Beinert, H. Iron-sulfur proteins: ancient structures, still full of surprises. J. Biol. Inorg. Chem. 5, 2–15 (2000). A review from a pioneer in the Fe–S protein field.

Article  CAS  PubMed  Google Scholar 

Fontecave, M. Iron-sulfur clusters: ever-expanding roles. Nature Chem. Biol. 2, 171–174 (2006).

Article  CAS  Google Scholar 

Kiley, P. J. & Beinert, H. The role of Fe-S proteins in sensing and regulation in bacteria. Curr. Opin. Microbiol. 6, 181–185 (2003).

Article  CAS  PubMed  Google Scholar 

Ayala-Castro, C., Saini, A. & Outten, F. W. Fe-S cluster assembly pathways in bacteria. Microbiol. Mol. Biol. Rev. 72, 110–125 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Fontecave, M., Py, B., Ollagnier de Choudens, S. & Barras, F. From iron and cysteine to iron-sulfur clusters: the biogenesis protein machineries. Ecosal [online] (2008).

Xu, X. M. & Møller, S. G. Iron-sulfur cluster biogenesis systems and their crosstalk. Chembiochem. 9, 2355–2362 (2008).

Article  CAS  PubMed  Google Scholar 

Lill, R. & Mühlenhoff, U. Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu. Rev. Biochem. 77, 669–700 (2008).

Article  CAS  PubMed  Google Scholar 

Rouault, T. A. & Tong, W. H. Iron-sulfur cluster biogenesis and human disease. Trends Genet. 24, 398–407 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Kessler, D. & Papenbrock, J. Iron-sulfur cluster biosynthesis in photosynthetic organisms. Photosynth. Res. 86, 391–407 (2005).

Article  CAS  PubMed  Google Scholar 

Balk, J. & Lobréaux, S. Biogenesis of iron-sulfur proteins in plants. Trends Plant. Sci. 10, 324–331 (2005).

Article  CAS  PubMed  Google Scholar 

Imlay, J. A. Iron-sulphur clusters and the problem with oxygen. Mol. Microbiol. 59, 1073–1082 (2006). A perspective on the use of Fe–S proteins in relation to the evolution of Earth's atmosphere.

Article  PubMed  Google Scholar 

Kuo, C. F., Mashino, T. & Fridovich, I. α,β-Dihydroxyisovalerate dehydratase. A superoxide-sensitive enzyme. J. Biol. Chem. 262, 4724–4727 (1987). A seminal paper on the relationship between oxidative stress and Fe–S proteins.

CAS  PubMed  Google Scholar 

Flint, D. H., Tuminello, J. F. & Emptage, M. H. The inactivation of Fe-S cluster containing hydrolyases by superoxide. J. Biol. Chem. 268, 22369–22376 (1993).

CAS  PubMed  Google Scholar 

Keyer, K. & Imlay, J. A. Inactivation of dehydratase [4Fe-4S] clusters and disruption of iron homeostasis upon cell exposure to peroxynitrite. J. Biol. Chem. 272, 27652–27659 (1997).

Article  CAS  PubMed  Google Scholar 

Jang, S. & Imlay, J. A. Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J. Biol. Chem. 282, 929–937 (2007).

Article  CAS  PubMed  Google Scholar 

Imlay, J. A. Pathways of oxidative damage. Annu. Rev. Microbiol. 57, 395–418 (2003).

Article  CAS  PubMed  Google Scholar 

Mello Filho, A. C., Hoffmann, M. E. & Meneghini, R. Cell killing and DNA damage by hydrogen peroxide are mediated by intracellular iron. Biochem. J. 218, 273–275 (1984).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Imlay, J. A., Chin, S. M. & Linn., S. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240, 640–642 (1988).

Article  CAS  PubMed  Google Scholar 

Kohanski, M. A., Dwyer, D. J., Hayete, B., Lawrence, C. A. & Collins, J. J. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130, 797–810 (2007).

Article  CAS  PubMed  Google Scholar 

Jacobson, M. R. et al. Biochemical and genetic analysis of the nifUSVWZM cluster from Azotobacter vinelandii. Mol. Gen. Genet. 219, 49–57 (1989). A landmark article signalling the start of the research into bacterial Fe–S cluster biogenesis.

