The general importance of the Fe-S cluster prosthetic groups in biology is primarily attributable to specific features of iron and sulfur chemistry, and the assembly and interplay of the Fe-S cluster core with the surrounding protein is the key to in-depth understanding of the underlying mechanisms. In the aerobic and thermoacidophilic archaea, zinc-containing ferredoxin is abundant in the cytoplasm, functioning as a key electron carrier, and many Fe-S enzymes are produced to participate in the central metabolic and energetic pathways. De novo formation of intracellular Fe-S clusters does not occur spontaneously but most likely requires the operation of a SufBCD complex of the SUF machinery, which is the only Fe-S cluster biosynthesis system conserved in these archaea. In this paper, a brief introduction to the buildup and maintenance of the intracellular Fe-S world in aerobic and hyperthermoacidophilic crenarchaeotes, mainly Sulfolobus, is given in the biochemical, genetic, and evolutionary context. 1. Introduction The structure of a metal site in metalloenzymes critically influences the fine-tuning of redox and/or catalytic activities in biology [1–3], and the substitution and/or displacement events at the local metal-binding site(s) in a protein might have greatly enhanced their capabilities of conducting a wide range of unique redox chemistry in biological electron transfer conduits which often use a limited number of basic protein scaffolds. Iron-sulfur (Fe-S) cluster prosthetic groups, consisting of nonheme iron and acid-labile inorganic sulfide atoms, are functionally highly versatile and may be among the most ancient modular metallocofactors to sustain biologically and evolutionary indispensable processes in the early days of primitive life on earth, such as electron transfer, substrate binding/activation in the iron/sulfur storage, hydrogen and nitrogen metabolisms, anaerobic respiration, and photosynthesis—some of the most complicated reactions in the chemistry of life processes [1, 2, 4, 5]. Among protein-bound Fe-S redox sites, which usually contain terminal sulfur ligands from cysteinyl groups, the mononuclear Fe atom in a tetrahedral environment of S ligands is the simplest form, as seen in the rubredoxin family. Other major forms are polynuclear clusters, such as those containing [2Fe-2S], [3Fe-4S], [4Fe-4S], or [8Fe-7S] core units, found in a variety of ferredoxins and complex Fe-S metalloenzymes. In addition to their electron transfer roles, Fe-S proteins are also known to participate in substrate binding/activation, environmental
References
[1]
R. H. Holm, P. Kennepohl, and E. I. Solomon, “Structural and functional aspects of metal sites in biology,” Chemical Reviews, vol. 96, no. 7, pp. 2239–2314, 1996.
[2]
H. Beinert, R. H. Holm, and E. Münck, “Iron-sulfur clusters: nature's modular, multipurpose structures,” Science, vol. 277, no. 5326, pp. 653–659, 1997.
[3]
D. C. Rees and J. B. Howard, “The interface between the biological and inorganic worlds: iron-sulfur metalloclusters,” Science, vol. 300, no. 5621, pp. 929–931, 2003.
[4]
M. W. W. Adams, “Novel iron-sulfur centers in metalloenzymes and redox proteins from extremely thermophilic bacteria,” Advances in Inorganic Chemistry, vol. 38, pp. 341–396, 1992.
[5]
H. Beinert, “Iron-sulfur proteins: ancient structures, still full of surprises,” Journal of Biological Inorganic Chemistry, vol. 5, no. 1, pp. 2–15, 2000.
[6]
H. Beinert, M. C. Kennedy, and C. D. Stout, “Aconitase as iron-sulfur protein, enzyme, and iron-regulatory protein,” Chemical Reviews, vol. 96, no. 7, pp. 2335–2373, 1996.
[7]
D. C. Johnson, D. R. Dean, A. D. Smith, and M. K. Johnson, “Structure, function, and formation of biological iron-sulfur clusters,” Annual Review of Biochemistry, vol. 74, pp. 247–281, 2005.
[8]
R. Lill and U. Mühlenhoff, “Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases,” Annual Review of Biochemistry, vol. 77, pp. 669–700, 2008.
[9]
T. A. Rouault and W.-H. Tong, “Iron-sulphur cluster biogenesis and mitochondrial iron homeostasis,” Nature Reviews Molecular Cell Biology, vol. 6, no. 4, pp. 345–351, 2005.
[10]
C. R. Woese, O. Kandler, and M. L. Wheelis, “Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 12, pp. 4576–4579, 1990.
[11]
G. J. Olsen, C. R. Woese, and R. Overbeek, “The winds of (evolutionary) change: breathing new life into microbiology,” Journal of Bacteriology, vol. 176, no. 1, pp. 1–6, 1994.
[12]
K. O. Stetter, “Microbial life in hyperthermal environments,” ASM News, vol. 61, pp. 285–290, 1995.
[13]
K. O. Stetter, “Hyperthermophiles in the history of life,” Philosophical Transactions of the Royal Society B, vol. 361, no. 1474, pp. 1837–1842, 2006.
[14]
L. Kerscher and D. Oesterhelt, “Ferredoxin is the coenzyme of α-ketoacid oxidoreductases in Halobacterium halobium,” FEBS Letters, vol. 83, no. 2, pp. 197–201, 1977.
[15]
L. Kerscher, S. Nowitzki, and D. Oesterhelt, “Thermoacidophilic archaebacteria contain bacterial-type ferredoxins acting as electron acceptors of 2-oxoacid: ferredoxin oxidoreductases,” European Journal of Biochemistry, vol. 128, no. 1, pp. 223–230, 1982.
