A unique ferrous iron binding mode is associated with large conformational changes for the transport protein FpvC of Pseudomonas aeruginosa.
Pseudomonas aeruginosa
iron
pyoverdine
siderophore
solute-binding protein
Journal
The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
16
04
2019
revised:
18
06
2019
accepted:
16
07
2019
pubmed:
19
7
2019
medline:
21
10
2020
entrez:
19
7
2019
Statut:
ppublish
Résumé
Pseudomonas aeruginosa secretes pyoverdine, a major siderophore to get access to iron, an essential nutrient. Pyoverdine scavenges ferric iron in the bacterial environment with the resulting complex internalized by bacteria. Releasing of iron from pyoverdine in the periplasm involves an iron reduction by an inner membrane reductase and two solute-binding proteins (SBPs) FpvC and FpvF in association with their ABC transporter. FpvC and FpvF belong to two different subgroups of SBPs within the structural cluster A: FpvC and FpvF were proposed to be a metal-binding protein and a ferrisiderophore-binding protein respectively. Here, we report the redox state and the binding mode of iron to FpvC. We first solved the crystal structure of FpvC bound to a fortuitous Ni
Substances chimiques
Bacterial Outer Membrane Proteins
0
Oligopeptides
0
Solute Carrier Proteins
0
Nickel
7OV03QG267
pyoverdin
8062-00-8
Iron
E1UOL152H7
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
295-309Informations de copyright
© 2019 Federation of European Biochemical Societies.
Références
Lyczak JB, Cannon CL & Pier GB (2000) Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2, 1051-1060.
Boukhalfa H & Crumbliss AL (2002) Chemical aspects of siderophore mediated iron transport. Biometals 15, 325-339.
Schalk IJ, Mislin GL & Brillet K (2012) Structure, function and binding selectivity and stereoselectivity of siderophore-iron outer membrane transporters. Curr Top Membr 69, 37-66.
Schalk IJ & Guillon L (2013) Fate of ferrisiderophores after import across bacterial outer membranes: different iron release strategies are observed in the cytoplasm or periplasm depending on the siderophore pathways. Amino Acids 44, 1267-1277.
Schalk IJ & Guillon L (2013) Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: implications for metal homeostasis. Environ Microbiol 15, 1661-1673.
Poole K, Neshat S, Krebes K & Heinrichs DE (1993) Cloning and nucleotide sequence analysis of the ferripyoverdine receptor gene fpvA of Pseudomonas aeruginosa. J Bacteriol 175, 4597-4604.
Ghysels B, Dieu BT, Beatson SA, Pirnay JP, Ochsner UA, Vasil ML & Cornelis P (2004) FpvB, an alternative type I ferripyoverdine receptor of Pseudomonas aeruginosa. Microbiology 150, 1671-1680.
Brillet K, Journet L, Celia H, Paulus L, Stahl A, Pattus F & Cobessi D (2007) A beta strand lock exchange for signal transduction in TonB-dependent transducers on the basis of a common structural motif. Structure 15, 1383-1391.
Schalk IJ, Abdallah MA & Pattus F (2002) Recycling of pyoverdin on the FpvA receptor after ferric pyoverdin uptake and dissociation in Pseudomonas aeruginosa. Biochemistry 41, 1663-1671.
Greenwald J, Hoegy F, Nader M, Journet L, Mislin GL, Graumann PL & Schalk IJ (2007) Real time fluorescent resonance energy transfer visualization of ferric pyoverdine uptake in Pseudomonas aeruginosa. A role for ferrous iron. J Biol Chem 282, 2987-2995.
Yeterian E, Martin LW, Lamont IL & Schalk IJ (2010) An efflux pump is required for siderophore recycling by Pseudomonas aeruginosa. Environ Microbiol Rep 2, 412-418.
Ganne G, Brillet K, Basta B, Roche B, Hoegy F, Gasser V & Schalk IJ (2017) Iron Release from the Siderophore Pyoverdine in Pseudomonas aeruginosa Involves Three New Actors: FpvC, FpvG, and FpvH. ACS Chem Biol 12, 1056-1065.
Brillet K, Ruffenach F, Adams H, Journet L, Gasser V, Hoegy F, Guillon L, Hannauer M, Page A & Schalk IJ (2012) An ABC transporter with two periplasmic binding proteins involved in iron acquisition in Pseudomonas aeruginosa. ACS Chem Biol 7, 2036-2045.
Lee YH, Deka RK, Norgard MV, Radolf JD & Hasemann CA (1999) Treponema pallidum TroA is a periplasmic zinc-binding protein with a helical backbone. Nat Struct Biol 6, 628-633.
Berntsson RP, Smits SH, Schmitt L, Slotboom DJ & Poolman B (2010) A structural classification of substrate-binding proteins. FEBS Lett 584, 2606-2617.
Sigfridsson KG, Chernev P, Leidel N, Popovic-Bijelic A, Graslund A & Haumann M (2013) Rapid X-ray photoreduction of dimetal-oxygen cofactors in ribonucleotide reductase. J Biol Chem 288, 9648-9661.
