Global identification of genes affecting Iron-sulfur cluster biogenesis and iron homeostasis

Journal of Bacteriology

Volumn 196, Issue 6, 2014, Pages 1238-1249

  Hidese, Ryota ^a   Mihara, Hisaaki ^b   Kurihara, Tatsuo ^a   Esaki, Nobuyoshi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b RITSUMEIKAN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE KNOCKOUT TECHNIQUES; HOMEOSTASIS; IRON; ISOTOPE LABELING; METABOLIC NETWORKS AND PATHWAYS; SULFUR; URACIL;

EID: 84894338514     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01160-13     Document Type: Article

References (105)

1. Py B, Barras F. 2010. Building Fe-S proteins: bacterial strategies. Nat. Rev. Microbiol. 8:436-446. http://dx.doi.org/10.1038/nrmicro2356.
2. Johnson DC, Dean DR, Smith AD, Johnson MK. 2005. Structure, function, and formation of biological iron-sulfur clusters. Annu. Rev. Biochem. 74:247-281. http://dx.doi.org/10.1146/annurev.biochem.74.082803.133518.
3. Beinert H. 2000. Iron-sulfur proteins: ancient structures, still full of surprises. J. Biol. Inorg. Chem. 5:2-15. http://dx.doi.org/10.1007/s007750050002.
4. Drennan CL, Peters JW. 2003. Surprising cofactors in metalloenzymes. Curr. Opin. Struct. Biol. 13:220-226. http://dx.doi.org/10.1016/S0959-440X(03)00038-1.
5. Schwartz CJ, Djaman O, Imlay JA, Kiley PJ. 2000. The cysteine desulfurase, IscS, has a major role in in vivo Fe-S cluster formation in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 97:9009-9014. http://dx.doi.org/10.1073/pnas.160261497.
6. Tokumoto U, Takahashi Y. 2001. Genetic analysis of the isc operon in Escherichia coli involved in the biogenesis of cellular iron-sulfur proteins. J. Biochem. 130:63-71. http://dx.doi.org/10.1093/oxfordjournals.jbchem.a002963.
7. Hidese R, Mihara H, Esaki N. 2011. Bacterial cysteine desulfurases: versatile key players in biosynthetic pathways of sulfur-containing bio-factors. Appl. Microbiol. Biotechnol. 91:47-61. http://dx.doi.org/10.1007/s00253-011-3336-x.
8. Lee JH, Yeo WS, Roe JH. 2004. 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. http://dx.doi.org/10.1111/j.1365-2958.2003.03946.x.
9. Yeo WS, Lee JH, Lee KC, Roe JH. 2006. IscR acts as an activator in response to oxidative stress for the suf operon encoding Fe-S assembly proteins. Mol. Microbiol. 61:206-218. http://dx.doi.org/10.1111/j.1365-2958.2006.05220.x.
10. Jang S, Imlay JA. 2010. Hydrogen peroxide inactivates the Escherichia coli Isc iron-sulphur assembly system, and OxyR induces the Suf system to compensate. Mol. Microbiol. 78:1448-1467. http://dx.doi.org/10.1111/j.1365-2958.2010.07418.x.
11. Adinolfi S, Iannuzzi C, Prischi F, Pastore C, Iametti S, Martin SR, Bonomi F, Pastore A. 2009. Bacterial frataxin CyaY is the gatekeeper of iron-sulfur cluster formation catalyzed by IscS. Nat. Struct. Mol. Biol. 16:390-396. http://dx.doi.org/10.1038/nsmb.1579.
12. Iannuzzi C, Adinolfi S, Howes BD, Garcia-Serres R, Clémancey M, Latour JM, Smulevich G, Pastore A. 2011. The role of CyaY in iron sulfur cluster assembly on the E. coli IscU scaffold protein. PLoS One 6:e21992. http://dx.doi.org/10.1371/journal.pone.0021992.
13. Velayudhan J, Castor M, Richardson A, Main-Hester KL, Fang FC. 2007. 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. http://dx.doi.org/10.1111/j.1365-2958.2007.05600.x.