[16]
T. Iwasaki, T. Wakagi, Y. Isogai, K. Tanaka, T. Iizuka, and T. Oshima, “Functional and evolutionary implications of a [3Fe-4S] cluster of the dicluster-type ferredoxin from the thermoacidophilic archaeon, Sulfolobus sp. strain 7,” Journal of Biological Chemistry, vol. 269, no. 47, pp. 29444–29450, 1994.
[17]
T. Iwasaki and T. Oshima, “Ferredoxin and related enzymes from Sulfolobus,” Methods in Enzymology, vol. 334, pp. 3–22, 2001.
[18]
H. Beinert, “Semi-micro methods for analysis of labile sulfide and of labile sulfide plus sulfane sulfur in unusually stable iron-sulfur proteins,” Analytical Biochemistry, vol. 131, no. 2, pp. 373–378, 1983.
[19]
M. Ciaramella, A. Napoli, and M. Rossi, “Another extreme genome: how to live at pH 0,” Trends in Microbiology, vol. 13, no. 2, pp. 49–51, 2005.
[20]
A. Angelov and W. Liebl, “Insights into extreme thermoacidophily based on genome analysis of Picrophilus torridus and other thermoacidophilic archaea,” Journal of Biotechnology, vol. 126, no. 1, pp. 3–10, 2006.
[21]
C. Baker-Austin and M. Dopson, “Life in acid: pH homeostasis in acidophiles,” Trends in Microbiology, vol. 15, no. 4, pp. 165–171, 2007.
[22]
K. S. Auernik, C. R. Cooper, and R. M. Kelly, “Life in hot acid: pathway analyses in extremely thermoacidophilic archaea,” Current Opinion in Biotechnology, vol. 19, no. 5, pp. 445–453, 2008.
[23]
M. W. W. Adams, “Enzymes and proteins from organisms that grow near and above ,” Annual Review of Microbiology, vol. 47, pp. 627–658, 1993.
[24]
M. W. W. Adams, “Biochemical diversity among sulfur-dependent, hyperthermophilic microorganisms,” FEMS Microbiology Reviews, vol. 15, no. 2-3, pp. 261–277, 1994.
[25]
M. K. Johnson, R. E. Duderstadt, and E. C. Duin, “Biological and synthetic [Fe3S4] clusters,” Advances in Inorganic Chemistry, vol. 47, pp. 1–82, 1999.
[26]
F. E. Jenney Jr. and M. W. W. Adams, “Hydrogenases of the model hyperthermophiles,” Annals of the New York Academy of Sciences, vol. 1125, pp. 252–266, 2008.
[27]
L. Kerscher and D. Oesterhelt, “Pyruvate: ferredoxin oxidoreductase—new findings on an ancient enzyme,” Trends in Biochemical Sciences, vol. 7, no. 10, pp. 371–374, 1982.
[28]
L. Kerscher and D. Oesterhelt, “The catalytic mechanism of 2-oxoacid: ferredoxin oxidoreductases from Halobacterium halobium. One electron transfer at two distinct steps of the catalytic cycle,” European Journal of Biochemistry, vol. 116, no. 3, pp. 595–600, 1981.
[29]
L. Kerscher and D. Oesterhelt, “Purification and properties of two 2-oxoacid: ferredoxin oxidoreductases from Halobacterium halobium,” European Journal of Biochemistry, vol. 116, no. 3, pp. 587–594, 1981.
[30]
Q. Zhang, T. Iwasaki, T. Wakagi, and T. Oshima, “2-oxoacid:ferredoxin oxidoreductase from the thermoacidophilic archaeon, Sulfolobus sp. strain 7,” Journal of Biochemistry, vol. 120, no. 3, pp. 587–599, 1996.
[31]
A. Kletzin and M. W. W. Adams, “Molecular and phylogenetic characterization of pyruvate and 2-ketoisovalerate ferredoxin oxidoreductases from Pyrococcus furiosus and pyruvate ferredoxin oxidoreductase from Thermotoga maritima,” Journal of Bacteriology, vol. 178, no. 1, pp. 248–257, 1996.
[32]
E. Chabrière, M.-H. Charon, A. Volbeda, L. Pieulle, E. C. Hatchikian, and J.-C. Fontecilla-Camps, “Crystal structures of the key anaerobic enzyme pyruvate ferredoxin oxidoreductase free and in complex with pyruvate,” Nature Structural Biology, vol. 6, no. 2, pp. 182–190, 1999.
[33]
E. Chabrière, X. Vernède, B. Guigliarelli, M.-H. Charon, E. C. Hatchikian, and J. C. Fontecilla-Camps, “Crystal structure of the free radical intermediate of pyruvate: ferredoxin oxidoreductase,” Science, vol. 294, no. 5551, pp. 2559–2563, 2001.
[34]
W. Plaga, F. Lottspeich, and D. Oesterhelt, “Improved purification, crystallization and primary structure of pyruvate: ferredoxin oxidoreductase from Halobacterium halobium,” European Journal of Biochemistry, vol. 205, no. 1, pp. 391–397, 1992.
[35]
T. Iwasaki, A. Kounosu, M. Aoshima et al., “Novel [2Fe-2S]-type redox center C in sdhC of archaeal respiratory complex II from Sulfolobus tokodaii strain 7,” Journal of Biological Chemistry, vol. 277, no. 42, pp. 39642–39648, 2002.