Article  CAS  PubMed  Google Scholar 

Zheng, L., Cash, V. L., Flint, D. H. & Dean, D. R. Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J. Biol. Chem. 273, 13264–13272 (1998). This paper reports the identification of the Isc system.

Article  CAS  PubMed  Google Scholar 

Patzer, S. I. & Hantke, K. SufS is a NifS-like protein, and SufD is necessary for stability of the [2Fe-2S] FhuF protein in Escherichia coli. J. Bacteriol. 181, 3307–3309 (1999).

CAS  PubMed  PubMed Central  Google Scholar 

Nachin, L., El Hassouni, M., Loiseau, L., Expert, D. & Barras, F. SoxR-dependent response to oxidative stress and virulence of Erwinia chrysanthemi: the key role of SufC, an orphan ABC ATPase. Mol. Microbiol. 39, 960–972 (2001).

Article  CAS  PubMed  Google Scholar 

Takahashi, Y. & Tokumoto, U. A third bacterial system for the assembly of iron-sulfur clusters with homologs in archaea and plastids. J. Biol. Chem. 277, 28380–28383 (2002). This paper reports the identification of the Suf system.

Article  CAS  PubMed  Google Scholar 

Outten, F. W., Djaman, O. & Storz, G. A suf operon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli. Mol. Microbiol. 52, 861–872 (2004).

Article  CAS  PubMed  Google Scholar 

Johnson, D. C., Unciuleac, M. C. & Dean, D. R. Controlled expression and functional analysis of iron-sulfur cluster biosynthetic components within Azotobacter vinelandii. J. Bacteriol. 188, 7551–7561 (2006).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Olson, J. W., Agar, J. N., Johnson, M. K. & Maier, R. J. Characterization of the NifU and NifS Fe-S cluster formation proteins essential for viability in Helicobacter pylori. Biochemistry 39, 16213–16219 (2000).

Article  CAS  PubMed  Google Scholar 

Takahashi, Y. & Nakamura, M. Functional assignment of the ORF2-iscS-iscU-iscA-hscB-hscA-fdx-ORF3 gene cluster involved in the assembly of Fe-S clusters in Escherichia coli. J. Biochem. 126, 917–926 (1999).

Article  CAS  PubMed  Google Scholar 

Tokumoto, U. & Takahashi, Y. Genetic analysis of the isc operon in Escherichia coli involved in the biogenesis of cellular iron-sulfur proteins. J. Biochem. 130, 63–71 (2001).

Article  CAS  PubMed  Google Scholar 

Rincon-Enriquez, G., Crété, P., Barras, F. & Py, B. Biogenesis of Fe/S proteins and pathogenicity: IscR plays a key role in allowing Erwinia chrysanthemi to adapt to hostile conditions. Mol. Microbiol. 67, 1257–1273 (2008).

Article  CAS  PubMed  Google Scholar 

Huet, G., Daffé, M. & Saves, I. Identification of the Mycobacterium tuberculosis SUF machinery as the exclusive mycobacterial system of [Fe-S] cluster assembly: evidence for its implication in the pathogen's survival. J. Bacteriol. 187, 6137–6146 (2005).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Mihara, H. & Esaki, N. Bacterial cysteine desulfurases: their function and mechanisms. Appl. Microbiol. Biotechnol. 60, 12–23 (2002).

Article  CAS  PubMed  Google Scholar 

Zheng, L., White, R. H., Cash, V. L., Jack, R. F. & Dean, D. R. Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc. Natl Acad. Sci. USA 90, 2754–2758 (1993). The first identification of the source and the mechanism of sulphur mobilization for Fe–S cluster formation.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Flint, D. H. Escherichia coli contains a protein that is homologous in function and N-terminal sequence to the protein encoded by the nifS gene of Azotobacter vinelandii and that can participate in the synthesis of the Fe-S cluster of dihydroxy-acid dehydratase. J. Biol. Chem. 271, 16068–16074 (1996).

Article  CAS  PubMed  Google Scholar 

Mihara, H., Kurihara, T., Yoshimura, T. & Esaki, N. Kinetic and mutational studies of three NifS homologs from Escherichia coli: mechanistic difference between L-cysteine desulfurase and L-selenocysteine lyase reactions. J. Biochem. 127, 559–567 (2000).