14. Py B, Gerez C, Angelini S, Planel R, Vinella D, Loiseau L, Talla E, Brochier-Armanet C, Garcia Serres R, Latour JM, Ollagnier-de Choudens S, Fontecave M, Barras F. 2012. Molecular organization, biochemical function, cellular role and evolution of NfuA, an atypical Fe-S carrier. Mol. Microbiol. 86:155-171. http://dx.doi.org/10.1111/j.1365-2958.2012.08181.x.
15. Angelini S, Gerez C, Ollagnier-de Choudens S, Sanakis Y, Fontecave M, Barras F, Py B. 2008. 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. http://dx.doi.org/10.1074/jbc.M709405200.
16. Yeung N, Gold B, Liu NL, Prathapam R, Sterling HJ, Willams ER, Butland G. 2011. The E. coli monothiol glutaredoxin GrxD forms homodimeric and heterodimeric FeS cluster containing complexes. Biochemistry 50:8957-8969. http://dx.doi.org/10.1021/bi2008883.
17. Boyd JM, Sondelski JL, Downs DM. 2009. Bacterial ApbC protein has two biochemical activities that are required for in vivo function. J. Biol. Chem. 284:110-118. http://dx.doi.org/10.1074/jbc.M807003200.
18. Loiseau L, Gerez C, Bekker M, Ollagnier-de Choudens S, Py B, Sanakis Y, Teixeira de Mattos J, Fontecave M, Barras F. 2007. ErpA, an iron sulfur (Fe-S) protein of the A-type essential for respiratory metabolism in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 104:13626-13631. http://dx.doi.org/10.1073/pnas.0705829104.
19. Vinella D, Loiseau L, de Choudens SO, Fontecave M, Barras F. 2013. In vivo [Fe-S] cluster acquisition by IscR and NsrR, two stress regulators in Escherichia coli. Mol. Microbiol. 87:493-508. http://dx.doi.org/10.1111/mmi.12135.
20. Justino MC, Almeida CC, Teixeira M, Saraiva LM. 2007. Escherichia coli di-iron YtfE protein is necessary for the repair of stress-damaged iron-sulfur clusters. J. Biol. Chem. 282:10352-10359. http://dx.doi.org/10.1074/jbc.M610656200.
21. Mihara H, Hidese R, Yamane M, Kurihara T, Esaki N. 2008. The iscS gene deficiency affects the expression of pyrimidine metabolism genes. Biochem. Biophys. Res. Commun. 372:407-411. http://dx.doi.org/10.1016/j.bbrc.2008.05.019.
22. Hidese R, Mihara H, Kurihara T, Esaki N. 2011. Escherichia coli dihydropyrimidine dehydrogenase is a novel NAD-dependent heterotetramer essential for the production of 5,6-dihydrouracil. J. Bacteriol. 193:989-993. http://dx.doi.org/10.1128/JB.01178-10.
23. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008. http://dx.doi.org/10.1038/msb4100050.
24. Bergstrom DE, Leonard NJ. 1972. Structure of the borohydride reduction product of photolinked 4-thiouracil and cytosine. Fluorescent probe of transfer ribonucleic acid tertiary structure. J. Am. Chem. Soc. 94: 6178-6182.
25. Fraenkel DG, Horecker BL. 1964. Pathways of D-glucose metabolism in Salmonella typhimurium. A study of a mutant lacking phosphoglucose isomerase. J. Biol. Chem. 239:2765-2771.
26. Miller RE, Stadtman ER. 1972. Glutamate synthase from Escherichia coli. An iron-sulfide flavoprotein. J. Biol. Chem. 247:7407-7419.
27. Cribbs R, Englesberg E. 1964. L-Arabinose negative mutants of the L-ribulokinase structural gene affecting the levels of L-arabinose isomerase in Escherichia coli. Genetics 49:95-108.