[36]
C. Enroth, B. T. Eger, K. Okamoto, T. Nishino, T. Nishino, and E. F. Pai, “Crystal structures of bovine milk xanthine dehydrogenase and xanthine oxidase: structure-based mechanism of conversion,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 20, pp. 10723–10728, 2000.
[37]
L. A. Sazanov and P. Hinchliffe, “Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus,” Science, vol. 311, no. 5766, pp. 1430–1436, 2006.
[38]
A. Hirata, B. J. Klein, and K. S. Murakami, “The X-ray crystal structure of RNA polymerase from Archaea,” Nature, vol. 451, no. 7180, pp. 851–854, 2008.
[39]
M. Teixeira, R. Batista, A. P. Campos et al., “A seven-iron ferredoxin from the thermoacidophilic archaeon Desulfurolobus ambivalens,” European Journal of Biochemistry, vol. 227, no. 1-2, pp. 322–327, 1995.
[40]
J. L. Breton, J. L. C. Duff, J. N. Butt et al., “Identification of the iron-sulfur clusters in a ferredoxin from the archaeon Sulfolobus acidocaldarius—evidence for a reduced [3Fe-4S] cluster with pH-dependent electronic properties,” European Journal of Biochemistry, vol. 233, no. 3, pp. 937–946, 1995.
[41]
T. Iwasaki, T. Suzuki, T. Kon et al., “Novel zinc-containing ferredoxin family in thermoacidophilic archaea,” Journal of Biological Chemistry, vol. 272, no. 6, pp. 3453–3458, 1997.
[42]
C. M. Gomes, A. Faria, J. C. Carita et al., “Di-cluster, seven-iron ferredoxins from hyperthermophilic Sulfolobales,” Journal of Biological Inorganic Chemistry, vol. 3, no. 5, pp. 499–507, 1998.
[43]
N. J. Cosper, C. M. V. St？lhandske, H. Iwasaki, T. Oshima, R. A. Scott, and T. Iwasaki, “Structural conservation of the isolated zinc site in archaeal zinc- containing ferredoxins as revealed by X-ray absorption spectroscopic analysis and its evolutionary implications,” Journal of Biological Chemistry, vol. 274, no. 33, pp. 23160–23168, 1999.
[44]
T. Iwasaki, E. Watanabe, D. Ohmori et al., “Spectroscopic investigation of selective cluster conversion of archaeal zinc-containing ferredoxin from Sulfolobus sp. strain 7,” Journal of Biological Chemistry, vol. 275, no. 33, pp. 25391–25401, 2000.
[45]
R. C. Conover, A. T. Kowal, W. Fu et al., “Spectroscopic characterization of the novel iron-sulfur cluster in Pyrococcus furiosus ferrodoxin,” Journal of Biological Chemistry, vol. 265, no. 15, pp. 8533–8541, 1990.
[46]
T. Imai, K. Taguchi, Y. Ogawara et al., “Characterization and cloning of an extremely thermostable, Pyrococcus furiosus-type 4Fe ferredoxin from Thermococcus profundus,” Journal of Biochemistry, vol. 130, no. 5, pp. 649–655, 2001.
[47]
T. Fujii, Y. Hata, T. Wakagi, N. Tanaka, and T. Oshima, “Novel zinc-binding centre in thermoacidophilic archaeal ferredoxins,” Nature Structural Biology, vol. 3, no. 10, pp. 834–837, 1996.
[48]
T. Fujii, Y. Hata, M. Oozeki et al., “The crystal structure of zinc-containing ferredoxin from the thermoacidophilic archaeon Sulfolobus sp. strain 7,” Biochemistry, vol. 36, no. 6, pp. 1505–1513, 1997.
[49]
C. Fraz？o, D. Arag？o, R. Coelho et al., “Crystallographic analysis of the intact metal centres and in a -containing ferredoxin,” FEBS Letters, vol. 582, no. 5, pp. 763–767, 2008.
[50]
K. Kojoh, H. Matsuzawa, and T. Wakagi, “Zinc and an N-terminal extra stretch of the ferredoxin from a thermoacidophilic archaeon stabilize the molecule at high temperature,” European Journal of Biochemistry, vol. 264, no. 1, pp. 85–91, 1999.
[51]
S. S. Leal and C. M. Gomes, “Studies of the molten globule state of ferredoxin: structural characterization and implications on protein folding and iron-sulfur center assembly,” Proteins, vol. 68, no. 3, pp. 606–616, 2007.
[52]
S. S. Leal and C. M. Gomes, “On the relative contribution of ionic interactions over iron-sulfur clusters to ferredoxin stability,” Biochimica et Biophysica Acta, vol. 1784, no. 11, pp. 1596–1600, 2008.
[53]
R. Rocha, S. S. Leal, V. H. Teixeira et al., “Natural domain design: enhanced thermal stability of a zinc-lacking ferredoxin isoform shows that a hydrophobic core efficiently replaces the structural metal site,” Biochemistry, vol. 45, no. 34, pp. 10376–10384, 2006.
[54]
S. Janssen, J. Trinc？o, M. Teixeira, G. Sch？fer, and S. Anemüller, “Ferredoxins from the archaeon Acidianus ambivalens: overexpression and characterization of the non-zinc-containing ferredoxin FdB,” Biological Chemistry, vol. 382, no. 10, pp. 1501–1507, 2001.
[55]
L. Kerscher, D. Oesterhelt, R. Cammack, and D. O. Hall, “A new plant type ferredoxin from halobacteria,” European Journal of Biochemistry, vol. 71, no. 1, pp. 101–108, 1976.