Article  CAS  PubMed  Google Scholar 

Schwartz, C. J., Djaman, O., Imlay, J. A. & Kiley, P. J. The cysteine desulfurase, IscS, has a major role in in vivo Fe-S cluster formation in Escherichia coli. Proc. Natl Acad. Sci. USA 97, 9009–9014 (2000).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Mueller, E. G. Trafficking in persulfides: delivering sulfur in biosynthetic pathways. Nature Chem. Biol. 2, 185–194 (2006).

Article  CAS  Google Scholar 

Ikeuchi, Y., Shigi, N., Kato, J., Nishimura, A. & Suzuki, T. Mechanistic insights into sulfur relay by multiple sulfur mediators involved in thiouridine biosynthesis at tRNA wobble positions. Mol. Cell 21, 97–108 (2006).

Article  CAS  PubMed  Google Scholar 

Nilsson, K, Lundgren, H. K., Hagervall, T. G. & Björk, G. R. The cysteine desulfurase IscS is required for synthesis of all five thiolated nucleosides present in tRNA from Salmonella enterica serovar typhimurium. J. Bacteriol. 184, 6830–6835 (2002).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Lauhon, C. T. Requirement for IscS in biosynthesis of all thionucleosides in Escherichia coli. J. Bacteriol. 184, 6820–6829 (2002).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Nachin, L., Loiseau, L., Expert, D. & Barras, F. SufC: an unorthodox cytoplasmic ABC/ATPase required for [Fe-S] biogenesis under oxidative stress. EMBO J. 22, 427–437 (2003).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Lee, J. H., Yeo, W. S. & Roe, J. H. Induction of the sufA operon encoding Fe-S assembly proteins by superoxide generators and hydrogen peroxide: involvement of OxyR, IHF and an unidentified oxidant-responsive factor. Mol. Microbiol. 51, 1745–1755 (2004).

Article  CAS  PubMed  Google Scholar 

Yeo, W. S., Lee, J. H., Lee, K. C. & Roe, J. H. IscR acts as an activator in response to oxidative stress for the suf operon encoding Fe-S assembly proteins. Mol. Microbiol. 61, 206–218 (2006).

Article  CAS  PubMed  Google Scholar 

Lee, K. C., Yeo, W. S. & Roe, J. H. Oxidant-responsive induction of the suf operon, encoding a Fe-S assembly system, through Fur and IscR in Escherichia coli. J. Bacteriol. 190, 8244–8247 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Tokumoto, U., Kitamura, S., Fukuyama, K. & Takahashi, Y. Interchangeability and distinct properties of bacterial Fe-S cluster assembly systems: functional replacement of the isc and suf operons in Escherichia coli with the nifSU-like operon from Helicobacter pylori. J. Biochem. 136, 199–209 (2004).

Article  CAS  PubMed  Google Scholar 

Loiseau, L. et. al. Analysis of the heteromeric CsdA-CsdE cysteine desulfurase, assisting Fe-S cluster biogenesis in Escherichia coli. J. Biol. Chem. 280, 26760–26769 (2005).

Article  CAS  PubMed  Google Scholar 

Trotter, V. et al. The CsdA cysteine desulphurase promotes Fe/S biogenesis by recruiting Suf components and participates to a new sulphur transfer pathway by recruiting CsdL (ex-YgdL), a ubiquitin-modifying-like protein. Mol. Microbiol. 74, 1527–1542 (2009).

Article  CAS  PubMed  Google Scholar 

Urbina, H. D., Silberg, J. J., Hoff, K. G. & Vickery, L. E. Transfer of sulfur from IscS to IscU during Fe/S cluster assembly. J. Biol. Chem. 276, 44521–44526 (2001).

Article  CAS  PubMed  Google Scholar 

Smith, A. D. et al. Sulfur transfer from IscS to IscU: the first step in iron-sulfur cluster biosynthesis. J. Am. Chem. Soc. 123, 11103–11104 (2001).

Article  CAS  PubMed  Google Scholar 

Loiseau, L., Ollagnier de Choudens, S., Nachin, L., Fontecave, M. & Barras, F. Biogenesis of Fe-S cluster by the bacterial Suf system: SufS and SufE form a new type of cysteine desulfurase. J. Biol. Chem. 278, 38352–38359 (2003).

