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• W2008035992 abstract "“Sulredoxin” of Sulfolobus sp. strain 7 is an archaeal soluble Rieske-type [2Fe-2S] protein and was initially characterized by several spectroscopic techniques (Iwasaki, T., Isogai, T., Iizuka, T., and Oshima, T. (1995) J. Bacteriol. 177, 2576-2582). It appears to have tightly linked ionization affecting the redox properties of the protein, which is characteristic of the Rieske FeS proteins found as part of the respiratory chain. Sulredoxin had an Em(low pH) value of +188 ± 9 mV, and the slope of pH dependence of the midpoint redox potential indicated two ionization equilibria in the oxidized form with pKa(ox1) of 6.23 ± 0.22 and pKa(ox2) of 8.57 ± 0.20. The absorption, CD, and resonance Raman spectra of oxidized sulredoxin are consistent with the proposed St2FeSb2Fe[N(His)]t2 core structure, and deprotonation of one of the two putative coordinated histidine imidazoles, having the pKa(ox2) of 8.57 ± 0.20, causes a decrease in the midpoint redox potential, the change in the optical and CD spectra, and the appearance of a new Raman transition at 278 cm−1, without major structural rearrangement of the [2Fe-2S] cluster as well as the overall protein conformation. The redox-linked ionization of sulredoxin is also contributed by local changes involving another ionizable group having the pKa(ox1) of 6.23 ± 0.22, which is probably attributed to a certain positively charged amino acid residue that may not be a ligand by itself but located very close to the cluster. We suggest that sulredoxin provides a new tractable model of the membrane-bound homologue of the respiratory chain, the Rieske FeS proteins of the cytochrome bc1-b6f complexes. “Sulredoxin” of Sulfolobus sp. strain 7 is an archaeal soluble Rieske-type [2Fe-2S] protein and was initially characterized by several spectroscopic techniques (Iwasaki, T., Isogai, T., Iizuka, T., and Oshima, T. (1995) J. Bacteriol. 177, 2576-2582). It appears to have tightly linked ionization affecting the redox properties of the protein, which is characteristic of the Rieske FeS proteins found as part of the respiratory chain. Sulredoxin had an Em(low pH) value of +188 ± 9 mV, and the slope of pH dependence of the midpoint redox potential indicated two ionization equilibria in the oxidized form with pKa(ox1) of 6.23 ± 0.22 and pKa(ox2) of 8.57 ± 0.20. The absorption, CD, and resonance Raman spectra of oxidized sulredoxin are consistent with the proposed St2FeSb2Fe[N(His)]t2 core structure, and deprotonation of one of the two putative coordinated histidine imidazoles, having the pKa(ox2) of 8.57 ± 0.20, causes a decrease in the midpoint redox potential, the change in the optical and CD spectra, and the appearance of a new Raman transition at 278 cm−1, without major structural rearrangement of the [2Fe-2S] cluster as well as the overall protein conformation. The redox-linked ionization of sulredoxin is also contributed by local changes involving another ionizable group having the pKa(ox1) of 6.23 ± 0.22, which is probably attributed to a certain positively charged amino acid residue that may not be a ligand by itself but located very close to the cluster. We suggest that sulredoxin provides a new tractable model of the membrane-bound homologue of the respiratory chain, the Rieske FeS proteins of the cytochrome bc1-b6f complexes. INTRODUCTIONThe respiratory Rieske iron-sulfur (FeS) protein is an intrinsic constituent of cytochrome bc1-b6f complexes from mitochondria, chloroplasts, and certain bacteria found as part of the respiratory chain (1Trumpower B.L. Biochim. Biophys. Acta. 1981; 639: 129-155Crossref PubMed Scopus (148) Google Scholar, 2Mason J.R. Cammack R. Annu. Rev. Microbiol. 1992; 46: 277-305Crossref PubMed Scopus (375) Google Scholar, 3Trumpower B.L. Microbiol. Rev. 1990; 54: 101-129Crossref PubMed Google Scholar, 4Fee J.A. Kuila D. Mather M.W. Yoshida T. Biochim. Biophys. Acta. 1986; 853: 153-185Crossref PubMed Scopus (70) Google Scholar). Although the Rieske-type FeS cluster consists of two Fe and two S2−, it has a high midpoint redox potential and shows characteristic optical and EPR spectra that are distinctively different from those of the conventional plant-type ferredoxins in which the [2Fe-2S] cluster is bound to four sulfide ligands contributed by four cysteine residues and two bridging sulfide ions. The [2Fe-2S] clusters of several ferredoxins involved in the bacterial dioxygenase systems also have spectral properties analogous to those of the respiratory Rieske FeS proteins (2Mason J.R. Cammack R. Annu. Rev. Microbiol. 