Structure and Mechanism of the Siderophore-Interacting Protein from the Fuscachelin Gene Cluster of Thermobifida fusca

Biochemistry

Volumn 54, Issue 25, 2015, Pages 3989-4000

  Li, Kunhua ^a   Chen, Wei Hung ^a   Bruner, Steven D ^a  

^a University of Florida   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; ENZYME ACTIVITY; GENES; IRON; MOBILE SECURITY; PROTEINS; REDOX REACTIONS; REDUCING AGENTS; REDUCTION;

BIOSYNTHETIC GENE CLUSTER; CHEMICAL EQUATIONS; COMPLEX PROCESSES; IRON ACQUISITION; SINGLE ELECTRON REDUCTION; SPECIFIC BINDING; THERAPEUTIC TREATMENTS; THERMOBIFIDA FUSCA;

IRON COMPOUNDS;

BACTERIAL PROTEIN; CYTOCHROME B5 REDUCTASE; FERRIC ION; FERROUS ION; FLAVINE ADENINE NUCLEOTIDE; SIDEROPHORE; SIDEROPHORE INTERACTING PROTEIN; UNCLASSIFIED DRUG; PROTEIN BINDING;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BINDING AFFINITY; BINDING SITE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; FUSCACHELIN GENE; GENE CLUSTER; ISOTHERMAL TITRATION CALORIMETRY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METAL BINDING; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; STRUCTURAL HOMOLOGY; THERMOBIFIDA FUSCA; X RAY CRYSTALLOGRAPHY; ACTINOBACTERIA; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; SEQUENCE ALIGNMENT;

THERMOBIFIDA FUSCA;

ACTINOBACTERIA; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PROTEIN BINDING; SEQUENCE ALIGNMENT; SIDEROPHORES;

EID: 84933510945     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00354     Document Type: Article

References (80)