Article  CAS  PubMed  Google Scholar 

Ollagnier de Choudens, S. et al. Mechanistic studies of the SufS-SufE cysteine desulfurase: evidence for sulfur transfer from SufS to SufE. FEBS Lett. 555, 263–267 (2003).

Article  CAS  PubMed  Google Scholar 

Outten, F. W., Wood, M. J., Munoz, F. M. & Storz, G. The SufE protein and the SufBCD complex enhance SufS cysteine desulfurase activity as part of a sulfur transfer pathway for Fe-S cluster assembly in Escherichia coli. J. Biol. Chem. 278, 45713–45719 (2003).

Article  CAS  PubMed  Google Scholar 

Layer, G. et al.SufE transfers sulfur from SufS to SufB for iron-sulfur cluster assembly. J. Biol. Chem. 282, 13342–13350 (2007). The first evidence for the identification of SufBCD as the scaffold in the Suf system.

Article  CAS  PubMed  Google Scholar 

Sendra, M., Ollagnier de Choudens, S., Lascoux, D., Sanakis, Y. & Fontecave, M. The SUF iron-sulfur cluster biosynthetic machinery: sulfur transfer from the SUFS-SUFE complex to SUFA. FEBS Lett. 581, 1362–1368 (2007).

Article  CAS  PubMed  Google Scholar 

Layer, G., Ollagnier de Choudens, S., Sanakis, Y. & Fontecave, M. Iron-sulfur cluster biosynthesis: characterization of Escherichia coli CyaY as an iron donor for the assembly of [2Fe-2S] clusters in the scaffold IscU. J. Biol. Chem. 281, 16256–16263 (2006).

Article  CAS  PubMed  Google Scholar 

Adinolfi, S. et al. Bacterial frataxin CyaY is the gatekeeper of iron-sulfur cluster formation catalyzed by IscS. Nature Struct. Mol. Biol. 16, 390–396 (2009).

Article  CAS  Google Scholar 

Shi, R. et al. Structural basis for Fe–S cluster assembly and tRNA thiolation mediated by IscS protein–protein interactions. PLoS Biol. 8, e1000354 (2010).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Pandolfo, M. & Pastore, A. The pathogenesis of Friedreich ataxia and the structure and function of frataxin. J. Neurol. 256, 9–17 (2009).

Article  CAS  PubMed  Google Scholar 

Bou-Abdallah, F., Adinolfi, S., Pastore, A., Laue, T. M. & Chasteen, D. N. Iron binding and oxidation kinetics in frataxin CyaY of Escherichia coli. J. Mol. Biol. 341, 605–615 (2004).

Article  CAS  PubMed  Google Scholar 

Pastore, C., Franzese, M., Sica, F., Temussi, P. & Pastore, A. Understanding the binding properties of an unusual metal-binding protein-a study of bacterial frataxin. FEBS J. 274, 4199–4210 (2007).

Article  CAS  PubMed  Google Scholar 

Nair, M. et al. Solution structure of the bacterial frataxin ortholog, CyaY: mapping the iron binding sites. Structure 12, 2037–2048 (2004).

Article  CAS  PubMed  Google Scholar 

Li, D. S., Ohshima, K., Jiralerspong, S., Bojanowski, M. W. & Pandolfo, M. Knock-out of the cyaY gene in Escherichia coli does not affect cellular iron content and sensitivity to oxidants. FEBS Lett. 456, 13–16 (1999).

Article  CAS  PubMed  Google Scholar 

Vivas, E., Skovran, E. & Downs, D. M. Salmonella enterica strains lacking the frataxin homolog CyaY show defects in Fe-S cluster metabolism in vivo. J. Bacteriol. 188, 1175–1179 (2006).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Thorgersen, M. P. & Downs, D. M. Oxidative stress and disruption of labile iron generate specific auxotrophic requirements in Salmonella enterica. Microbiology 155, 295–304 (2009).

Article  CAS  PubMed  Google Scholar 

Ding, H. & Clark, R. J. Characterization of iron binding in IscA, an ancient iron-sulphur cluster assembly protein. Biochem. J. 379, 433–440 (2004).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Ding, H., Harrison, K. & Lu, J. Thioredoxin reductase system mediates iron binding in IscA and iron delivery for the iron-sulfur cluster assembly in IscU. J. Biol. Chem. 280, 30432–30437 (2005).