1992; 46: 277-305Crossref PubMed Scopus (375) Google Scholar). These spectral properties have been interpreted by the asymmetric ligand environments around the [2Fe-2S] cluster, such that one of its iron atoms is coordinated to the protein by two sulfide ligands contributed by two cysteine residues, while the other is coordinated by two nitrogens contributed by two putative histidine residues (4Fee J.A. Kuila D. Mather M.W. Yoshida T. Biochim. Biophys. Acta. 1986; 853: 153-185Crossref PubMed Scopus (70) Google Scholar, 5Fee J.A. Findling K.L. Yoshida T. Hille R. Tarr G.E. Hearshen D.O. Dunham W.R. Day E.P. Kent T.A. Münck E. J. Biol. Chem. 1984; 259: 124-133Abstract Full Text PDF PubMed Google Scholar, 6Cline J.F. Hoffman B.M. Mims W.B. LaHaie E. Ballou D.P. Fee J.A. J. Biol. Chem. 1985; 260: 3251-3254Abstract Full Text PDF PubMed Google Scholar, 7Gurbiel R.J. Batie C.J. Sivaraja M. True A.E. Fee J.A. Hoffman B.M. Ballou D.P. Biochemistry. 1989; 28: 4861-4871Crossref PubMed Scopus (182) Google Scholar, 8Kuila D. Fee J.A. Schoonover J.R. Woodruff W.H. Batie C.J. Ballou D.P. J. Am. Chem. Soc. 1987; 109: 1559-1561Crossref Scopus (42) Google Scholar, 9Britt R.D. Sauer K. Klein M.P. Knaff D.B. Kriauciunas A. Yu C.-A. Yu L. Malkin R. Biochemistry. 1991; 30: 1892-1901Crossref PubMed Scopus (106) Google Scholar, 10Kuila D. Schoonover J.R. Dyer R.B. Batie C.J. Ballou D.P. Fee J.A. Woodruff W.H. Biochim. Biophys. Acta. 1992; 1140: 175-183Crossref PubMed Scopus (68) Google Scholar, 11Gurbiel R.J. Ohnishi T. Robertson D.E. Daldal F. Hoffman B.M. Biochemistry. 1991; 30: 11579-11584Crossref PubMed Scopus (86) Google Scholar, 12Davidson E. Ohnishi T. Atta-asafo-Adjei E. Daldal F. Biochemistry. 1992; 31: 3342-3351Crossref PubMed Scopus (109) Google Scholar).The midpoint redox potentials of the mitochondrial and Rhodobacter sphaeroides Rieske FeS centers (+280 and +285 mV at pH 7.0, respectively) are independent of pH between 6 and 8 and decrease ∼60 mV/pH above pH 8 (13Prince R.C. Dutton P.L. FEBS Lett. 1976; 65: 117-119Crossref PubMed Scopus (80) Google Scholar). A similar redox-linked ionization effect has been reported for Thermus thermophilus Rieske FeS protein (+140 mV at pH 7.0) (5Fee J.A. Findling K.L. Yoshida T. Hille R. Tarr G.E. Hearshen D.O. Dunham W.R. Day E.P. Kent T.A. Münck E. J. Biol. Chem. 1984; 259: 124-133Abstract Full Text PDF PubMed Google Scholar, 14Kuila D. Fee J.A. J. Biol. Chem. 1986; 261: 2768-2771Abstract Full Text PDF PubMed Google Scholar) and a Rieske FeS cluster in Bacillus sp. PS3 (+165 mV at pH 7.0) (15Liebl U. Pezennec S. Riedel A. Kellner E. Nitschke W. J. Biol. Chem. 1992; 267: 14068-14072Abstract Full Text PDF PubMed Google Scholar), both of which had the pKa(ox) of protonic equilibrium of ∼8. The midpoint redox potential of the Rieske FeS center in a green sulfur bacterium Chlorobium limicola (+160 mV at pH 7.0) decreases ∼60 mV/pH from pH 6.8 to 8.4 (16Knaff D.B. Malkin R. Biochim. Biophys. Acta. 1976; 430: 244-252Crossref PubMed Scopus (62) Google Scholar), implying a significantly lower pKa in this particular case. On the other hand, the midpoint redox potentials of the Rieske-type [2Fe-2S] proteins involved in the bacterial dioxygenase systems are invariant, at least up to pH 10 (2Mason J.R. Cammack R. Annu. Rev. Microbiol. 1992; 46: 277-305Crossref PubMed Scopus (375) Google Scholar, 4Fee J.A. Kuila D. Mather M.W. Yoshida T. Biochim. Biophys. Acta. 1986; 853: 153-185Crossref PubMed Scopus (70) Google Scholar, 14Kuila D. Fee J.A. J. Biol. Chem. 1986; 261: 2768-2771Abstract Full Text PDF PubMed Google Scholar). Thus, the respiratory Rieske FeS proteins involved in the cytochrome bc1-b6f complexes of the aerobic respiratory and photosynthetic systems have an “redox-linked ionization,” usually with the pKa(ox) of the protonic equilibrium of ∼8.Sulfolobus sp. strain 7 (originally named Sulfolobus acidocaldarius strain 7) grows optimally at 80°C and at pH 2.5-3 and acquires biological energy by aerobic respiration rather than by simple fermentation, at least under the chemoheterotrophic growth conditions (17Wakagi T. Oshima T. Syst. Appl. Microbiol. 1986; 7: 342-345Crossref Scopus (31) Google Scholar, 18Konishi J. Wakagi T. Oshima T. Yoshida M. J. Biochem. (Tokyo). 