28. Banerjee S, Fraenkel DG. 1972. Glucose-6-phosphate dehydrogenase from Escherichia coli and from a "high-level" mutant. J. Bacteriol. 110: 155-160.
29. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254. http://dx.doi.org/10.1016/0003-2697(76)90527-3.
30. Kato S, Mihara H, Kurihara T, Takahashi Y, Tokumoto U, Yoshimura T, Esaki N. 2002. 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. U. S. A. 99:5948-5952. http://dx.doi.org/10.1073/pnas.082123599.
31. Djaman O, Outten FW, Imlay JA. 2004. Repair of oxidized iron-sulfur clusters in Escherichia coli. J. Biol. Chem. 279:44590-44599. http://dx.doi.org/10.1074/jbc.M406487200.
32. Zhang W, Urban A, Mihara H, Leimkühler S, Kurihara T, Esaki N. 2010. IscS functions as a primary sulfur-donating enzyme by interacting specifically with MoeB and MoaD in the biosynthesis of molybdopterin in Escherichia coli. J. Biol. Chem. 285:2302-2308. http://dx.doi.org/10.1074/jbc.M109.082172.
33. Iobbi-Nivol C, Leimkühler S. 2013. Molybdenum enzymes, their maturation and molybdenum cofactor biosynthesis in Escherichia coli. Biochim. Biophys. Acta 1827:1086-1101. http://dx.doi.org/10.1016/j.bbabio.2012.11.007.
34. Yoshizawa S, Böck A. 2009. The many levels of control on bacterial selenoprotein synthesis. Biochim. Biophys. Acta 1790:1404-1414. http://dx.doi.org/10.1016/j.bbagen.2009.03.010.
35. Thomé R, Gust A, Toci R, Mendel R, Bittner F, Magalon A, Walburger A. 2012. A sulfur transferase is essential for activity of formate dehydrogenases in Escherichia coli. J. Biol. Chem. 287:4671-4678. http://dx.doi.org/10.1074/jbc.M111.327122.
36. Chan Chung KC, Zamble DB. 2011. Protein interactions and localization of the Escherichia coli accessory protein HypA during nickel insertion to [NiFe] hydrogenase. J. Biol. Chem. 286:43081-43090. http://dx.doi.org/10.1074/jbc.M111.290726.
37. Malpica R, Sandoval GR, Rodríguez C, Franco B, Georgellis D. 2006. Signaling by the arc two-component system provides a link between the redox state of the quinone pool and gene expression. Antioxid. Redox Signal. 8:781-795. http://dx.doi.org/10.1089/ars.2006.8.781.
38. Vogt SL, Raivio TL. 2012. Just scratching the surface: an expanding view of the Cpx envelope stress response. FEMS Microbiol. Lett. 326:2-11. http://dx.doi.org/10.1111/j.1574-6968.2011.02406.x.
39. Kato J, Katayama T. 2001. Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli.EMBOJ. 20:4253-4262. http://dx.doi.org/10.1093/emboj/20.15.4253.
40. Witte G, Urbanke C, Curth U. 2003. DNA polymerase III chi subunit ties single-stranded DNA binding protein to the bacterial replication machinery. Nucleic Acids Res. 31:4434-4440. http://dx.doi.org/10.1093/nar/gkg498.
41. Berg BL, Li J, Heider J, Stewart V. 1991. Nitrate-inducible formate dehydrogenase in Escherichia coli K-12. I. Nucleotide sequence of the fdnGHI operon and evidence that opal (UGA) encodes selenocysteine. J. Biol. Chem. 266:22380-22385.
42. Abaibou H, Pommier J, Benoit S, Giordano G, Mandrand-Berthelot MA. 1995. Expression and characterization of the Escherichia coli fdo locus and a possible physiological role for aerobic formate dehydrogenase. J. Bacteriol. 177:7141-7149.
43. Boyington JC, Gladyshev VN, Khangulov SV, Stadtman TC, Sun PD. 1997. Crystal structure of formate dehydrogenase H: catalysis involving Mo, molybdopterin, selenocysteine, and an Fe4S4 cluster. Science 275: 1305-1308. http://dx.doi.org/10.1126/science.275.5304.1305.
