annurev.micro.54.1.881. View

Kulasekara H, Ventre I, Kulasekara B, Lazdunski A, Filloux A, Lory S . A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol Microbiol. 2005; 55(2):368-80. DOI: 10.1111/j.1365-2958.2004.04402.x. View

10.

Lapouge K, Schubert M, Allain F, Haas D . Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. Mol Microbiol. 2007; 67(2):241-53. DOI: 10.1111/j.1365-2958.2007.06042.x. View

11.

NEILANDS J . Siderophores: structure and function of microbial iron transport compounds. J Biol Chem. 1995; 270(45):26723-6. DOI: 10.1074/jbc.270.45.26723. View

12.

Kay E, Humair B, Denervaud V, Riedel K, Spahr S, Eberl L . Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J Bacteriol. 2006; 188(16):6026-33. PMC: 1540078. DOI: 10.1128/JB.00409-06. View

13.

Miethke M, Marahiel M . Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev. 2007; 71(3):413-51. PMC: 2168645. DOI: 10.1128/MMBR.00012-07. View

14.

Matthijs S, Abbaspour Tehrani K, Laus G, Jackson R, Cooper R, Cornelis P . Thioquinolobactin, a Pseudomonas siderophore with antifungal and anti-Pythium activity. Environ Microbiol. 2007; 9(2):425-34. DOI: 10.1111/j.1462-2920.2006.01154.x. View

15.

Braun V, Killmann H . Bacterial solutions to the iron-supply problem. Trends Biochem Sci. 1999; 24(3):104-9. DOI: 10.1016/s0968-0004(99)01359-6. View

16.

Mercado-Blanco J, van der Drift K, Olsson P, Thomas-Oates J, van Loon L, Bakker P . Analysis of the pmsCEAB gene cluster involved in biosynthesis of salicylic acid and the siderophore pseudomonine in the biocontrol strain Pseudomonas fluorescens WCS374. J Bacteriol. 2001; 183(6):1909-20. PMC: 95085. DOI: 10.1128/JB.183.6.1909-1920.2001. View

17.

Gao J, Yu X, Xie Z . Draft genome sequence of high-siderophore-yielding Pseudomonas sp. strain HYS. J Bacteriol. 2012; 194(15):4121. PMC: 3416532. DOI: 10.1128/JB.00688-12. View

18.

Hassan K, Johnson A, Shaffer B, Ren Q, Kidarsa T, Elbourne L . Inactivation of the GacA response regulator in Pseudomonas fluorescens Pf-5 has far-reaching transcriptomic consequences. Environ Microbiol. 2010; 12(4):899-915. DOI: 10.1111/j.1462-2920.2009.02134.x. View

19.

Franza T, Mahe B, Expert D . Erwinia chrysanthemi requires a second iron transport route dependent of the siderophore achromobactin for extracellular growth and plant infection. Mol Microbiol. 2004; 55(1):261-75. DOI: 10.1111/j.1365-2958.2004.04383.x. View

20.

Crosa J, Walsh C . Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev. 2002; 66(2):223-49. PMC: 120789. DOI: 10.1128/MMBR.66.2.223-249.2002. View