1. Sigel, A. and Sigel, H. (1998) Iron Transport and Storage in Microorganisms, Plants, and Animals, Vol. 35, Marcel Dekker, Inc., New York.
2. Sutak, R., Lesuisse, E., Tachezy, J., and Richardson, D. R. (2008) Crusade for iron: Iron uptake in unicellular eukaryotes and its significance for virulence Trends Microbiol. 16, 261-268
3. Kobayashi, T. and Nishizawa, N. K. (2012) Iron uptake, translocation, and regulation in higher plants Annu. Rev. Plant Biol. 63, 131-152
4. Weinberg, E. D. (2009) Iron availability and infection Biochim. Biophys. Acta 1790, 600-605
5. Miethke, M. and Marahiel, M. A. (2007) Siderophore-based iron acquisition and pathogen control Microbiol. Mol. Biol. Rev. 71, 413-451
6. Goetz, D. H., Holmes, M. A., Borregaard, N., Bluhm, M. E., Raymond, K. N., and Strong, R. K. (2002) The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition Mol. Cell 10, 1033-1043
7. Sandy, M. and Butler, A. (2009) Microbial iron acquisition: Marine and terrestrial siderophores Chem. Rev. 109, 4580-4595
8. Deneer, H. G., Healey, V., and Boychuk, I. (1995) Reduction of exogenous ferric iron by a surface-associated ferric reductase of Listeria spp Microbiology 141, 1985-1992
9. Tong, Y. and Guo, M. (2009) Bacterial heme-transport proteins and their heme-coordination modes Arch. Biochem. Biophys. 481, 1-15
10. Braun, V. (2001) Iron uptake mechanisms and their regulation in pathogenic bacteria Int. J. Med. Microbiol. 291, 67-79
11. Raymond, K. N., Dertz, E. A., and Kim, S. S. (2003) Enterobactin: An archetype for microbial iron transport Proc. Natl. Acad. Sci. U.S.A. 100, 3584-3588
12. Gründlinger, M., Yasmin, S., Lechner, B. E., Geley, S., Schrettl, M., Hynes, M., and Haas, H. (2013) Fungal siderophore biosynthesis is partially localized in peroxisomes Mol. Microbiol. 88, 862-875
13. Furrer, J. L., Sanders, D. N., Hook-Barnard, I. G., and McIntosh, M. A. (2002) Export of the siderophore enterobactin in Escherichia coli: Involvement of a 43 kDa membrane exporter Mol. Microbiol. 44, 1225-1234
14. Gehring, A. M., Bradley, K. A., and Walsh, C. T. (1997) Enterobactin biosynthesis in Escherichia coli: Isochorismate lyase (EntB) is a bifunctional enzyme that is phosphopantetheinylated by EntD and then acylated by EntE using ATP and 2,3-dihydroxybenzoate Biochemistry 36, 8495-8503
15. Seyedsayamdost, M. R., Traxler, M. F., Zheng, S., Kolter, R., and Clardy, J. (2011) Structure and biosynthesis of amychelin, an unusual mixed-ligand siderophore from Amycolatopsis sp. AA4 J. Am. Chem. Soc. 133, 11434-11437
16. de Lorenzo, V. and Bindereif, A. (1986) Aerobactin biosynthesis and transport genes of plasmid ColV-K30 in Escherichia coli K-12 J. Bacteriol. 165, 601-611
17. Hider, R. C. and Kong, X. (2010) Chemistry and biology of siderophores Nat. Prod. Rep. 27, 637-657
18. Biegel Carson, S. D. B., Klebba, P. E., Newton, S. M. C., and Sparling, P. F. (1999) Ferric enterobactin binding and utilization by Neisseria gonorrhoeae J. Bacteriol. 181, 2895-2901
19. Wallner, A., Blatzer, M., Schrettl, M., Sarg, B., Lindner, H., and Haas, H. (2009) Ferricrocin, a siderophore involved in intra- and transcellular iron distribution in Aspergillus fumigatus Appl. Environ. Microbiol. 75, 4194-4196
20. Johnstone, T. and Nolan, E. (2015) Beyond Iron: Non-classical functions of bacterial siderophores Dalton Trans. 6320-6339
21. Bao, G., Clifton, M., Hoette, T. M., Mori, K., Deng, S.-X., Qiu, A., Viltard, M., Williams, D., Paragas, N., Leete, T., Kulkarni, R., Li, X., Lee, B., Kalandadze, A., Ratner, A. J., Pizarro, J. C., Schmidt-Ott, K. M., Landry, D. W., Raymond, K. N., Strong, R. K., and Barasch, J. (2010) Iron traffics in circulation bound to a siderocalin (Ngal)-catechol complex Nat. Chem. Biol. 6, 602-609
22. Bobrov, A. G., Kirillina, O., Fetherston, J. D., Miller, M. C., Burlison, J. A., and Perry, R. D. (2014) The Yersinia pestis siderophore, yersiniabactin, and the ZnuABC system both contribute to zinc acquisition and the development of lethal septicaemic plague in mice Mol. Microbiol. 93, 759-775