Peisach J, Blumberg WE, Lode ET & Coon MJ (1971) An analysis of the electron paramagnetic resonance spectrum of pseudomonas oleovorans rubredoxin. A method for determination of the liganids of ferric iron in completely rhombic sites. J Biol Chem 246, 5877-5881.
Radka CD, DeLucas LJ, Wilson LS, Lawrenz MB, Perry RD & Aller SG (2017) Crystal structure of Yersinia pestis virulence factor YfeA reveals two polyspecific metal-binding sites. Acta Crystallogr D Struct Biol 73, 557-572.
Zheng B, Zhang Q, Gao J, Han H, Li M, Zhang J, Qi J, Yan J & Gao GF (2011) Insight into the interaction of metal ions with TroA from Streptococcus suis. PLoS ONE 6, e19510.
Yatsunyk LA, Easton JA, Kim LR, Sugarbaker SA, Bennett B, Breece RM, Vorontsov II, Tierney DL, Crowder MW & Rosenzweig AC (2008) Structure and metal binding properties of ZnuA, a periplasmic zinc transporter from Escherichia coli. J Biol Inorg Chem 13, 271-288.
Sun X, Baker HM, Ge R, Sun H, He QY & Baker EN (2009) Crystal structure and metal binding properties of the lipoprotein MtsA, responsible for iron transport in Streptococcus pyogenes. Biochemistry 48, 6184-6190.
Damo SM, Kehl-Fie TE, Sugitani N, Holt ME, Rathi S, Murphy WJ, Zhang Y, Betz C, Hench L, Fritz G et al. (2013) Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc Natl Acad Sci USA 110, 3841-3846.
Nakashige TG, Zygiel EM, Drennan CL & Nolan EM (2017) Nickel sequestration by the host-defense protein human calprotectin. J Am Chem Soc 139, 8828-8836.
Srivastava SS, Jamkhindikar AA, Raman R, Jobby MK, Chadalawada S, Sankaranarayanan R & Sharma Y (2017) A transition metal-binding, trimeric betagamma-crystallin from methane-producing Thermophilic Archaea, Methanosaeta thermophila. Biochemistry 56, 1299-1310.
Browning C, Shneider MM, Bowman VD, Schwarzer D & Leiman PG (2012) Phage pierces the host cell membrane with the iron-loaded spike. Structure 20, 326-339.
Bartual SG, Otero JM, Garcia-Doval C, Llamas-Saiz AL, Kahn R, Fox GC & van Raaij MJ (2010) Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proc Natl Acad Sci USA 107, 20287-20292.
Koc C, Xia G, Kuhner P, Spinelli S, Roussel A, Cambillau C & Stehle T (2016) Structure of the host-recognition device of Staphylococcus aureus phage varphi11. Sci Rep 6, 27581.
Carver G, Tregenna-Piggott PL, Barra AL, Neels A & Stride JA (2003) Spectroscopic and structural characterization of the [Fe(imidazole)(6)](2+) cation. Inorg Chem 42, 5771-5777.
Counago RM, Ween MP, Begg SL, Bajaj M, Zuegg J, O'Mara ML, Cooper MA, McEwan AG, Paton JC, Kobe B et al. (2014) Imperfect coordination chemistry facilitates metal ion release in the Psa permease. Nat Chem Biol 10, 35-41.
de Boer M, Gouridis G, Vietrov R, Begg SL, Schuurman-Wolters GK, Husada F, Eleftheriadis N, Poolman B, McDevitt CA & Cordes T (2019) Conformational and dynamic plasticity in substrate-binding proteins underlies selective transport in ABC importers. Elife 8, pii: e44652.
Nakashige TG & Nolan EM (2017) Human calprotectin affects the redox speciation of iron. Metallomics 9, 1086-1095.
Dudev T & Lim C (2008) Metal binding affinity and selectivity in metalloproteins: insights from computational studies. Annu Rev Biophys 37, 97-116.
Waldron KJ, Rutherford JC, Ford D & Robinson NJ (2009) Metalloproteins and metal sensing. Nature 460, 823-830.
Hannauer M, Braud A, Hoegy F, Ronot P, Boos A & Schalk IJ (2012) The PvdRT-OpmQ efflux pump controls the metal selectivity of the iron uptake pathway mediated by the siderophore pyoverdine in Pseudomonas aeruginosa. Environ Microbiol 14, 1696-1708.
Visca P, Leoni L, Wilson MJ & Lamont IL (2002) Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas. Mol Microbiol 45, 1177-1190.
Kabsch W (2010) Xds. Acta Crystallogr D Biol Crystallogr 66, 125-132.
McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC & Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40, 658-674.
Blanc E, Roversi P, Vonrhein C, Flensburg C, Lea SM & Bricogne G (2004) Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr D Biol Crystallogr 60, 2210-2221.
Emsley P & Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132.
Sreerama N & Woody RW (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287, 252-260.
Whitmore L & Wallace BA (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32, W668-W673.
Wiseman T, Williston S, Brandts JF & Lin LN (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem 179, 131-137.