[56]
F. Pfeifer, J. Griffig, and D. Oesterhelt, “The fdx gene encoding the [2Fe-2S] ferredoxin of Halobacterium salinarium (H. halobium),” Molecular and General Genetics, vol. 239, no. 1-2, pp. 66–71, 1993.
[57]
F. Frolow, M. Harel, J. L. Sussman, M. Mevarech, and M. Shoham, “Insights into protein adaptation to a saturated salt environment from the crystal structure of a halophilic 2Fe-2S ferredoxin,” Nature Structural Biology, vol. 3, no. 5, pp. 452–458, 1996.
[58]
R. Moll and G. Sch？fer, “Chemiosmotic cycling across the plasma membrane of the thermoacidophilic archaebacterium Sulfolobus acidocaldarius,” FEBS Letters, vol. 232, no. 2, pp. 359–363, 1988.
[59]
D. G. Searcy, “Thermoplasma acidophilum: intracellular pH and potassium concentration,” Biochimica et Biophysica Acta, vol. 451, no. 1, pp. 278–286, 1976.
[60]
M. Lübben and G. Sch？fer, “Chemiosmotic energy conversion of the archaebacterial thermoacidophile Sulfolobus acidocaldarius: oxidative phosphorylation and the presence of an Fo-related N,N'-dicyclohexylcarbodiimide-binding proteolipid,” Journal of Bacteriology, vol. 171, no. 11, pp. 6106–6116, 1989.
[61]
O. Djaman, F. W. Outten, and J. A. Imlay, “Repair of oxidized iron-sulfur clusters in Escherichia coli,” Journal of Biological Chemistry, vol. 279, no. 43, pp. 44590–44599, 2004.
[62]
S. Knapp, S. Kardinahl, N. Hellgren, G. Tibbelin, G. Sch？fer, and R. Ladenstein, “Refined crystal structure of a superoxide dismutase from the hyperthermophilic archaeon Sulfolobus acidocaldarius at 2.2 ？ resolution,” Journal of Molecular Biology, vol. 285, no. 2, pp. 689–702, 1999.
[63]
T. Ursby, B. S. Adinolfi, S. Al-Karadaghi, E. De Vendittis, and V. Bocchini, “Iron superoxide dismutase from the archaeon Sulfolobus solfataricus: analysis of structure and thermostability,” Journal of Molecular Biology, vol. 286, no. 1, pp. 189–205, 1999.
[64]
B. Wiedenheft, J. Mosolf, D. Willits et al., “An archaeal antioxidant: characterization of a Dps-like protein from Sulfolobus solfataricus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 30, pp. 10551–10556, 2005.
[65]
G. H. Gauss, P. Benas, B. Wiedenheft, M. Young, T. Douglas, and C. M. Lawrence, “Structure of the DPS-like protein from Sulfolobus solfataricus reveals a bacterioferritin-like dimetal binding site within a DPS-like dodecameric assembly,” Biochemistry, vol. 45, no. 36, pp. 10815–10827, 2006.
[66]
W. S. Maaty, B. Wiedenheft, P. Tarlykov et al., “Something old, something new, something borrowed; how the thermoacidophilic archaeon Sulfolobus solfataricus responds to oxidative stress,” PLoS ONE, vol. 4, no. 9, Article ID e6964, 2009.
[67]
J. A. Hayden and M. P. Hendrich, “EPR spectroscopy and catalase activity of manganese-bound DNA-binding protein from nutrient starved cells,” Journal of Biological Inorganic Chemistry, vol. 15, no. 5, pp. 729–736, 2010.
[68]
G. Sch？fer, M. Engelhard, and V. Müller, “Bioenergetics of the archaea,” Microbiology and Molecular Biology Reviews, vol. 63, no. 3, pp. 570–620, 1999.
[69]
K. Denda, J. Konishi, K. Hajiro, T. Oshima, T. Date, and M. Yoshida, “Structure of an ATPase operon of an acidothermophilic archaebacterium, Sulfolobus acidocaldarius,” Journal of Biological Chemistry, vol. 265, no. 35, pp. 21509–21513, 1990.
[70]
M. Lübben and K. Morand, “Novel prenylated hemes as cofactors of cytochrome oxidases. Archaea have modified hemes A and O,” Journal of Biological Chemistry, vol. 269, no. 34, pp. 21473–21479, 1994.
[71]
T. Iwasaki, K. Matsuura, and T. Oshima, “Resolution of the aerobic respiratory system of the thermoacidophilic archaeon, Sulfolobus sp. strain 7: I. The archaeal terminal oxidase supercomplex is a functional fusion of respiratory complexes III and IV with no c-type cytochromes,” Journal of Biological Chemistry, vol. 270, no. 52, pp. 30881–30892, 1995.
[72]
M. Lübben, “Cytochromes of archaeal electron transfer chains,” Biochimica et Biophysica Acta, vol. 1229, no. 1, pp. 1–22, 1995.
[73]
T. Suzuki, T. Iwasaki, T. Uzawa et al., “Sulfolobus tokodaii sp. nov. (f. Sulfolobus sp. strain 7), a new member of the genus Sulfolobus isolated from Beppu Hot Springs, Japan,” Extremophiles, vol. 6, no. 1, pp. 39–44, 2002.
[74]
Y. Kawarabayasi, Y. Hino, H. Horikawa et al., “Complete genome sequence of an aerobic thermoacidophilic crenarchaeon, Sulfolobus tokodaii strain,” DNA Research, vol. 8, no. 4, pp. 123–140, 2001.