23. Jurchen, K. M. C. and Raymond, K. N. (2006) A bidentate terephthalamide ligand, TAMmeg, as an entry into terephthalamide-containing therapeutic iron chelating agents Inorg. Chem. 45, 2438-2447
24. Abergel, R. J. and Raymond, K. N. (2011) Multidentate terephthalamidate and hydroxypyridonate ligands: Towards new orally active chelators Hemoglobin 35, 276-290
25. Ji, C., Miller, P. A., and Miller, M. J. (2012) Iron transport-mediated drug delivery: Practical syntheses and in vitro antibacterial studies of tris-catecholate siderophore-aminopenicillin conjugates reveals selectively potent antipseudomonal activity J. Am. Chem. Soc. 134, 9898-9901
26. Starr, J., Brown, M. F., Aschenbrenner, L., Caspers, N., Che, Y., Gerstenberger, B. S., Huband, M., Knafels, J. D., Lemmon, M. M., Li, C., McCurdy, S. P., McElroy, E., Rauckhorst, M. R., Tomaras, A. P., Young, J. A., Zaniewski, R. P., Shanmugasundaram, V., and Han, S. (2014) Siderophore receptor-mediated uptake of lactivicin analogues in Gram-negative bacteria J. Med. Chem. 57, 3845-3855
27. Górska, A., Sloderbach, A., and Marszałł, M. P. (2014) Siderophore-drug complexes: Potential medicinal applications of the "Trojan horse" strategy Trends Pharmacol. Sci. 35, 442-449
28. Jones, C. M., Wells, R. M., Madduri, A. V. R., Renfrow, M. B., Ratledge, C., Moody, D. B., and Niederweis, M. (2014) Self-poisoning of Mycobacterium tuberculosis by interrupting siderophore recycling Proc. Natl. Acad. Sci. U.S.A. 111, 1945-1950
29. Mathavan, I., Zirah, S., Mehmood, S., Choudhury, H. G., Goulard, C., Li, Y., Robinson, C. V., Rebuffat, S., and Beis, K. (2014) Structural basis for hijacking siderophore receptors by antimicrobial lasso peptides Nat. Chem. Biol. 10, 340-342
30. Wurst, J. M., Drake, E. J., Theriault, J. R., Jewett, I. T., Verplank, L., Perez, J. R., Dandapani, S., Palmer, M., Moskowitz, S. M., Schreiber, S. L., Munoz, B., and Gulick, A. M. (2014) Identification of inhibitors of PvdQ, an enzyme involved in the synthesis of the siderophore pyoverdine ACS Chem. Biol. 9, 1536-1544
31. Garénaux, A., Caza, M., and Dozois, C. M. (2011) The ins and outs of siderophore mediated iron uptake by extra-intestinal pathogenic Escherichia coli Vet. Microbiol. 153, 89-98
32. Brickman, T. J. and Armstrong, S. K. (2005) Bordetella AlcS transporter functions in alcaligin siderophore export and is central to inducer sensing in positive regulation of alcaligin system gene expression J. Bacteriol. 187, 3650-3661
33. Stintzi, A., Barnes, C., Xu, J., and Raymond, K. N. (2000) Microbial iron transport via a siderophore shuttle: A membrane ion transport paradigm Proc. Natl. Acad. Sci. U.S.A. 97, 10691-10696
34. Dertz, E. A., Stintzi, A., and Raymond, K. N. (2006) Siderophore-mediated iron transport in Bacillus subtilis and Corynebacterium glutamicum JBIC, J. Biol. Inorg. Chem. 11, 1087-1097
35. Chu, B. C. H., Otten, R., Krewulak, K. D., Mulder, F. A. A., and Vogel, H. J. (2014) The solution structure, binding properties, and dynamics of the bacterial siderophore-binding protein FepB J. Biol. Chem. 289, 29219-29234
36. Lin, H., Fischbach, M. A., Liu, D. R., and Walsh, C. T. (2005) In vitro characterization of salmochelin and enterobactin trilactone hydrolases IroD, IroE, and Fes J. Am. Chem. Soc. 127, 11075-11084
37. Larsen, N. A., Lin, H., Wei, R., Fischbach, M. A., and Walsh, C. T. (2006) Structural characterization of enterobactin hydrolase IroE Biochemistry 45, 10184-10190
38. Morton, D. J., Turman, E. J., Hensley, P. D., VanWagoner, T. M., Seale, T. W., Whitby, P. W., and Stull, T. L. (2010) Identification of a siderophore utilization locus in nontypeable Haemophilus influenzae BMC Microbiol. 10, 113
39. Brickman, T. J. and Mcintosh, M. A. (1992) Overexpression and purification of ferric enterobactin esterase from Escherichia coli J. Biol. Chem. 267, 12350-12355
40. Miethke, M., Hou, J., and Marahiel, M. A. (2011) The siderophore-interacting protein YqjH acts as a ferric reductase in different iron assimilation pathways of Escherichia coli Biochemistry 50, 10951-10964