1987; 102: 1379-1387Crossref PubMed Scopus (47) Google Scholar, 19Iwasaki T. Wakagi T. Isogai Y. Tanaka K. Iizuka T. Oshima T. J. Biol. Chem. 1994; 269: 29444-29450Abstract Full Text PDF PubMed Google Scholar, 20Iwasaki T. Wakagi T. Oshima T. J. Biol. Chem. 1995; 270: 17878-17883Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar, 21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar, 22Iwasaki T. Matsuura K. Oshima T. J. Biol. Chem. 1995; 270: 30881-30892Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, 23Iwasaki T. Wakagi T. Isogai Y. Iizuka T. Oshima T. J. Biol. Chem. 1995; 270: 30893-30901Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar, 24Iwasaki T. Wakagi T. Oshima T. J. Biol. Chem. 1995; 270: 30902-30908Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). Since the archaeon contains only a- and b-type cytochromes but no c-types (17Wakagi T. Oshima T. Syst. Appl. Microbiol. 1986; 7: 342-345Crossref Scopus (31) Google Scholar, 22Iwasaki T. Matsuura K. Oshima T. J. Biol. Chem. 1995; 270: 30881-30892Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, 23Iwasaki T. Wakagi T. Isogai Y. Iizuka T. Oshima T. J. Biol. Chem. 1995; 270: 30893-30901Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar), it was unexpected that two different species of the thermoacidophilic archaea Sulfolobus contained the Rieske-type [2Fe-2S] centers (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar, 22Iwasaki T. Matsuura K. Oshima T. J. Biol. Chem. 1995; 270: 30881-30892Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, 25Anemüller S. Schmidt C.L. Schäfer G. Teixeira M. FEBS Lett. 1993; 318: 61-64Crossref PubMed Scopus (27) Google Scholar, 26Lübben M. Arnaud S. Castresana J. Warne A. Albracht S.P.J. Saraste M. Eur. J. Biochem. 1994; 224: 151-159Crossref PubMed Scopus (84) Google Scholar, 27Schmidt C.L. Anemüller S. Teixeira M. Schäfer G. FEBS Lett. 1995; 359: 239-243Crossref PubMed Scopus (24) Google Scholar). In the case of Sulfolobus sp. strain 7, at least two different Rieske-type FeS centers have been detected in the membranes; one exhibiting the gy = 1.89 EPR signal is a constituent of the archaeal respiratory terminal oxidase supercomplex, while the other exhibiting the gy = 1.91 signal is of unknown function (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar, 22Iwasaki T. Matsuura K. Oshima T. J. Biol. Chem. 1995; 270: 30881-30892Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar). The latter center is only loosely attached to the membrane and is readily removed by washing the membrane in the presence of cholate, 1T. Iwasaki, and T. Oshima, unpublished results. as in the cases of the cognate weakly associated membrane proteins such as NADH dehydrogenase (28Wakao H. Wakagi T. Oshima T. J. Biochem. (Tokyo). 1987; 102: 255-262Crossref PubMed Scopus (48) Google Scholar) and V1-ATPase (18Konishi J. Wakagi T. Oshima T. Yoshida M. J. Biochem. (Tokyo). 1987; 102: 1379-1387Crossref PubMed Scopus (47) Google Scholar, 29Denda K. Konishi J. Hajiro K. Oshima T. Date T. Yoshida M. J. Biol. Chem. 1990; 265: 21509-21513Abstract Full Text PDF PubMed Google Scholar). In addition to these membrane-bound FeS centers, the archaeal soluble fraction exhibits another gy = 1.91 EPR signal, which is attributed to a soluble purple FeS protein, tentatively called “sulredoxin.” The initial characterization of sulredoxin by the absorption, CD, and EPR spectroscopic techniques, in conjunction with chemical analysis, suggested the presence of a single Rieske-type [2Fe-2S] cluster in sulredoxin with an average g-factor of 1.90 (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar). The size of sulredoxin determined by mass spectroscopy (12,155 Da (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar)) is similar to those of the [2Fe-2S] proteins involved in the bacterial dioxygenase systems (12 kDa (2Mason J.R. Cammack R. Annu. Rev. Microbiol. 1992; 46: 277-305Crossref PubMed Scopus (375) Google Scholar)) but much smaller than that of a membrane-bound respiratory Rieske FeS protein of S. acidocaldarius strain DSM 639 (32 kDa (27Schmidt C.L. Anemüller S. Teixeira M. Schäfer G. FEBS Lett. 1995; 359: 239-243Crossref PubMed Scopus (24) Google Scholar)).Although the physiological function of sulredoxin remains unknown, as it did not function as an electron acceptor of the cognate NADH dehydrogenase (28Wakao H. Wakagi T. Oshima T. J. Biochem. (Tokyo). 1987; 102: 255-262Crossref PubMed Scopus (48) Google Scholar), or the cognate ferredoxin-dependent enzymes such as 2-oxoacid:ferredoxin oxidoreductase (30Zhang Q. Iwasaki T. Wakagi T. Oshima T. J. Biochem. (Tokyo). 