Article  CAS  PubMed  Google Scholar 

Yang, J., Bitoun, J. P. & Ding, H. Interplay of IscA and IscU in biogenesis of iron-sulfur clusters. J. Biol. Chem. 281, 27956–27963 (2006).

Article  CAS  PubMed  Google Scholar 

Lu, J., Yang, J., Tan, G. & Ding, H. Complementary roles of SufA and IscA in the biogenesis of iron-sulfur clusters in Escherichia coli. Biochem. J. 409, 535–543 (2008).

Article  CAS  PubMed  Google Scholar 

Djaman, O., Outten, F. W. & Imlay, J. A. Repair of oxidized iron-sulfur clusters in Escherichia coli. J. Biol. Chem. 279, 44590–44599 (2004). A rigorous testing of the hypothesis that an Fe–S cluster repair system exists.

Article  CAS  PubMed  Google Scholar 

Bitoun, J. P., Wu, G. & Ding, H. Escherichia coli FtnA acts as an iron buffer for re-assembly of iron-sulfur clusters in response to hydrogen peroxide stress. Biometals 21, 693–703 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Velayudhan, J., Castor, M., Richardson, A., Main-Hester, K. L. & Fang, F. C. The role of ferritins in the physiology of Salmonella enterica sv. Typhimurium: a unique role for ferritin B in iron-sulphur cluster repair and virulence. Mol. Microbiol. 63, 1495–1507 (2007).

Article  CAS  PubMed  Google Scholar 

Expert, D., Boughammoura, A. & Franza, T. Siderophore-controlled iron assimilation in the enterobacterium Erwinia chrysanthemi: evidence for the involvement of bacterioferritin and the Suf iron-sulfur cluster assembly machinery. J. Biol. Chem. 283, 36564–36572 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Dean, D. R. & Brigle, K. E. Azotobacter vinelandii nifD- and nifE-encoded polypeptides share structural homology. Proc. Natl Acad. Sci. USA 82, 5720–5723 (1985).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Goodwin, P. J. et al. The Azotobacter vinelandii NifEN complex contains two identical [4Fe-4S] clusters. Biochemistry 37, 10420–10428 (1998).

Article  CAS  PubMed  Google Scholar 

Bandyopadhyay, S., Chandramouli, K. & Johnson, M. K. Iron-sulfur cluster biosynthesis. Biochem. Soc. Trans. 36, 1112–1119 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Raulfs, E. C., O'Carroll, I. P., Dos Santos, P. C., Unciuleac, M. C. & Dean, D. R. In vivo iron-sulfur cluster formation. Proc. Natl Acad. Sci. USA 105, 8591–8596 (2008). A genetic analysis supporting the existence of the scaffold.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Agar, J. N. et al. IscU as a scaffold for iron-sulfur cluster biosynthesis: sequential assembly of [2Fe-2S] and [4Fe-4S] clusters in IscU. Biochemistry 39, 7856–7862 (2000). Spectroscopy-based evidence for the occurrence of multiple forms of IscU.

Article  CAS  PubMed  Google Scholar 

Chandramouli, K. et al. Formation and properties of [4Fe-4S] clusters on the IscU scaffold protein. Biochemistry 46, 6804–6811 (2007).

Article  CAS  PubMed  Google Scholar 

Kato, S. et al. Cys-328 of IscS and Cys-63 of IscU are the sites of disulfide bridge formation in a covalently bound IscS/IscU complex: implications for the mechanism of iron-sulfur cluster assembly. Proc. Natl Acad. Sci. USA 99, 5948–5952 (2002).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Unciuleac, M. C. et al. In vitro activation of apo-aconitase using a [4Fe-4S] cluster-loaded form of the IscU [Fe-S] cluster scaffolding protein. Biochemistry 46, 6812–6821 (2007).

Article  CAS  PubMed  Google Scholar 

Shimomura, Y., Wada, K., Fukuyama, K. & Takahashi, Y. The asymmetric trimeric architecture of [2Fe-2S] IscU: implications for its scaffolding during iron-sulfur cluster biosynthesis. J. Mol. Biol. 383, 133–143 (2008).