[75]
Q. She, R. K. Singh, F. Confalonieri et al., “The complete genome of the crenarchaeon Sulfolobus solfataricus P2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 14, pp. 7835–7840, 2001.
[76]
M. Lübben, B. Kolmerer, and M. Saraste, “An archaebacterial terminal oxidase combines core structures of two mitochondrial respiratory complexes,” EMBO Journal, vol. 11, no. 3, pp. 805–812, 1992.
[77]
M. Lübben, S. Arnaud, J. Castresana, A. Warne, S. P. J. Albracht, and M. Saraste, “A second terminal oxidase in Sulfolobus acidocaldarius,” European Journal of Biochemistry, vol. 224, no. 1, pp. 151–159, 1994.
[78]
J. Castresana, M. Lübben, and M. Saraste, “New archaebacterial genes coding for redox proteins: implications for the evolution of aerobic metabolism,” Journal of Molecular Biology, vol. 250, no. 2, pp. 202–210, 1995.
[79]
L. Chen, K. Brügger, M. Skovgaard et al., “The genome of Sulfolobus acidocaldarius, a model organism of the Crenarchaeota,” Journal of Bacteriology, vol. 187, no. 14, pp. 4992–4999, 2005.
[80]
J. Hemp and R. B. Gennis, “Diversity of the heme-copper superfamily in archaea: insights from genomics and structural modeling,” Results and Problems in Cell Differentiation, vol. 45, pp. 1–31, 2008.
[81]
J. P. Hosler, S. Ferguson-Miller, and D. A. Mills, “Energy transduction: proton transfer through the respiratory complexes,” Annual Review of Biochemistry, vol. 75, pp. 165–187, 2006.
[82]
K. Shimokata, Y. Katayama, H. Murayama et al., “The proton pumping pathway of bovine heart cytochrome c oxidase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 10, pp. 4200–4205, 2007.
[83]
L. Qin, J. Liu, D. A. Mills, D. A. Proshlyakov, C. Hiser, and S. Ferguson-Miller, “Redox-dependent conformational changes in cytochrome c oxidase suggest a gating mechanism for proton uptake,” Biochemistry, vol. 48, no. 23, pp. 5121–5130, 2009.
[84]
G. Br？ndén, R. B. Gennis, and P. Brzezinski, “Transmembrane proton translocation by cytochrome c oxidase,” Biochimica et Biophysica Acta, vol. 1757, no. 8, pp. 1052–1063, 2006.
[85]
E. A. Berry, M. Guergova-Kuras, L.-S. Huang, and A. R. Crofts, “Structure and function of cytochrome bc complexes,” Annual Review of Biochemistry, vol. 69, pp. 1005–1075, 2000.
[86]
A. R. Crofts, “The cytochrome bc1 complex: function in the context of structure,” Annual Review of Physiology, vol. 66, pp. 689–733, 2004.
[87]
W. A. Cramer, H. Zhang, J. Yan, G. Kurisu, and J. L. Smith, “Transmembrane traffic in the cytochrome b6f complex,” Annual Review of Biochemistry, vol. 75, pp. 769–790, 2006.
[88]
U. Kappler, L. I. Sly, and A. G. McEwan, “Respiratory gene clusters of Metallosphaera sedula—differential expression and transcriptional organization,” Microbiology, vol. 151, no. 1, pp. 35–43, 2005.
[89]
S. Bathe and P. R. Norris, “Ferrons iron- and sulfur-induced genes in Sulfolobus metallicus,” Applied and Environmental Microbiology, vol. 73, no. 8, pp. 2491–2497, 2007.
[90]
K. S. Auernik and R. M. Kelly, “Identification of components of electron transport chains in the extremely thermoacidophilic crenarchaeon Metallosphaera sedula through iron and sulfur compound oxidation transcriptomes,” Applied and Environmental Microbiology, vol. 74, no. 24, pp. 7723–7732, 2008.
[91]
A. Brooun, J. Bell, T. Freitas, R. W. Larsen, and M. Alam, “An archaeal aerotaxis transducer combines subunit I core structures of eukaryotic cytochrome c oxidase and eubacterial methyl-accepting chemotaxis proteins,” Journal of Bacteriology, vol. 180, no. 7, pp. 1642–1646, 1998.
[92]
R. I. Samoilova, D. Kolling, T. Uzawa, T. Iwasaki, A. R. Crofts, and S. A. Dikanov, “The interaction of the Rieske iron-sulfur protein with occupants of the Qo-site of the bc1 complex, probed by electron spin echo envelope modulation,” Journal of Biological Chemistry, vol. 277, no. 7, pp. 4605–4608, 2002.
[93]
M. L. Reno, N. L. Held, C. J. Fields, P. V. Burke, and R. J. Whitaker, “Biogeography of the Sulfolobus islandicus pan-genome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 21, pp. 8605–8610, 2009.
[94]
K. Deigweiher, T. L. Drell IV, A. Prutsch, A. J. Scheidig, and M. Lübben, “Expression, isolation, and crystallization of the catalytic domain of CopB, a putative copper transporting ATPase from the thermoacidophilic archaeon Sulfolobus solfataricus,” Journal of Bioenergetics and Biomembranes, vol. 36, no. 1, pp. 151–159, 2004.
[95]
B. De Hertogh, A.-C. Lantin, P. V. Baret, and A. Goffeau, “The archaeal P-type ATPases,” Journal of Bioenergetics and Biomembranes, vol. 36, no. 1, pp. 135–142, 2004.