41. Wang, S., Wu, Y., and Outten, F. W. (2011) Fur and the novel regulator YqjI control transcription of the ferric reductase gene yqjH in Escherichia coli J. Bacteriol. 563-574
42. Kaplan, C. D. and Kaplan, J. (2009) Iron Acquisition and Transcriptional Regulation Chem. Rev. 109, 4536-4552
43. Wang, S., Blahut, M., Wu, Y., Philipkosky, K. E., and Outten, F. W. (2014) Communication between binding sites is required for YqjI regulation of target promoters within the yqjH-yqjI intergenic region J. Bacteriol. 196, 3199-3207
44. Matzanke, B. F., Anemüller, S., Schünemann, V., Trautwein, A. X., and Hantke, K. (2004) FhuF, part of a siderophore-reductase system Biochemistry 43, 1386-1392
45. Miethke, M., Pierik, A., Peuckert, F., Seubert, A., and Marahiel, M. (2011) Identification and characterization of a novel-type ferric siderophore reductase from a Gram-positive extremophile J. Biol. Chem. 286, 2245-2260
46. Dimise, E. J., Widboom, P. F., and Bruner, S. D. (2008) Structure elucidation and biosynthesis of fuscachelins, peptide siderophores from the moderate thermophile Thermobifida fusca Proc. Natl. Acad. Sci. U.S.A. 105, 15311-15316
47. Dimise, E. J., Condurso, H. L., Stoker, G. E., and Bruner, S. D. (2012) Synthesis and structure confirmation of fuscachelins A and B, structurally unique natural product siderophores from Thermobifida fusca Org. Biomol. Chem. 10, 5353-5356
48. Lykidis, A., Mavromatis, K., Ivanova, N., Anderson, I., Land, M., DiBartolo, G., Martinez, M., Lapidus, A., Lucas, S., Copeland, A., Richardson, P., Wilson, D. B., and Kyrpides, N. (2007) Genome sequence and analysis of the soil cellulolytic actinomycete Thermobifida fusca YX J. Bacteriol. 189, 2477-2486
49. Deng, Y. and Zhang, X. (2014) DtxR, an iron-dependent transcriptional repressor that regulates the expression of siderophore gene clusters in Thermobifida fusca FEMS Microbiol. Lett. 362, 1-6
50. Bamford, V. A., Armour, M., Mitchell, S. A., Cartron, M., Andrews, S. C., and Watson, K. A. (2008) Preliminary X-ray diffraction analysis of YqjH from Escherichia coli: A putative cytoplasmic ferri-siderophore reductase Acta Crystallogr. F64, 792-796
51. PDB entry 2GPJ. Crystal structure of siderophore-interacting protein (ZP-00813641.1) from S. putrefaciens CN-32 at 2.20 Å resolution.
52. Kabsch, W. (2010) XDS Acta Crystallogr. D66, 125-132
53. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674
54. Afonine, P. V., Grosse-Kunstleve, R. W., Echols, N., Headd, J. J., Moriarty, N. W., Mustyakimov, M., Terwilliger, T. C., Urzhumtsev, A., Zwart, P. H., and Adams, P. D. (2012) Towards automated crystallographic structure refinement with phenix.refine Acta Crystallogr. D68, 352-367
55. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66, 213-221
56. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
57. Pymol: The PyMOL Molecular Graphics System, version 1.4.1 (2012) Schrödinger, LLC, Portland, OR.
58. Fox, J. L. (1974) Sodium dithionite reduction of flavin FEBS Lett. 39, 53-55
59. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372, 774-797
60. Holm, L. and Rosenström, P. (2010) Dali server: Conservation mapping in 3D Nucleic Acids Res. 38, 545-549
61. Yamada, M., Tamada, T., Takeda, K., Matsumoto, F., Ohno, H., Kosugi, M., Takaba, K., Shoyama, Y., Kimura, S., Kuroki, R., and Miki, K. (2013) Elucidations of the catalytic cycle of NADH-cytochrome b5 reductase by X-ray crystallography: New insights into regulation of efficient electron transfer J. Mol. Biol. 425, 4295-4306
62. Koder, R. L. and Miller, A. F. (1998) Steady-state kinetic mechanism, stereospecificity, substrate and inhibitor specificity of Enterobacter cloacae nitroreductase Biochim. Biophys. Acta 1387, 395-405
63. Rane, M. J. and Calvo, K. C. (1997) Reversal of the nucleotide specificity of ketol acid reductoisomerase by site-directed mutagenesis identifies the NADPH binding site Arch. Biochem. Biophys. 338, 83-89