Article  CAS  PubMed  Google Scholar 

Vickery, L. E. & Cupp-Vickery, J. R. Molecular chaperones HscA/Ssq1 and HscB/Jac1 and their roles in iron-sulfur protein maturation. Crit. Rev. Biochem. Mol. Biol. 42, 95–111 (2007). An account of the studies of co-chaperones in Fe–Scluster biogenesis by prominent contributors in the field.

Article  CAS  PubMed  Google Scholar 

Chandramouli, K. & Johnson, M. K. HscA and HscB stimulate [2Fe-2S] cluster transfer from IscU to apoferredoxin in an ATP-dependent reaction. Biochemistry 45, 11087–11095 (2006).

Article  CAS  PubMed  Google Scholar 

Bonomi, F., Iametti, S., Morleo, A., Ta, D. & Vickery, L. E. Studies on the mechanism of catalysis of iron-sulfur cluster transfer from IscU[2Fe2S] by HscA/HscB chaperones. Biochemistry 47, 12795–12801 (2008).

Article  CAS  PubMed  Google Scholar 

Petrovic, A. et al. Hydrodynamic characterization of the SufBC and SufCD complexes and their interaction with fluorescent adenosine nucleotides. Protein Sci. 17, 1264–1274 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Wada, K. et al. Molecular dynamism of Fe-S cluster biosynthesis implicated by the structure of the SufC2-SufD2 complex. J. Mol. Biol. 387, 245–258 (2009).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Chahal, H. K, Dai, Y., Saini, A., Ayala-Castro, C. & Outten, F. W. The SufBCD Fe-S scaffold complex interacts with SufA for Fe-S cluster transfer. Biochemistry 48, 10644–10653 (2009).

Article  CAS  PubMed  Google Scholar 

Eccleston, J. F., Petrovic, A., Davis, C. T., Rangachari, K. & Wilson, R. J. The kinetic mechanism of the SufC ATPase: the cleavage step is accelerated by SufB. J. Biol. Chem. 281, 8371–8378 (2006).

Article  CAS  PubMed  Google Scholar 

Vinella, D., Brochier-Armanet, C., Loiseau, L., Talla, E. & Barras, F. Iron-sulfur (Fe/S) protein biogenesis: phylogenomic and genetic studies of A-type carriers. PLoS Genet. 5, e1000497 (2009). An in vivo analysis of the specificities and redundancies of A-type proteins.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Krebs, C. et al. IscA, an alternate scaffold for Fe-S cluster biosynthesis. Biochemistry 40, 14069–14680 (2001).

Article  CAS  PubMed  Google Scholar 

Ollagnier de Choudens, S. et al. SufA from Erwinia chrysanthemi. Characterization of a scaffold protein required for iron-sulfur cluster assembly. J. Biol. Chem. 278, 17993–18001 (2003).

Article  CAS  PubMed  Google Scholar 

Loiseau, L. et al. ErpA, an iron sulfur (Fe S) protein of the A-type essential for respiratory metabolism in Escherichia coli. Proc. Natl Acad. Sci. USA 104, 13626–13631 (2007). This paper reports the first case of in vivo specificity between an A-type protein and a target apoprotein.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Gupta, V. et al. Native Escherichia coli SufA, coexpressed with SufBCDSE, purifies as a [2Fe-2S] protein and acts as an Fe-S transporter to Fe-S target enzymes. J. Am. Chem. Soc. 131, 6149–6153 (2009). A demonstration that, in vivo , IscA binds to Fe–S clusters.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Zeng, J. et al. The IscA from Acidithiobacillus ferrooxidans is an iron-sulfur protein, which assembles the [4Fe-4S] cluster with intracellular iron and sulfur. Arch. Biochem. Biophys. 463, 237–244 (2007).

Article  CAS  PubMed  Google Scholar 

Ollagnier de Choudens, S., Sanakis, Y. & Fontecave, M. SufA/IscA: reactivity studies of a class of scaffold proteins involved in [Fe-S] cluster assembly. J. Biol. Inorg. Chem. 9, 828–838 (2004).