[96]
R. Lill and G. Kispal, “Maturation of cellular Fe-S proteins: an essential function of mitochondria,” Trends in Biochemical Sciences, vol. 25, no. 8, pp. 352–356, 2000.
[97]
J. Frazzon, J. R. Fick, and D. R. Dean, “Biosynthesis of iron-sulphur clusters is a complex and highly conserved process,” Biochemical Society Transactions, vol. 30, no. 4, pp. 680–685, 2002.
[98]
Y. Takahashi and U. Tokumoto, “A third bacterial system for the assembly of iron-sulfur clusters with homologs in Archaea and plastids,” Journal of Biological Chemistry, vol. 277, no. 32, pp. 28380–28383, 2002.
[99]
S. Bandyopadhyay, K. Chandramouli, and M. K. Johnson, “Iron-sulfur cluster biosynthesis,” Biochemical Society Transactions, vol. 36, no. 6, pp. 1112–1119, 2008.
[100]
M. Fontecave and S. Ollagnier-de-Choudens, “Iron-sulfur cluster biosynthesis in bacteria: mechanisms of cluster assembly and transfer,” Archives of Biochemistry and Biophysics, vol. 474, no. 2, pp. 226–237, 2008.
[101]
C. Ayala-Castro, A. Saini, and F. W. Outten, “Fe-S cluster assembly pathways in bacteria,” Microbiology and Molecular Biology Reviews, vol. 72, no. 1, pp. 110–125, 2008.
[102]
Y. Takahashi and M. Nakamura, “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,” Journal of Biochemistry, vol. 126, no. 5, pp. 917–926, 1999.
[103]
U. Tokumoto and Y. Takahashi, “Genetic analysis of the isc operon in Escherichia coli involved in the biogenesis of cellular iron-sulfur proteins,” Journal of Biochemistry, vol. 130, no. 1, pp. 63–71, 2001.
[104]
U. Tokumoto, S. Nomura, Y. Minami et al., “Network of protein-protein interactions among iron-sulfur cluster assembly proteins in Escherichia coli,” Journal of Biochemistry, vol. 131, no. 5, pp. 713–719, 2002.
[105]
S. I. Patzer and K. Hantke, “SufS is a NifS-like protein, and sufd is necessary for stability of the [2Fe-2S] FhuF protein in Escherichia coli,” Journal of Bacteriology, vol. 181, no. 10, pp. 3307–3309, 1999.
[106]
N. Rouhier, J. Couturier, M. K. Johnson, and J.-P. Jacquot, “Glutaredoxins: roles in iron homeostasis,” Trends in Biochemical Sciences, vol. 35, no. 1, pp. 43–52, 2010.
[107]
D. J. A. Netz, A. J. Pierik, M. Stümpfig, U. Mühlenhoff, and R. Lill, “The Cfd1-Nbp35 complex acts as a scaffold for iron-sulfur protein assembly in the yeast cytosol,” Nature Chemical Biology, vol. 3, no. 5, pp. 278–286, 2007.
[108]
L. Zheng and D. R. Dean, “Catalytic formation of a nitrogenase iron-sulfur cluster,” Journal of Biological Chemistry, vol. 269, no. 29, pp. 18723–18726, 1994.
[109]
L. Zheng, V. L. Cash, D. H. Flint, and D. R. Dean, “Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii,” Journal of Biological Chemistry, vol. 273, no. 21, pp. 13264–13272, 1998.
[110]
D. H. Flint, “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,” Journal of Biological Chemistry, vol. 271, no. 27, pp. 16068–16074, 1996.
[111]
S.-I. Kato, H. Mihara, T. Kurihara 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,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 9, pp. 5948–5952, 2002.
[112]
L. Loiseau, S. Ollagnier-de-Choudens, L. Nachin, M. Fontecave, and F. Barras, “Biogenesis of Fe-S cluster by the bacterial suf system. SufS and SufE form a new type of cysteine desulfurase,” Journal of Biological Chemistry, vol. 278, no. 40, pp. 38352–38359, 2003.
[113]
F. W. Outten, M. J. Wood, F. M. Mu？oz, and G. Storz, “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,” Journal of Biological Chemistry, vol. 278, no. 46, pp. 45713–45719, 2003.
[114]
J. N. Agar, C. Krebs, J. Frazzon, B. H. Huynh, D. R. Dean, and M. K. Johnson, “IscU as a scaffold for iron-sulfur cluster biosynthesis: sequential assembly of [2Fe-2S] and [4Fe-4S] clusters in IscU,” Biochemistry, vol. 39, no. 27, pp. 7856–7862, 2000.
[115]
K. Chandramouli and M. K. Johnson, “HscA and HscB stimulate [2Fe-2S] cluster transfer from IscU to apoferredoxin in an ATP-dependent reaction,” Biochemistry, vol. 45, no. 37, pp. 11087–11095, 2006.
[116]
K. Chandramouli, M.-C. Unciuleac, S. Naik, D. R. Dean, H. H. Boi, and M. K. Johnson, “Formation and properties of [4Fe-4S] clusters on the IscU scaffold protein,” Biochemistry, vol. 46, no. 23, pp. 6804–6811, 2007.
[117]
M.-C. Unciuleac, K. Chandramouli, S. Naik et al., “In vitro activation of apo-aconitase using a [4Fe-4S] cluster-loaded form of the IscU [Fe-S] cluster scaffolding protein,” Biochemistry, vol. 46, no. 23, pp. 6812–6821, 2007.