1996; 120: 587-599Crossref PubMed Scopus (78) Google Scholar) and NADPH:ferredoxin oxidoreductase (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar),1 it can be reproducibly purified in high purity and in the water-soluble and very stable form without detergents, thus being suitable for further physicochemical studies. In addition, because sulredoxin represents the only example of a soluble Rieske-type [2Fe-2S] protein so far purified from an archaeal species, it is of particular interest to investigate its redox property and to compare it with those of the mitochondrial and bacterial Rieske-type FeS proteins. In this paper, we report the potentiometric and the absorption, CD, and low temperature resonance Raman spectral properties of sulredoxin and discuss the nature of the redox-linked ionization of the archaeal Rieske-type [2Fe-2S] protein. We suggest that sulredoxin provides a new tractable model of the membrane-bound Rieske FeS protein found as part of the respiratory chain. INTRODUCTIONThe respiratory Rieske iron-sulfur (FeS) protein is an intrinsic constituent of cytochrome bc1-b6f complexes from mitochondria, chloroplasts, and certain bacteria found as part of the respiratory chain (1Trumpower B.L. Biochim. Biophys. Acta. 1981; 639: 129-155Crossref PubMed Scopus (148) Google Scholar, 2Mason J.R. Cammack R. Annu. Rev. Microbiol. 1992; 46: 277-305Crossref PubMed Scopus (375) Google Scholar, 3Trumpower B.L. Microbiol. Rev. 1990; 54: 101-129Crossref PubMed Google Scholar, 4Fee J.A. Kuila D. Mather M.W. Yoshida T. Biochim. Biophys. Acta. 1986; 853: 153-185Crossref PubMed Scopus (70) Google Scholar). Although the Rieske-type FeS cluster consists of two Fe and two S2−, it has a high midpoint redox potential and shows characteristic optical and EPR spectra that are distinctively different from those of the conventional plant-type ferredoxins in which the [2Fe-2S] cluster is bound to four sulfide ligands contributed by four cysteine residues and two bridging sulfide ions. The [2Fe-2S] clusters of several ferredoxins involved in the bacterial dioxygenase systems also have spectral properties analogous to those of the respiratory Rieske FeS proteins (2Mason J.R. Cammack R. Annu. Rev. Microbiol. 1992; 46: 277-305Crossref PubMed Scopus (375) Google Scholar). These spectral properties have been interpreted by the asymmetric ligand environments around the [2Fe-2S] cluster, such that one of its iron atoms is coordinated to the protein by two sulfide ligands contributed by two cysteine residues, while the other is coordinated by two nitrogens contributed by two putative histidine residues (4Fee J.A. Kuila D. Mather M.W. Yoshida T. Biochim. Biophys. Acta. 1986; 853: 153-185Crossref PubMed Scopus (70) Google Scholar, 5Fee J.A. Findling K.L. Yoshida T. Hille R. Tarr G.E. Hearshen D.O. Dunham W.R. Day E.P. Kent T.A. Münck E. J. Biol. Chem. 1984; 259: 124-133Abstract Full Text PDF PubMed Google Scholar, 6Cline J.F. Hoffman B.M. Mims W.B. LaHaie E. Ballou D.P. Fee J.A. J. Biol. Chem. 1985; 260: 3251-3254Abstract Full Text PDF PubMed Google Scholar, 7Gurbiel R.J. Batie C.J. Sivaraja M. True A.E. Fee J.A. Hoffman B.M. Ballou D.P. Biochemistry. 1989; 28: 4861-4871Crossref PubMed Scopus (182) Google Scholar, 8Kuila D. Fee J.A. Schoonover J.R. Woodruff W.H. Batie C.J. Ballou D.P. J. Am. Chem. Soc. 1987; 109: 1559-1561Crossref Scopus (42) Google Scholar, 9Britt R.D. Sauer K. Klein M.P. Knaff D.B. Kriauciunas A. Yu C.-A. Yu L. Malkin R. Biochemistry. 1991; 30: 1892-1901Crossref PubMed Scopus (106) Google Scholar, 10Kuila D. Schoonover J.R. Dyer R.B. Batie C.J. Ballou D.P. Fee J.A. Woodruff W.H. Biochim. Biophys. Acta. 1992; 1140: 175-183Crossref PubMed Scopus (68) Google Scholar, 11Gurbiel R.J. Ohnishi T. Robertson D.E. Daldal F. Hoffman B.M. Biochemistry. 1991; 30: 11579-11584Crossref PubMed Scopus (86) Google Scholar, 12Davidson E. Ohnishi T. Atta-asafo-Adjei E. Daldal F. Biochemistry. 1992; 31: 3342-3351Crossref PubMed Scopus (109) Google Scholar).The midpoint redox potentials of the mitochondrial and Rhodobacter sphaeroides Rieske FeS centers (+280 and +285 mV at pH 7.0, respectively) are independent of pH between 6 and 8 and decrease ∼60 mV/pH above pH 8 (13Prince R.C. Dutton P.L. FEBS Lett. 1976; 65: 117-119Crossref PubMed Scopus (80) Google Scholar). A similar redox-linked ionization effect has been reported for Thermus thermophilus Rieske FeS protein (+140 mV at pH 7.0) (5Fee J.A. Findling K.L. Yoshida T. Hille R. Tarr G.E. Hearshen D.O. Dunham W.R. Day E.P. Kent T.A. Münck E. J. Biol. Chem. 1984; 259: 124-133Abstract Full Text PDF PubMed Google Scholar, 14Kuila D. Fee J.A. J. Biol. Chem. 1986; 261: 2768-2771Abstract Full Text PDF PubMed Google Scholar) and a Rieske FeS cluster in Bacillus sp. PS3 (+165 mV at pH 7.0) (15Liebl U. Pezennec S. Riedel A. Kellner E. Nitschke W. J. Biol. Chem. 1992; 267: 14068-14072Abstract Full Text PDF PubMed Google Scholar), both of which had the pKa(ox) of protonic equilibrium of ∼8. The midpoint redox potential of the Rieske FeS center in a green sulfur bacterium Chlorobium limicola (+160 mV at pH 7.0) decreases ∼60 mV/pH from pH 6.8 to 8.4 (16Knaff D.B. Malkin R. Biochim. Biophys. Acta. 1976; 430: 244-252Crossref PubMed Scopus (62) Google Scholar), implying a significantly lower pKa in this particular case. On the other hand, the midpoint redox potentials of the Rieske-type [2Fe-2S] proteins involved in the bacterial dioxygenase systems are invariant, at least up to pH 10 (2Mason J.R. Cammack R. Annu. Rev. Microbiol. 