Article  CAS  PubMed  Google Scholar 

Mettert, E. L., Outten, F. W., Wanta, B. & Kiley, P. J. The impact of O2 on the Fe-S. cluster biogenesis requirements of Escherichia coli FNR. J. Mol. Biol. 384, 798–811 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Tan, G., Lu, J., Bitoun, J. P., Huang, H. & Ding, H. IscA/SufA paralogues are required for the [4Fe-4S] cluster assembly in enzymes of multiple physiological pathways in Escherichia coli under aerobic growth conditions. Biochem. J. 420, 463–472 (2009).

Article  CAS  PubMed  Google Scholar 

Angelini, S. et al. NfuA, a new factor required for maturing Fe/S proteins in Escherichia coli under oxidative stress and iron starvation conditions. J. Biol. Chem. 283, 14084–14091 (2008).

Article  CAS  PubMed  Google Scholar 

Bandyopadhyay, S. et al. A proposed role for the Azotobacter vinelandii NfuA protein as an intermediate iron-sulfur cluster carrier. J. Biol. Chem. 283, 14092–14099 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Balasubramanian, R., Shen, G., Bryant, D. A. & Golbeck, J. H. Regulatory roles for IscA and SufA in iron homeostasis and redox stress responses in the cyanobacterium Synechococcus sp. strain PCC 7002. J. Bacteriol. 188, 3182–3191 (2006).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Jin, Z. et al. Biogenesis of iron-sulfur clusters in photosystem I: holo-NfuA from the cyanobacterium Synechococcus sp. PCC 7002 rapidly and efficiently transfers [4Fe-4S] clusters to apo-PsaC in vitro. J. Biol. Chem. 283, 28426–28435 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Agar, J. N. et al. Modular organization and identification of a mononuclear iron-binding site within the NifU protein. J. Biol. Inorg. Chem. 5, 167–177 (2000).

Article  CAS  PubMed  Google Scholar 

Boyd, J. M., Sondelski, J. L. & Downs, D. M. Bacterial ApbC protein has two biochemical activities that are required for in vivo function. J. Biol. Chem. 284, 110–118 (2009). An important contribution to the understanding of the role of one of the most conserved proteins in all living organisms.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Boyd, J. M., Pierik, A. J., Netz, D. J., Lill, R. & Downs, D. M. Bacterial ApbC can bind and effectively transfer iron-sulfur clusters. Biochemistry 47, 8195–81202 (2008).

Article  CAS  PubMed  Google Scholar 

Boyd, J. M., Lewis, J. A., Escalante-Semerena, J. C. & Downs, D. M. Salmonella enterica requires ApbC function for growth on tricarballylate: evidence of functional redundancy between ApbC and IscU. J. Bacteriol. 190, 4596–4602 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Bych, K. et al. The iron-sulphur protein Ind1 is required for effective complex I assembly. EMBO J. 27, 1736–1746 (2008). An example of the use of in vivo labelling to elucidate the position of an Fe–S cluster biogenesis factor in a pathway.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Justino, M. C., Baptista, J. M. & Saraiva, L. M. Di-iron proteins of the Ric family are involved in iron-sulfur cluster repair. Biometals 22, 99–108 (2009).

Article  CAS  PubMed  Google Scholar 

Overton, T. W. et al. Widespread distribution in pathogenic bacteria of di-iron proteins that repair oxidative and nitrosative damage to iron-sulfur centers. J. Bacteriol. 190, 2004–2013 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Harrington, J. C. et al. Resistance of Haemophilus influenzae to reactive nitrogen donors and gamma interferon-stimulated macrophages requires the formate-dependent nitrite reductase regulator-activated ytfE gene. Infect. Immun. 77, 1945–1958 (2009).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Vine, C. E., Justino, M. C., Saraiva, L. M. & Cole, J. Detection by whole genome microarrays of a spontaneous 126-gene deletion during construction of a ytfE mutant: confirmation that a ytfE mutation results in loss of repair of iron-sulfur centres in proteins damaged by oxidative or nitrosative stress. J. Microbiol. Methods. 81, 77–79 (2010)

Article  CAS  PubMed  Google Scholar 

Justino, M. C., Vicente, J. B., Teixeira, M. & Saraiva, L. M. New genes implicated in the protection of anaerobically grown Escherichia coli against nitric oxide. J. Biol. Chem. 280, 2636–2643 (2005).