44. Mihara H, Kurihara T, Yoshimura T, Esaki N. 2000. 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. http://dx.doi.org/10.1093/oxfordjournals.jbchem.a022641.
45. Flint DH. 1996. 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.
46. Urbina HD, Silberg JJ, Hoff KG, Vickery LE. 2001. Transfer of sulfur from IscS to IscU during Fe/S cluster assembly. J. Biol. Chem. 276: 44521-44526. http://dx.doi.org/10.1074/jbc.M106907200.
47. Smith AD, Agar JN, Johnson KA, Frazzon J, Amster IJ, Dean DR, Johnson MK. 2001. Sulfur transfer from IscS to IscU: the first step in iron-sulfur cluster biosynthesis. J. Am. Chem. Soc. 123:11103-11104. http://dx.doi.org/10.1021/ja016757n.
48. Chandramouli K, Unciuleac MC, Naik S, Dean DR, Huynh BH, Johnson MK. 2007. Formation and properties of [4Fe-4S] clusters on the IscU scaffold protein. Biochemistry 46:6804-6811. http://dx.doi.org/10.1021/bi6026659.
49. Unciuleac MC, Chandramouli K, Naik S, Mayer S, Huynh BH, Johnson MK, Dean DR. 2007. 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. http://dx.doi.org/10.1021/bi6026665.
50. Chandramouli K, Johnson MK. 2006. HscA and HscB stimulate [2Fe-2S] cluster transfer from IscU to apoferredoxin in an ATP-dependent reaction. Biochemistry 45:11087-11095. http://dx.doi.org/10.1021/bi061237w.
51. Bonomi F, Iametti S, Morleo A, Ta D, Vickery LE. 2008. Studies on the mechanism of catalysis of iron-sulfur cluster transfer from IscU[2Fe2S] by HscA/HscB chaperones. Biochemistry 47:12795-12801. http://dx.doi.org/10.1021/bi801565j.
52. Kim JH, Tonelli M, Frederick RO, Chow DC, Markley JL. 2012. Specialized Hsp70 chaperone (HscA) binds preferentially to the disordered form, whereas J-protein (HscB) binds preferentially to the structured form of the iron-sulfur cluster scaffold protein (IscU). J. Biol. Chem. 287:31406-31413. http://dx.doi.org/10.1074/jbc.M112.352617.
53. Dai Z, Tonelli M, Markley JL. 2012. Metamorphic protein IscU changes conformation by cis-trans isomerizations of two peptidyl-prolyl peptide bonds. Biochemistry 51:9595-9602. http://dx.doi.org/10.1021/bi301413y.
54. Kim JH, Füzéry AK, Tonelli M, Ta DT, Westler WM, Vickery LE, Markley JL. 2009. Structure and dynamics of the iron-sulfur cluster assembly scaffold protein IscU and its interaction with the cochaperone HscB. Biochemistry 48:6062-6071. http://dx.doi.org/10.1021/bi9002277.
55. Kim JH, Tonelli M, Markley JL. 2012. Disordered form of the scaffold protein IscU is the substrate for iron-sulfur cluster assembly on cysteine desulfurase. Proc. Natl. Acad. Sci. U. S. A. 109:454-459. http://dx.doi.org/10.1073/pnas.1114372109.
56. Bonomi F, Iametti S, Morleo A, Ta D, Vickery LE. 2011. Facilitated transfer of IscU-[2Fe2S] clusters by chaperone-mediated ligand exchange. Biochemistry 50:9641-9650. http://dx.doi.org/10.1021/bi201123z.
57. Johnson DC, Unciuleac MC, Dean DR. 2006. Controlled expression and functional analysis of iron-sulfur cluster biosynthetic components within Azotobacter vinelandii. J. Bacteriol. 188:7551-7561. http://dx.doi.org/10.1128/JB.00596-06.