1992; 46: 277-305Crossref PubMed Scopus (375) Google Scholar, 4Fee J.A. Kuila D. Mather M.W. Yoshida T. Biochim. Biophys. Acta. 1986; 853: 153-185Crossref PubMed Scopus (70) Google Scholar, 14Kuila D. Fee J.A. J. Biol. Chem. 1986; 261: 2768-2771Abstract Full Text PDF PubMed Google Scholar). Thus, the respiratory Rieske FeS proteins involved in the cytochrome bc1-b6f complexes of the aerobic respiratory and photosynthetic systems have an “redox-linked ionization,” usually with the pKa(ox) of the protonic equilibrium of ∼8.Sulfolobus sp. strain 7 (originally named Sulfolobus acidocaldarius strain 7) grows optimally at 80°C and at pH 2.5-3 and acquires biological energy by aerobic respiration rather than by simple fermentation, at least under the chemoheterotrophic growth conditions (17Wakagi T. Oshima T. Syst. Appl. Microbiol. 1986; 7: 342-345Crossref Scopus (31) Google Scholar, 18Konishi J. Wakagi T. Oshima T. Yoshida M. J. Biochem. (Tokyo). 1987; 102: 1379-1387Crossref PubMed Scopus (47) Google Scholar, 19Iwasaki T. Wakagi T. Isogai Y. Tanaka K. Iizuka T. Oshima T. J. Biol. Chem. 1994; 269: 29444-29450Abstract Full Text PDF PubMed Google Scholar, 20Iwasaki T. Wakagi T. Oshima T. J. Biol. Chem. 1995; 270: 17878-17883Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar, 21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar, 22Iwasaki T. Matsuura K. Oshima T. J. Biol. Chem. 1995; 270: 30881-30892Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, 23Iwasaki T. Wakagi T. Isogai Y. Iizuka T. Oshima T. J. Biol. Chem. 1995; 270: 30893-30901Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar, 24Iwasaki T. Wakagi T. Oshima T. J. Biol. Chem. 1995; 270: 30902-30908Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). Since the archaeon contains only a- and b-type cytochromes but no c-types (17Wakagi T. Oshima T. Syst. Appl. Microbiol. 1986; 7: 342-345Crossref Scopus (31) Google Scholar, 22Iwasaki T. Matsuura K. Oshima T. J. Biol. Chem. 1995; 270: 30881-30892Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, 23Iwasaki T. Wakagi T. Isogai Y. Iizuka T. Oshima T. J. Biol. Chem. 1995; 270: 30893-30901Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar), it was unexpected that two different species of the thermoacidophilic archaea Sulfolobus contained the Rieske-type [2Fe-2S] centers (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar, 22Iwasaki T. Matsuura K. Oshima T. J. Biol. Chem. 1995; 270: 30881-30892Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, 25Anemüller S. Schmidt C.L. Schäfer G. Teixeira M. FEBS Lett. 1993; 318: 61-64Crossref PubMed Scopus (27) Google Scholar, 26Lübben M. Arnaud S. Castresana J. Warne A. Albracht S.P.J. Saraste M. Eur. J. Biochem. 1994; 224: 151-159Crossref PubMed Scopus (84) Google Scholar, 27Schmidt C.L. Anemüller S. Teixeira M. Schäfer G. FEBS Lett. 1995; 359: 239-243Crossref PubMed Scopus (24) Google Scholar). In the case of Sulfolobus sp. strain 7, at least two different Rieske-type FeS centers have been detected in the membranes; one exhibiting the gy = 1.89 EPR signal is a constituent of the archaeal respiratory terminal oxidase supercomplex, while the other exhibiting the gy = 1.91 signal is of unknown function (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar, 22Iwasaki T. Matsuura K. Oshima T. J. Biol. Chem. 1995; 270: 30881-30892Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar). The latter center is only loosely attached to the membrane and is readily removed by washing the membrane in the presence of cholate, 1T. Iwasaki, and T. Oshima, unpublished results. as in the cases of the cognate weakly associated membrane proteins such as NADH dehydrogenase (28Wakao H. Wakagi T. Oshima T. J. Biochem. (Tokyo). 1987; 102: 255-262Crossref PubMed Scopus (48) Google Scholar) and V1-ATPase (18Konishi J. Wakagi T. Oshima T. Yoshida M. J. Biochem. (Tokyo). 