[118]
E. C. Raulfs, I. P. O'Carroll, P. C. Dos Santos, M.-C. Unciuleac, and D. R. Dean, “In vivo iron-sulfur cluster formation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 25, pp. 8591–8596, 2008.
[119]
H. K. Chahal, Y. Dai, A. Saini, C. Ayala-Castro, and F. W. Outten, “The SufBCD Fe-S scaffold complex interacts with sufa for Fe-s cluster transfer,” Biochemistry, vol. 48, no. 44, pp. 10644–10653, 2009.
[120]
S. Wollers, G. Layer, R. Garcia-Serres et al., “Iron-sulfur (Fe-S) cluster assembly: the SufBCD complex is a new type of Fe-S scaffold with a flavin redox cofactor,” Journal of Biological Chemistry, vol. 285, no. 30, pp. 23331–23341, 2010.
[121]
C. J. Schwartz, J. L. Giel, T. Patschkowski et al., “IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 26, pp. 14895–14900, 2001.
[122]
F. W. Outten, O. Djaman, and G. Storz, “A suf operon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli,” Molecular Microbiology, vol. 52, no. 3, pp. 861–872, 2004.
[123]
U. Tokumoto, S. Kitamura, K. Fukuyama, and Y. Takahashi, “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,” Journal of Biochemistry, vol. 136, no. 2, pp. 199–209, 2004.
[124]
M. Zheng, X. Wang, L. J. Templeton, D. R. Smulski, R. A. LaRossa, and G. Storz, “DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide,” Journal of Bacteriology, vol. 183, no. 15, pp. 4562–4570, 2001.
[125]
K.-C. Lee, W.-S. Yeo, and J.-H. Roe, “Oxidant-responsive induction of the suf operon, encoding a Fe-S assembly system, through Fur and IscR in Escherichia coli,” Journal of Bacteriology, vol. 190, no. 24, pp. 8244–8247, 2008.
[126]
D. Vinella, C. Brochier-Armanet, L. Loiseau, E. Talla, and F. Barras, “Iron-sulfur (Fe/S) protein biogenesis: phylogenomic and genetic studies of A-type carriers,” PLoS Genetics, vol. 5, no. 5, Article ID e1000497, 2009.
[127]
L. Nachin, L. Loiseau, D. Expert, and F. Barras, “SufC: an unorthodox cytoplasmic ABC/ATPase required for [Fe-S] biogenesis under oxidative stress,” EMBO Journal, vol. 22, no. 3, pp. 427–437, 2003.
[128]
A. L. Menon, F. L. Poole II, A. Cvetkovic et al., “Novel multiprotein complexes identified in the hyperthermophilic archaeon Pyrococcus furiosus by non-denaturing fractionation of the native proteome,” Molecular & Cellular Proteomics, vol. 8, no. 4, pp. 735–751, 2009.
[129]
V. Gupta, M. Sendra, S. G. Naik 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,” Journal of the American Chemical Society, vol. 131, no. 17, pp. 6149–6153, 2009.
[130]
J. M. Boyd, A. J. Pierik, D. J. A. Netz, R. Lill, and D. M. Downs, “Bacterial ApbC can bind and effectively transfer iron-sulfur clusters,” Biochemistry, vol. 47, no. 31, pp. 8195–8202, 2008.
[131]
J. M. Boyd, J. L. Sondelski, and D. M. Downs, “Bacterial apbC protein has two biochemical activities that are required for in vivo function,” Journal of Biological Chemistry, vol. 284, no. 1, pp. 110–118, 2009.
[132]
H. Kohbushi, Y. Nakai, S. Kikuchi, T. Yabe, H. Hori, and M. Nakai, “Arabidopsis cytosolic Nbp35 homodimer can assemble both [2Fe-2S] and [4Fe-4S] clusters in two distinct domains,” Biochemical and Biophysical Research Communications, vol. 378, no. 4, pp. 810–815, 2009.
[133]
J. M. Boyd, R. M. Drevland, D. M. Downs, and D. E. Graham, “Archaeal ApbC/Nbp35 homologs function as iron-sulfur cluster carrier proteins,” Journal of Bacteriology, vol. 191, no. 5, pp. 1490–1497, 2009.
[134]
E. Skovran and D. M. Downs, “Lack of the ApbC or ApbE protein results in a defect in Fe-S cluster metabolism in Salmonella enterica serovar typhimurium,” Journal of Bacteriology, vol. 185, no. 1, pp. 98–106, 2003.
[135]
B. Zafrilla, R.M. Martínez-Espinosa, J. Esclapez, F. Pérez-Pomares, and M. J. Bonete, “SufS protein from Haloferax volcanii involved in Fe-S cluster assembly in haloarchaea,” Biochimica et Biophysica Acta, vol. 1804, no. 7, pp. 1476–1482, 2010.
[136]
Y. Kawarabayasi, Y. Hino, H. Horikawa et al., “Complete genome sequence of an aerobic hyper-thermophilic crenarchaeon, Aeropyrum pernix K1,” DNA Research, vol. 6, no. 2, pp. 83–101, 1999.
[137]
N. J. Cosper, D. M. Eby, A. Kounosu et al., “Redox-dependent structural changes in archaeal and bacterial Rieske-type [2Fe-2S] clusters,” Protein Science, vol. 11, no. 12, pp. 2969–2973, 2002.
[138]
A. Kounosu, Z. Li, N. J. Cosper et al., “Engineering a three-cysteine, one-histidine ligand environment into a new hyperthermophilic archaeal rieske-type [2Fe-2S] ferredoxin from Sulfolobus solfataricus,” Journal of Biological Chemistry, vol. 279, no. 13, pp. 12519–12528, 2004.