58. Marinoni EN, de Oliveira JS, Nicolet Y, Raulfs EC, Amara P, Dean DR, Fontecilla-Camps JC. 2012. (IscS-IscU)2 complex structures provide insights into Fe2S2 biogenesis and transfer. Angew. Chem. Int. Ed. Engl. 51:5439-5442. http://dx.doi.org/10.1002/anie.201201708.
59. Raulfs EC, O'Carroll IP, Dos Santos PC, Unciuleac MC, Dean DR. 2008. In vivo iron-sulfur cluster formation. Proc. Natl. Acad. Sci. U. S. A. 105:8591-8596. http://dx.doi.org/10.1073/pnas.0803173105.
60. Pinske C, Sawers RG. 2012. A-type carrier protein ErpA is essential for formation of an active formate-nitrate respiratory pathway in Escherichia coli K-12. J. Bacteriol. 194:346-353. http://dx.doi.org/10.1128/JB.06024-11.
61. Giel JL, Rodionov D, Liu M, Blattner FR, Kiley PJ. 2006. IscRdependent gene expression links iron-sulphur cluster assembly to the control of O2-regulated genes in Escherichia coli. Mol. Microbiol. 60: 1058-1075. http://dx.doi.org/10.1111/j.1365-2958.2006.05160.x.
62. Giel JL, Nesbit AD, Mettert EL, Fleischhacker AS, Wanta BT, Kiley PJ. 2013. Regulation of iron-sulphur cluster homeostasis through transcriptional control of the Isc pathway by [2Fe-2S]-IscR in Escherichia coli. Mol. Microbiol. 87:478-492. http://dx.doi.org/10.1111/mmi.12052.
63. Lee JW, Helmann JD. 2007. Functional specialization within the Fur family of metalloregulators. Biometals 20:485-499. http://dx.doi.org/10.1007/s10534-006-9070-7.
64. Chen Z, Lewis KA, Shultzaberger RK, Lyakhov IG, Zheng M, Doan B, Storz G, Schneider TD. 2007. Discovery of Fur binding site clusters in Escherichia coli by information theory models. Nucleic Acids Res. 35: 6762-6777. http://dx.doi.org/10.1093/nar/gkm631.
65. Massé E, Gottesman S. 2002. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 99:4620-4625. http://dx.doi.org/10.1073/pnas.032066599.
66. Jacques JF, Jang S, Prévost K, Desnoyers G, Desmarais M, Imlay J, Massé E. 2006. RyhB small RNA modulates the free intracellular iron pool and is essential for normal growth during iron limitation in Escherichia coli. Mol. Microbiol. 62:1181-1190. http://dx.doi.org/10.1111/j.1365-2958.2006.05439.x.
67. Desnoyers G, Morissette A, Prévost K, Massé E. 2009. Small RNAinduced differential degradation of the polycistronic mRNA iscRSUA. EMBO J. 28:1551-1561. http://dx.doi.org/10.1038/emboj.2009.116.
68. Geissmann TA, Touati D. 2004. Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator. EMBO J. 23:396-405. http://dx.doi.org/10.1038/sj.emboj.7600058.
69. Večerek B, Moll I, Afonyushkin T, Kaberdin V, Blasi U. 2003. Interaction of the RNA chaperone Hfq with mRNAs: direct and indirect roles of Hfq in iron metabolism of Escherichia coli. Mol. Microbiol. 50:897-909. http://dx.doi.org/10.1046/j.1365-2958.2003.03727.x.
70. Kammler M, Schön C, Hantke K. 1993. Characterization of the ferrous iron uptake system of Escherichia coli. J. Bacteriol. 175:6212-6219.
71. Liu X, De Wulf P. 2004. Probing the ArcA-P modulon of Escherichia coli by whole genome transcriptional analysis and sequence recognition profiling. J. Biol. Chem. 279:12588-12597. http://dx.doi.org/10.1074/jbc.M313454200.
72. Price NL, Raivio TL. 2009. Characterization of the Cpx regulon in Escherichia coli strain MC4100. J. Bacteriol. 191:1798-1815. http://dx.doi.org/10.1128/JB.00798-08.