Article  CAS  PubMed  Google Scholar 

Justino, M. C., Almeida, C. C., Gonçalves, V. L., Teixeira, M. & Saraiva, L. M. Escherichia coli YtfE is a di-iron protein with an important function in assembly of iron-sulphur clusters. FEMS Microbiol. Lett. 257, 278–284 (2006).

Article  CAS  PubMed  Google Scholar 

Todorovic, S. et al. Iron-sulfur repair YtfE protein from Escherichia coli: structural characterization of the di-iron center. J. Biol. Inorg. Chem. 13, 765–770 (2008).

Article  CAS  PubMed  Google Scholar 

Gralnick, J. & Downs, D. Protection from superoxide damage associated with an increased level of the YggX protein in Salmonella enterica. Proc. Natl Acad. Sci. USA 98, 8030–8035 (2001).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Tucker, N. P. et al. The transcriptional repressor protein NsrR senses nitric oxide directly via a [2Fe-2S] cluster. PLoS ONE 3, e3623 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Schwartz, C. J. et al. IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins. Proc. Natl Acad. Sci. USA 98, 14895–14900 (2001). The proposal that an autoregulatory system allows bacterial cells to sense Fe–S cluster homeostasis.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Giel, J. L., Rodionov, D., Liu, M., Blattner, F. R. & Kiley, P. J. IscR-dependent gene expression links iron-sulphur cluster assembly to the control of O2-regulated genes in Escherichia coli. Mol. Microbiol. 60, 1058–1075 (2006). This paper shows that IscR regulates a broad range of genes.

Article  CAS  PubMed  Google Scholar 

Wu, Y. & Outten, F. W. IscR controls iron-dependent biofilm formation in Escherichia coli by regulating type I fimbria expression. J. Bacteriol. 191, 1248–1257 (2009).

Article  CAS  PubMed  Google Scholar 

Nesbit, A. D., Giel, J. L., Rose, J. C. & Kiley, P. J. Sequence-specific binding to a subset of IscR-regulated promoters does not require IscR Fe-S cluster ligation. J. Mol. Biol. 387, 28–41 (2009).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Shen, G. et al. SufR coordinates two [4Fe-4S]2+, 1+ clusters and functions as a transcriptional repressor of the sufBCDS operon and an autoregulator of sufR in cyanobacteria. J. Biol. Chem. 282, 31909–31919 (2007). Adescription of the Fe–S cluster biogenesis strategy in cyanobacteria.

Article  CAS  PubMed  Google Scholar 

Butland, G. et al. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433, 531–537 (2005).

Article  CAS  PubMed  Google Scholar 

Arifuzzaman, M. et al. Large-scale identification of protein-protein interaction of Escherichia coli K-12. Genome Res. 16, 686–691 (2006).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Butland, G. et al. eSGA: E. coli synthetic genetic array analysis. Nature Methods 5, 789–795 (2008).

Article  CAS  PubMed  Google Scholar 

Bandyopadhyay, S. et al. Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe-2S] clusters. EMBO J. 27, 1122–1133 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Mandrand-Berthelot, M. A., Couchoux-Luthaud, G., Santini, C. L. & Giordano, G. Mutants of Escherichia coli specifically deficient in respiratory formate dehydrogenase activity. J. Gen. Microbiol. 134, 3129–3139 (1988).

CAS  PubMed  Google Scholar 

Ote, T. et al. Involvement of the Escherichia coli folate-binding protein YgfZ in RNA modification and regulation of chromosomal replication initiation. Mol. Microbiol. 59, 265–275 (2006).

Article  CAS  PubMed  Google Scholar 

Seaton, B. L. & Vickery, L. E. A gene encoding a DnaK/hsp70 homolog in Escherichia coli. Proc. Natl Acad. Sci. USA 91, 2066–2070 (1994).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Lelivelt, M. J. & Kawula, T. H. Hsc66, an Hsp70 homolog in Escherichia coli, is induced by cold shock but not by heat shock. J. Bacteriol. 177, 4900–4907 (1995).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Desnoyers, G., Morissette, A., Prévost, K. & Massé, E. Small RNA-induced differential degradation of the polycistronic mRNA iscRSUA. EMBO J. 28, 1551–1561 (2009). The first example of a role for small-RNA-mediated regulation in Fe–S cluster homeostasis.

Article  CAS  PubMed  PubMed Central  Google Scholar