[139]
T. Iwasaki, A. Kounosu, D. R. J. Kolling et al., “Characterization of the pH-dependent resonance Raman transitions of archaeal and bacterial Rieske [2Fe-2S] proteins,” Journal of the American Chemical Society, vol. 126, no. 15, pp. 4788–4789, 2004.
[140]
S. A. Dikanov, A. A. Shubin, A. Kounosu, T. Iwasaki, and R. I. Samoilova, “A comparative, two-dimensional 14N ESEEM characterization of reduced [2Fe-2S] clusters in hyperthermophilic archaeal high- and low-potential Rieske-type proteins,” Journal of Biological Inorganic Chemistry, vol. 9, no. 6, pp. 753–767, 2004.
[141]
T. Iwasaki, R. I. Samoilova, A. Kounosu, and S. A. Dikanov, “Two-dimensional pulsed electron spin resonance characterization of -labeled archaeal Rieske-type ferredoxin,” FEBS Letters, vol. 583, no. 21, pp. 3467–3472, 2009.
[142]
A. Kounosu, K. Hasegawa, T. Iwasaki, and T. Kumasaka, “Crystallization and preliminary X-ray diffraction studies of hyperthermophilic archaeal Rieske-type ferredoxin (ARF) from Sulfolobus solfataricus P1,” Acta Crystallographica F, vol. 66, no. 7, pp. 842–845, 2010.
[143]
J. R. Mason and R. Cammack, “The electron-transport proteins of hydroxylating bacterial dioxygenases,” Annual Review of Microbiology, vol. 46, pp. 277–305, 1992.
[144]
T. A. Link, “The structures of Rieske and Rieske-type proteins,” Advances in Inorganic Chemistry, vol. 47, pp. 83–157, 1999.
[145]
S. Iwata, M. Saynovits, T. A. Link, and H. Michel, “Structure of a water soluble fragment of the ‘Rieske' iron-sulfur protein of the bovine heart mitochondrial cytochrome bc1 complex determined by MAD phasing at 1.5？？ resolution,” Structure, vol. 4, no. 5, pp. 567–579, 1996.
[146]
C. J. Carrell, H. Zhang, W. A. Cramer, and J. L. Smith, “Biological identity and diversity in photosynthesis and respiration: structure of the lumen-side domain of the chloroplast Rieske protein,” Structure, vol. 5, no. 12, pp. 1613–1625, 1997.
[147]
B. Kauppi, K. Lee, E. Carredano et al., “Structure of an aromatic-ring-hydroxylating dioxygenasenaphthalene 1,2-dioxygenase,” Structure, vol. 6, no. 5, pp. 571–586, 1998.
[148]
C. L. Colbert, M. M.-J. Couture, L. D. Eltis, and J. T. Bolin, “A cluster exposed: structure of the rieske ferredoxin from biphenyl dioxygenase and the redox properties of Rieske Fe-S proteins,” Structure, vol. 8, no. 12, pp. 1267–1278, 2000.
[149]
H. B？nisch, C. L. Schmidt, G. Sch？fer, and R. Ladenstein, “The structure of the soluble domain of an archaeal Rieske iron-sulfur protein at 1.1 ？ resolution,” Journal of Molecular Biology, vol. 319, no. 3, pp. 791–805, 2002.
[150]
L. M. Hunsicker-Wang, A. Heine, Y. Chen et al., “High-resolution structure of the soluble, respiratory-type Rieske protein from Thermus thermophilus: analysis and comparison,” Biochemistry, vol. 42, no. 24, pp. 7303–7317, 2003.
[151]
D. J. Kolling, J. S. Brunzelle, S. Lhee, A. R. Crofts, and S. K. Nair, “Atomic resolution structures of Rieske iron-sulfur protein: role of hydrogen bonds in tuning the redox potential of iron-sulfur clusters,” Structure, vol. 15, no. 1, pp. 29–38, 2007.
[152]
M. W. Day, B. T. Hsu, L. Joshua-Tor et al., “X-ray crystal structures of the oxidized and reduced forms of the rubredoxin from the marine hyperthermophilic archaebacterium Pyrococcus furiosus,” Protein Science, vol. 1, no. 11, pp. 1494–1507, 1992.
[153]
T. Iwasaki, A. Kounosu, Y. Tao et al., “Rational design of a mononuclear metal site into the archaeal Rieske-type protein scaffold,” Journal of Biological Chemistry, vol. 280, no. 10, pp. 9129–9134, 2005.
[154]
J. Meyer, J. Gagnon, J. Gaillard et al., “Assembly of a cluster in a molecular variant of Clostridium pasteurianum rubredoxin,” Biochemistry, vol. 36, no. 43, pp. 13374–13380, 1997.
[155]
P. A. Frey, A. D. Hegeman, and F. J. Ruzicka, “The radical SAM superfamily,” Critical Reviews in Biochemistry and Molecular Biology, vol. 43, no. 1, pp. 63–88, 2008.
[156]
K. S. Duschene, S. E. Veneziano, S. C. Silver, and J. B. Broderick, “Control of radical chemistry in the AdoMet radical enzymes,” Current Opinion in Chemical Biology, vol. 13, no. 1, pp. 74–83, 2009.
[157]
H. Irving and R. J. P. Williams, “The stability of transition-metal complexes,” Journal of the Chemical Society, pp. 3192–3210, 1953.