73. Zhao G, Winkler ME. 1995. Kinetic limitation and cellular amount of pyridoxine (pyridoxamine) 5'-phosphate oxidase of Escherichia coli K-12. J. Bacteriol. 177:883-891.
74. Safo MK, Musayev FN, di Salvo ML, Schirch V. 2001. X-ray structure of Escherichia coli pyridoxine 5'-phosphate oxidase complexed with pyridoxal 5'-phosphate at 2.0 Å resolution. J. Mol. Biol. 310:817-826. http://dx.doi.org/10.1006/jmbi.2001.4734.
75. Nakamoto RK, Baylis Scanlon JA, Al-Shawi MK. 2008. The rotary mechanism of the ATP synthase. Arch. Biochem. Biophys. 476:43-50. http://dx.doi.org/10.1016/j.abb.2008.05.004.
76. Pittman MS, Robinson HC, Poole RK. 2005. A bacterial glutathione transporter (Escherichia coli CydDC) exports reductant to the periplasm. J. Biol. Chem. 280:32254-32261. http://dx.doi.org/10.1074/jbc.M503075200.
77. Pittman MS, Corker H, Wu G, Binet MB, Moir AJ, Poole RK. 2002. Cysteine is exported from the Escherichia coli cytoplasm by CydDC, an ATP-binding cassette-type transporter required for cytochrome assembly. J. Biol. Chem. 277:49841-49849. http://dx.doi.org/10.1074/jbc.M205615200.
78. Andrews SC, Robinson AK, Rodríguez-Quinones F. 2003. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27:215-237. http://dx.doi.org/10.1016/S0168-6445(03)00055-X.
79. Braun V, Braun M. 2002. Iron transport and signaling in Escherichia coli. FEBS Lett. 529:78-85. http://dx.doi.org/10.1016/S0014-5793(02)03185-X.
80. Buchanan SK, Smith BS, Venkatramani L, Xia D, Esser L, Palnitkar M, Chakraborty R, van der Helm D, Deisenhofer J. 1999. Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nat. Struct. Biol. 6:56-63. http://dx.doi.org/10.1038/4931.
81. Locher KP, Rees B, Koebnik R, Mitschler A, Moulinier L, Rosenbusch JP, Moras D. 1998. Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95:771-778. http://dx.doi.org/10.1016/S0092-8674(00)81700-6.
82. Sauer M, Hantke K, Braun V. 1987. Ferric-coprogen receptor FhuE of Escherichia coli: processing and sequence common to all TonBdependent outer membrane receptor proteins. J. Bacteriol. 169:2044-2049.
83. Ferguson AD, Chakraborty R, Smith BS, Esser L, van der Helm D, Deisenhofer J. 2002. Structural basis of gating by the outer membrane transporter FecA. Science 295:1715-1719. http://dx.doi.org/10.1126/science.1067313.
84. 2+ transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157:H7. Mol. Microbiol. 65:857-875. http://dx.doi.org/10.1111/j.1365-2958.2007.05802.x.
85. Schröder I, Johnson E, de Vries S. 2003. Microbial ferric iron reductases. FEMS Microbiol. Rev. 27:427-447. http://dx.doi.org/10.1016/S0168-6445(03)00043-3.
86. + reductase and oxygen-insensitive nitroreductase are capable of functioning as ferric reductase and of driving the Fenton reaction. Biometals 23:727-737. http://dx.doi.org/10.1007/s10534-010-9339-8.
87. Ingelman M, Ramaswamy S, Niviere V, Fontecave M, Eklund H. 1999. Crystal structure of NAD(P)H:flavin oxidoreductase from Escherichia coli. Biochemistry 38:7040-7049. http://dx.doi.org/10.1021/bi982849m.
88. Miethke M, Hou J, Marahiel MA. 2011. The siderophore-interacting protein YqjH acts as a ferric reductase in different iron assimilation pathways of Escherichia coli. Biochemistry 50:10951-10964. http://dx.doi.org/10.1021/bi201517h.