1987; 102: 1379-1387Crossref PubMed Scopus (47) Google Scholar, 29Denda K. Konishi J. Hajiro K. Oshima T. Date T. Yoshida M. J. Biol. Chem. 1990; 265: 21509-21513Abstract Full Text PDF PubMed Google Scholar). In addition to these membrane-bound FeS centers, the archaeal soluble fraction exhibits another gy = 1.91 EPR signal, which is attributed to a soluble purple FeS protein, tentatively called “sulredoxin.” The initial characterization of sulredoxin by the absorption, CD, and EPR spectroscopic techniques, in conjunction with chemical analysis, suggested the presence of a single Rieske-type [2Fe-2S] cluster in sulredoxin with an average g-factor of 1.90 (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar). The size of sulredoxin determined by mass spectroscopy (12,155 Da (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar)) is similar to those of the [2Fe-2S] proteins involved in the bacterial dioxygenase systems (12 kDa (2Mason J.R. Cammack R. Annu. Rev. Microbiol. 1992; 46: 277-305Crossref PubMed Scopus (375) Google Scholar)) but much smaller than that of a membrane-bound respiratory Rieske FeS protein of S. acidocaldarius strain DSM 639 (32 kDa (27Schmidt C.L. Anemüller S. Teixeira M. Schäfer G. FEBS Lett. 1995; 359: 239-243Crossref PubMed Scopus (24) Google Scholar)).Although the physiological function of sulredoxin remains unknown, as it did not function as an electron acceptor of the cognate NADH dehydrogenase (28Wakao H. Wakagi T. Oshima T. J. Biochem. (Tokyo). 1987; 102: 255-262Crossref PubMed Scopus (48) Google Scholar), or the cognate ferredoxin-dependent enzymes such as 2-oxoacid:ferredoxin oxidoreductase (30Zhang Q. Iwasaki T. Wakagi T. Oshima T. J. Biochem. (Tokyo). 1996; 120: 587-599Crossref PubMed Scopus (78) Google Scholar) and NADPH:ferredoxin oxidoreductase (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar),1 it can be reproducibly purified in high purity and in the water-soluble and very stable form without detergents, thus being suitable for further physicochemical studies. In addition, because sulredoxin represents the only example of a soluble Rieske-type [2Fe-2S] protein so far purified from an archaeal species, it is of particular interest to investigate its redox property and to compare it with those of the mitochondrial and bacterial Rieske-type FeS proteins. In this paper, we report the potentiometric and the absorption, CD, and low temperature resonance Raman spectral properties of sulredoxin and discuss the nature of the redox-linked ionization of the archaeal Rieske-type [2Fe-2S] protein. We suggest that sulredoxin provides a new tractable model of the membrane-bound Rieske FeS protein found as part of the respiratory chain. The respiratory Rieske iron-sulfur (FeS) protein is an intrinsic constituent of cytochrome bc1-b6f complexes from mitochondria, chloroplasts, and certain bacteria found as part of the respiratory chain (1Trumpower B.L. Biochim. Biophys. Acta. 1981; 639: 129-155Crossref PubMed Scopus (148) Google Scholar, 2Mason J.R. Cammack R. Annu. Rev. Microbiol. 1992; 46: 277-305Crossref PubMed Scopus (375) Google Scholar, 3Trumpower B.L. Microbiol. Rev. 1990; 54: 101-129Crossref PubMed Google Scholar, 4Fee J.A. Kuila D. Mather M.W. Yoshida T. Biochim. Biophys. Acta. 1986; 853: 153-185Crossref PubMed Scopus (70) Google Scholar). Although the Rieske-type FeS cluster consists of two Fe and two S2−, it has a high midpoint redox potential and shows characteristic optical and EPR spectra that are distinctively different from those of the conventional plant-type ferredoxins in which the [2Fe-2S] cluster is bound to four sulfide ligands contributed by four cysteine residues and two bridging sulfide ions. The [2Fe-2S] clusters of several ferredoxins involved in the bacterial dioxygenase systems also have spectral properties analogous to those of the respiratory Rieske FeS proteins (2Mason J.R. Cammack R. Annu. Rev. Microbiol. 1992; 46: 277-305Crossref PubMed Scopus (375) Google Scholar). These spectral properties have been interpreted by the asymmetric ligand environments around the [2Fe-2S] cluster, such that one of its iron atoms is coordinated to the protein by two sulfide ligands contributed by two cysteine residues, while the other is coordinated by two nitrogens contributed by two putative histidine residues (4Fee J.A. Kuila D. Mather M.W. Yoshida T. Biochim. Biophys. Acta. 1986; 853: 153-185Crossref PubMed Scopus (70) Google Scholar, 5Fee J.A. Findling K.L. Yoshida T. Hille R. Tarr G.E. Hearshen D.O. Dunham W.R. Day E.P. Kent T.A. Münck E. J. Biol. Chem. 1984; 259: 124-133Abstract Full Text PDF PubMed Google Scholar, 6Cline J.F. Hoffman B.M. Mims W.B. LaHaie E. Ballou D.P. Fee J.A. J. Biol. Chem. 1985; 260: 3251-3254Abstract Full Text PDF PubMed Google Scholar, 7Gurbiel R.J. Batie C.J. Sivaraja M. True A.E. Fee J.A. Hoffman B.M. Ballou D.P. Biochemistry. 1989; 28: 4861-4871Crossref PubMed Scopus (182) Google Scholar, 8Kuila D. Fee J.A. Schoonover J.R. Woodruff W.H. Batie C.J. Ballou D.P. J. Am. Chem. Soc. 1987; 109: 1559-1561Crossref Scopus (42) Google Scholar, 9Britt R.D. Sauer K. Klein M.P. Knaff D.B. Kriauciunas A. Yu C.