64. Petschacher, B., Leitgeb, S., Kavanagh, K. L., Wilson, D. K., and Nidetzky, B. (2005) The coenzyme specificity of Candida tenuis xylose reductase (AKR2B5) explored by site-directed mutagenesis and X-ray crystallography Biochem. J. 385, 75-83
65. Brinkmann-Chen, S., Flock, T., Cahn, J. K. B., Snow, C. D., Brustad, E. M., McIntosh, J. A., Meinhold, P., Zhang, L., and Arnold, F. H. (2013) General approach to reversing ketol-acid reductoisomerase cofactor dependence from NADPH to NADH Proc. Natl. Acad. Sci. U.S.A. 110, 10946-10951
66. Butterton, J. R. and Calderwood, S. B. (1994) Identification, cloning, and sequencing of a gene required for ferric vibriobactin utilization by Vibrio cholerae J. Bacteriol. 176, 5631-5638
67. McWilliam, H., Li, W., Uludag, M., Squizzato, S., Park, Y. M., Buso, N., Cowley, A. P., and Lopez, R. (2013) Analysis tool web services from the EMBL-EBI Nucleic Acids Res. 41, 597-600
68. Söding, J., Biegert, A., and Lupas, A. N. (2005) The HHpred interactive server for protein homology detection and structure prediction Nucleic Acids Res. 33, 244-248
69. Mewies, M., McIntire, W. S., and Scrutton, N. S. (1998) Covalent attachment of flavin adenine dinucleotide (FAD) and flavin mononucleotide (FMN) to enzymes: The current state of affairs Protein Sci. 7, 7-20
70. Huang, C. H., Lai, W. L., Lee, M. H., Chen, C. J., Vasella, A., Tsai, Y. C., and Liaw, S. H. (2005) Crystal structure of glucooligosaccharide oxidase from Acremonium strictum: A novel flavinylation of 6-S-cysteinyl, 8a-N1-histidyl FAD J. Biol. Chem. 280, 38831-38838
71. Macindoe, G., Mavridis, L., Venkatraman, V., Devignes, M. D., and Ritchie, D. W. (2010) HexServer: An FFT-based protein docking server powered by graphics processors Nucleic Acids Res. 38, 445-449
72. Karlsson, A., Beharry, Z. M., Matthew Eby, D., Coulter, E. D., Neidle, E. L., Kurtz, D. M., Eklund, H., and Ramaswamy, S. (2002) X-ray crystal structure of benzoate 1,2-dioxygenase reductase from Acinetobacter sp. strain ADP1 J. Mol. Biol. 318, 261-272
73. Correll, C. C., Batie, C. J., Ballou, D. P., Ludwig, M. L., Batie, J., Ballou, D. P., Correll, C. C., and Ludwig, M. L. (1992) Phthalate dioxygenase reductase: A modular structure for electron transfer from pyridine nucleotides to [2Fe-2S] Science 258, 1604-1610
74. Rosenzweig, A. C., Frederick, C. A., Lippard, S. J., and Nordlund, P. (1993) Crystal structure of a bacterial non-haem iron hydroxylase that catalyses the biological oxidation of methane Nature 366, 537-543
75. Senda, M., Kishigami, S., Kimura, S., Fukuda, M., Ishida, T., and Senda, T. (2007) Molecular mechanism of the redox-dependent interaction between NADH-dependent ferredoxin reductase and Rieske-type [2Fe-2S] ferredoxin J. Mol. Biol. 373, 382-400
76. Fang, R., Chen, F., Dong, Z., Hu, D., Barbera, A. J., Clark, E. A., Fang, J., Yang, Y., Mei, P., Rutenberg, M., Li, Z., Zhang, Y., Xu, Y., Yang, H., Wang, P., Simon, M. D., Zhou, Q., Li, J., Marynick, M. P., Li, X., Lu, H., Kaiser, U. B., Kingston, R. E., Xu, Y., and Shi, Y. G. (2013) LSD2/KDM1B and its cofactor NPAC/GLYR1 endow a structural and molecular model for regulation of H3K4 demethylation Mol. Cell 49, 558-570
77. Butterton, J. R., Choi, M. H., Watnick, P. I., Carroll, P. A., and Calderwood, S. B. (2000) Vibrio cholerae VibF is required for vibriobactin synthesis and is a member of the family of nonribosomal peptide synthetases J. Bacteriol. 182, 1731-1738
78. Altschup, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic Local Alignment Search Tool J. Mol. Biol. 215, 403-410
79. Granger, J. B., Lu, Z., Ferguson, J. B., Santa Maria, P. J., and Novak, W. R. P. (2013) Cloning, expression, purification and characterization of an iron-dependent regulator protein from Thermobifida fusca Protein Expression Purif. 92, 190-194
80. Patel, K., Kumar, A., and Durani, S. (2007) Analysis of the structural consensus of the zinc coordination centers of metalloprotein structures Biochim. Biophys. Acta 1774, 1247-1253