89. Cartron ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC. 2006. Feo-transport of ferrous iron into bacteria. Biometals 19:143-157. http://dx.doi.org/10.1007/s10534-006-0003-2.
90. Fahey RC, Brown WC, Adams WB, Worsham MB. 1978. Occurrence of glutathione in bacteria. J. Bacteriol. 133:1126-1129.
91. Hider RC, Kong XL. 2011. Glutathione: a key component of the cytoplasmic labile iron pool. Biometals 24:1179-1187. http://dx.doi.org/10.1007/s10534-011-9476-8.
92. Maringanti S, Imlay JA. 1999. An intracellular iron chelator pleiotropically suppresses enzymatic and growth defects of superoxide dismutasedeficient Escherichia coli. J. Bacteriol. 181:3792-3802.
93. Richaud C, Higgins W, Mengin-Lecreulx D, Stragier P. 1987. Molecular cloning, characterization, and chromosomal localization of dapF, the Escherichia coli gene for diaminopimelate epimerase. J. Bacteriol. 169:1454-1459.
94. Faloona GR, Srere PA. 1969. Escherichia coli citrate synthase. Purification and the effect of potassium on some properties. Biochemistry 8:4497-4503.
95. McHugh JP, Rodríguez-Quiñones F, Abdul-Tehrani H, Svistunenko DA, Poole RK, Cooper CE, Andrews SC. 2003. Global iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis. J. Biol. Chem. 278:29478-29486. http://dx.doi.org/10.1074/jbc.M303381200.
96. Gulmezian M, Hyman KR, Marbois BN, Clarke CF, Javor GT. 2007. The role of UbiX in Escherichia coli coenzyme Q. biosynthesis. Arch. Biochem. Biophys. 467:144-153. http://dx.doi.org/10.1016/j.abb.2007.08.009.
97. Bader M, Muse W, Ballou DP, Gassner C, Bardwell JC. 1999. Oxidative protein folding is driven by the electron transport system. Cell 98:217-227. http://dx.doi.org/10.1016/S0092-8674(00)81016-8.
98. Missiakas D, Raina S. 1997. Protein folding in the bacterial periplasm. J. Bacteriol. 179:2465-2471.
99. Zeng H, Snavely I, Zamorano P, Javor GT. 1998. Low ubiquinone content in Escherichia coli causes thiol hypersensitivity. J. Bacteriol. 180: 3681-3685.
100. Collis CM, Grigg GW. 1989. An Escherichia coli mutant resistant to phleomycin, bleomycin, and heat inactivation is defective in ubiquinone synthesis. J. Bacteriol. 171:4792-4798.
101. - mutants of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 102:9317-9322. http://dx.doi.org/10.1073/pnas.0502051102.
102. McCool JD, Ford CC, Sandler SJ. 2004. A dnaT mutant with phenotypes similar to those of a priA2::kan mutant in Escherichia coli K-12. Genetics 167:569-578. http://dx.doi.org/10.1534/genetics.103.025296.
103. Guo Q, Goto S, Chen Y, Feng B, Xu Y, Muto A, Himeno H, Deng H, Lei J, Gao N. 2013. Dissecting the in vivo assembly of the 30S ribosomal subunit reveals the role of RimM and general features of the assembly process. Nucleic Acids Res. 41:2609-2620. http://dx.doi.org/10.1093/nar/gks1256.
104. Newby Z, Lee TT, Morse RJ, Liu Y, Liu L, Venkatraman P, Santi DV, Finer-Moore JS, Stroud RM. 2006. The role of protein dynamics in thymidylate synthase catalysis: variants of conserved 2'-deoxyuridine 5'-monophosphate (dUMP)-binding Tyr-261. Biochemistry 45:7415-7428. http://dx.doi.org/10.1021/bi060152s.
105. 2(CO) moiety of [NiFe] hydrogenase. J. Biol. Chem. 287:38845-38853. http://dx.doi.org/10.1074/jbc.M112.376947.