-A. Yu L. Malkin R. Biochemistry. 1991; 30: 1892-1901Crossref PubMed Scopus (106) Google Scholar, 10Kuila D. Schoonover J.R. Dyer R.B. Batie C.J. Ballou D.P. Fee J.A. Woodruff W.H. Biochim. Biophys. Acta. 1992; 1140: 175-183Crossref PubMed Scopus (68) Google Scholar, 11Gurbiel R.J. Ohnishi T. Robertson D.E. Daldal F. Hoffman B.M. Biochemistry. 1991; 30: 11579-11584Crossref PubMed Scopus (86) Google Scholar, 12Davidson E. Ohnishi T. Atta-asafo-Adjei E. Daldal F. Biochemistry. 1992; 31: 3342-3351Crossref PubMed Scopus (109) Google Scholar). The midpoint redox potentials of the mitochondrial and Rhodobacter sphaeroides Rieske FeS centers (+280 and +285 mV at pH 7.0, respectively) are independent of pH between 6 and 8 and decrease ∼60 mV/pH above pH 8 (13Prince R.C. Dutton P.L. FEBS Lett. 1976; 65: 117-119Crossref PubMed Scopus (80) Google Scholar). A similar redox-linked ionization effect has been reported for Thermus thermophilus Rieske FeS protein (+140 mV at pH 7.0) (5Fee J.A. Findling K.L. Yoshida T. Hille R. Tarr G.E. Hearshen D.O. Dunham W.R. Day E.P. Kent T.A. Münck E. J. Biol. Chem. 1984; 259: 124-133Abstract Full Text PDF PubMed Google Scholar, 14Kuila D. Fee J.A. J. Biol. Chem. 1986; 261: 2768-2771Abstract Full Text PDF PubMed Google Scholar) and a Rieske FeS cluster in Bacillus sp. PS3 (+165 mV at pH 7.0) (15Liebl U. Pezennec S. Riedel A. Kellner E. Nitschke W. J. Biol. Chem. 1992; 267: 14068-14072Abstract Full Text PDF PubMed Google Scholar), both of which had the pKa(ox) of protonic equilibrium of ∼8. The midpoint redox potential of the Rieske FeS center in a green sulfur bacterium Chlorobium limicola (+160 mV at pH 7.0) decreases ∼60 mV/pH from pH 6.8 to 8.4 (16Knaff D.B. Malkin R. Biochim. Biophys. Acta. 1976; 430: 244-252Crossref PubMed Scopus (62) Google Scholar), implying a significantly lower pKa in this particular case. On the other hand, the midpoint redox potentials of the Rieske-type [2Fe-2S] proteins involved in the bacterial dioxygenase systems are invariant, at least up to pH 10 (2Mason J.R. Cammack R. Annu. Rev. Microbiol. 1992; 46: 277-305Crossref PubMed Scopus (375) Google Scholar, 4Fee J.A. Kuila D. Mather M.W. Yoshida T. Biochim. Biophys. Acta. 1986; 853: 153-185Crossref PubMed Scopus (70) Google Scholar, 14Kuila D. Fee J.A. J. Biol. Chem. 1986; 261: 2768-2771Abstract Full Text PDF PubMed Google Scholar). Thus, the respiratory Rieske FeS proteins involved in the cytochrome bc1-b6f complexes of the aerobic respiratory and photosynthetic systems have an “redox-linked ionization,” usually with the pKa(ox) of the protonic equilibrium of ∼8. Sulfolobus sp. strain 7 (originally named Sulfolobus acidocaldarius strain 7) grows optimally at 80°C and at pH 2.5-3 and acquires biological energy by aerobic respiration rather than by simple fermentation, at least under the chemoheterotrophic growth conditions (17Wakagi T. Oshima T. Syst. Appl. Microbiol. 1986; 7: 342-345Crossref Scopus (31) Google Scholar, 18Konishi J. Wakagi T. Oshima T. Yoshida M. J. Biochem. (Tokyo). 1987; 102: 1379-1387Crossref PubMed Scopus (47) Google Scholar, 19Iwasaki T. Wakagi T. Isogai Y. Tanaka K. Iizuka T. Oshima T. J. Biol. Chem. 1994; 269: 29444-29450Abstract Full Text PDF PubMed Google Scholar, 20Iwasaki T. Wakagi T. Oshima T. J. Biol. Chem. 1995; 270: 17878-17883Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar, 21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar, 22Iwasaki T. Matsuura K. Oshima T. J. Biol. Chem. 1995; 270: 30881-30892Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, 23Iwasaki T. Wakagi T. Isogai Y. Iizuka T. Oshima T. J. Biol. Chem. 1995; 270: 30893-30901Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar, 24Iwasaki T. Wakagi T. Oshima T. J. Biol. Chem. 1995; 270: 30902-30908Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). Since the archaeon contains only a- and b-type cytochromes but no c-types (17Wakagi T. Oshima T. Syst. Appl. Microbiol. 1986; 7: 342-345Crossref Scopus (31) Google Scholar, 22Iwasaki T. Matsuura K. Oshima T. J. Biol. Chem. 1995; 270: 30881-30892Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, 23Iwasaki T. Wakagi T. Isogai Y. Iizuka T. Oshima T. J. Biol. Chem. 1995; 270: 30893-30901Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar), it was unexpected that two different species of the thermoacidophilic archaea Sulfolobus contained the Rieske-type [2Fe-2S] centers (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar, 22Iwasaki T. Matsuura K. Oshima T. J. Biol. Chem. 1995; 270: 30881-30892Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, 25Anemüller S. Schmidt C.L. Schäfer G. Teixeira M. FEBS Lett. 1993; 318: 61-64Crossref PubMed Scopus (27) Google Scholar, 26Lübben M. Arnaud S. Castresana J. Warne A. Albracht S.P.J. Saraste M. Eur. J. Biochem. 1994; 224: 151-159Crossref PubMed Scopus (84) Google Scholar, 27Schmidt C.L. Anemüller S. Teixeira M. Schäfer G. FEBS Lett. 1995; 359: 239-243Crossref PubMed Scopus (24) Google Scholar). In the case of Sulfolobus sp. strain 7, at least two different Rieske-type FeS centers have been detected in the membranes; one exhibiting the gy = 1.89 EPR signal is a constituent of the archaeal respiratory terminal oxidase supercomplex, while the other exhibiting the gy = 1.91 signal is of unknown function (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar, 22Iwasaki T. Matsuura K. Oshima T. J. Biol. Chem. 1995; 270: 30881-30892Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar). The latter center is only loosely attached to the membrane and is readily removed by washing the membrane in the presence of cholate, 1T. Iwasaki, and T. Oshima, unpublished results. as in the cases of the cognate weakly associated membrane proteins such as NADH dehydrogenase (28Wakao H. Wakagi T. Oshima T. J. Biochem. (Tokyo). 1987; 102: 255-262Crossref PubMed Scopus (48) Google Scholar) and V1-ATPase (18Konishi J. Wakagi T. Oshima T. Yoshida M. J. Biochem. (Tokyo). 1987; 102: 1379-1387Crossref PubMed Scopus (47) Google Scholar, 29Denda K. Konishi J. Hajiro K. Oshima T. Date T. Yoshida M. J. Biol. Chem. 1990; 265: 21509-21513Abstract Full Text PDF PubMed Google Scholar). In addition to these membrane-bound FeS centers, the archaeal soluble fraction exhibits another gy = 1.91 EPR signal, which is attributed to a soluble purple FeS protein, tentatively called “sulredoxin.” The initial characterization of sulredoxin by the absorption, CD, and EPR spectroscopic techniques, in conjunction with chemical analysis, suggested the presence of a single Rieske-type [2Fe-2S] cluster in sulredoxin with an average g-factor of 1.90 (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar). The size of sulredoxin determined by mass spectroscopy (12,155 Da (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar)) is similar to those of the [2Fe-2S] proteins involved in the bacterial dioxygenase systems (12 kDa (2Mason J.R. Cammack R. Annu. Rev. Microbiol. 1992; 46: 277-305Crossref PubMed Scopus (375) Google Scholar)) but much smaller than that of a membrane-bound respiratory Rieske FeS protein of S. acidocaldarius strain DSM 639 (32 kDa (27Schmidt C.L. Anemüller S. Teixeira M. Schäfer G. FEBS Lett. 1995; 359: 239-243Crossref PubMed Scopus (24) Google Scholar)). Although the physiological function of sulredoxin remains unknown, as it did not function as an electron acceptor of the cognate NADH dehydrogenase (28Wakao H. Wakagi T. Oshima T. J. Biochem. (Tokyo). 1987; 102: 255-262Crossref PubMed Scopus (48) Google Scholar), or the cognate ferredoxin-dependent enzymes such as 2-oxoacid:ferredoxin oxidoreductase (30Zhang Q. Iwasaki T. Wakagi T. Oshima T. J. Biochem. (Tokyo). 1996; 120: 587-599Crossref PubMed Scopus (78) Google Scholar) and NADPH:ferredoxin oxidoreductase (21Iwasaki T. Isogai T. Iizuka T. Oshima T. J. Bacteriol. 1995; 177: 2576-2582Crossref PubMed Google Scholar),1 it can be reproducibly purified in high purity and in the water-soluble and very stable form without detergents, thus being suitable for further physicochemical studies. In addition, because sulredoxin represents the only example of a soluble Rieske-type [2Fe-2S] protein so far purified from an archaeal species, it is of particular interest to investigate its redox property and to compare it with those of the mitochondrial and bacterial Rieske-type FeS proteins. In this paper, we report the potentiometric and the absorption, CD, and low temperature resonance Raman spectral properties of sulredoxin and discuss the nature of the redox-linked ionization of the archaeal Rieske-type [2Fe-2S] protein. We suggest that sulredoxin provides a new tractable model of the membrane-bound Rieske FeS protein found as part of the respiratory chain. We thank Dr. Y. Fukumori (Tokyo Institute of Technology) for the laboratory facilities, and Drs. K. Matsuura (Tokyo Metropolitan University) and Y. Hayashi (Tokyo Institute of Technology) for helpful technical advice." @default.
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• W2008035992 title "Redox-linked Ionization of Sulredoxin, an Archaeal Rieske-type [2Fe-2S] Protein from Sulfolobus sp. Strain 7" @default.
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