Evidence for a Rieske‐type FeS center in the thermoacidophilic archaebacterium <i>Sulfolobus acidocaldarius</i>

Anemüller, Stefan; Schmidt, Christian; Schäfer, Günter; Teixeira, Miguel

doi:10.1016/0014-5793(93)81328-w

Cited by 31 publications

(20 citation statements)

References 13 publications

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“…These data clearly show the presence of a respiratory Rieske FeS center in the membranes of Sulfolobus sp. strain 7, as recently reported also for S. acidocaldarius DSM 639 (g x,y,z ϭ 1.725, 1.890, 2.031; g av ϭ 1.88 [1]), which appears to be a constituent of the SoxCM oxidase complex (26). It thus seems plausible that the membranebound Rieske center newly detected in this study may also be a constituent of the terminal oxidase complex of Sulfolobus sp.…”

supporting

confidence: 87%

Sulredoxin: a novel iron-sulfur protein of the thermoacidophilic archaeon Sulfolobus sp. strain 7 with a Rieske-type [2Fe-2S] center

et al. 1995

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A novel pink [2Fe-2S] protein has been purified from the cytosol fraction of the thermoacidophilic archaeon Sulfolobus sp. strain 7 (originally named Sulfolobus acidocaldarius 7) and called ''sulredoxin. ' The plant-type [2Fe-2S] ferredoxins have midpoint redox potentials ranging from Ϫ230 to Ϫ450 mV (35) and serve as low-potential, single-electron carriers from the photosystem I reaction center to various ferredoxin-dependent oxidoreductases in cyanobacteria and chloroplasts of plants (21,35). Their redox centers, namely, the plant ferredoxin-type [2Fe-2S] clusters, coordinate to the proteins by four sulfide ligands contributed by four cysteine residues and give a low-temperature electron paramagnetic resonance (EPR) signal only in the reduced state, with an average g-factor (g av ) of around 1.96 (28, 29). Essentially similar ferredoxins have also been isolated from the mammalian adrenal mitochondria (adrenodoxin), purple bacteria, and the extremely halophilic archaea, which participate in the cytochrome P-450-dependent steroid-hydroxylating system, nitrogen fixation system, and coenzyme A-acylating 2-oxoacid-oxidizing system, respectively (35).Another class of the [2Fe-2S] cluster-containing FeS proteins comprises the respiratory Rieske proteins, which are an important constituent of the cytochrome bc (bc 1 /b 6 f) complex (respiratory complex III) of the aerobic respiratory and photosynthetic systems (28, 34). They have relatively high midpoint redox potentials ranging from Ϫ150 to ϩ350 mV and elicit a characteristic EPR signal with an unusually low g av of ϳ1.91 in the reduced state, as well as red-shifted visible spectra in the oxidized state. The [2Fe-2S] clusters of several ferredoxins involved in the bacterial dioxygenase systems also have spectral properties more similar to those of the Rieske-type FeS proteins than those of the plant-type ferredoxins (28). These spectral properties are due most likely to the asymmetrical ligand environments; extensive analyses of the Riesketype [2Fe-2S] clusters of Thermus thermophilus respiratory Rieske protein (8) and Pseudomonas cepacia phthalate dioxygenase (3) suggested that one iron atom of the FeS cluster coordinated to the protein by two sulfide ligands contributed by two cysteine residues, while the other coordinated by two ␦-nitrogens of the imidazole rings contributed by two histidine residues (5, 9, 13, 23).Sulfolobus sp. strain 7 (originally named Sulfolobus acidocaldarius 7) is a typical aerobic and thermoacidophilic archaeon that grows optimally at pH 2.5 to 3 and at 75 to 80ЊC (36). Chemoheterotrophically grown cells acquire biological energy by aerobic respiration rather than simple fermentation (22,36), and the aerobic respiratory chain, which is coupled to the oxidative tricarboxylic acid cycle at the level of succinate (17), contains the unusual membrane-bound terminal cytochrome oxidase system; it consists solely of a-and b-type but no c-type cytochromes (17,36,37), and the presence of a respiratory Rieske FeS protein or its analog has not been r...

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supporting

confidence: 87%

Sulredoxin: a novel iron-sulfur protein of the thermoacidophilic archaeon Sulfolobus sp. strain 7 with a Rieske-type [2Fe-2S] center

et al. 1995

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“…Redox Midpoint Potentials-g av ϭ 1.91 2Fe2S clusters were found with redox midpoint potentials at (a) ϩ400 mV in plasma membranes of the archaeon Sulfolobus acidocaldarius (Anemü ller et al, 1993(Anemü ller et al, , 1994, (b) at around ϩ300 mV in cytochrome bc 1 and b 6 f complexes with ubiquinonol and plastoquinol as electron donors to the complex (Ding et al, 1992;Nitschke et al, 1992), (c) at around ϩ130 mV in the menaquinol-oxidizing cytochrome bc complexes Riedel et al 1993), and (d) at around Ϫ100 mV in bacterial oxygenases (Mason and Cammack, 1992;Rosche et al, 1995b). The class of these 2Fe2S centers thus covers a range of more than 500 mV.…”

Section: The G Av ϭ 191 2fe2s Centers From Bacterial Oxygenases and mentioning

confidence: 99%

EPR, Electron Spin Echo Envelope Modulation, and Electron Nuclear Double Resonance Studies of the 2Fe2S Centers of the 2-Halobenzoate 1,2-Dioxygenase from Burkholderia (Pseudomonas) cepacia 2CBS

Riedel

Fetzner

Rampp

et al. 1995

Journal of Biological Chemistry

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The 2-halobenzoate 1,2-dioxygenase from Burkholderia (Pseudomonas) cepacia 2CBS (Fetzner, S., Mü ller, R., and Lingens, F. (1992) J. Bacteriol. 174, 279 -290) contains both a ferredoxin-type and a Rieske-type 2Fe2S center. These two significantly different 2Fe2S clusters were characterized with respect to their EPR spectra, electrochemical properties (Rieske-type cluster with g z ‫؍‬ 2.025, g y ‫؍‬ 1.91, g x ‫؍‬ 1.79, g av ‫؍‬ 1.91, E m ‫؍‬ ؊125 ؎ 10 mV; ferredoxin-type center with g z ‫؍‬ 2.05, g y ‫؍‬ 1.96, g x ‫؍‬ 1.89, g av ‫؍‬ 1.97, E m ‫؍‬ ؊200 ؎ 10 mV) and pH dependence thereof. X band electron spin echo envelope modulation and electron nuclear double resonance spectroscopy was applied to study the interaction of the Rieske-type center of the 2-halobenzoate 1,2-dioxygenase with 2Fe2S clusters are usually divided into two distinct groups on the basis of their EPR spectra. The ferredoxin-type 2Fe2S centers are characterized by an average g-value of g av ϭ 1.96, whereas the so-called Rieske-type 2Fe2S centers show a pronounced g-factor anisotropy with g av ϭ 1.91.For a long time, the membership in either of the two classes was considered to be correlated with significantly different redox midpoint potentials, i.e. with an E m 1 Ͻ Ϫ400 mV for the ferredoxins and an E m Ͼ ϩ260 mV for the Rieske centers of the cytochrome bc complexes, the enzymes in which such a 2Fe2S center had been discovered (Rieske et al., 1964). The midpoint potential of the Rieske centers was supposed to arise from a different coordination of the cluster compared to ferredoxintype centers.To date, crystal structures of six 2Fe2S ferredoxins are available (Tsukihara et al., 1981;Tsutsui et al., 1983;Rypniewski et al., 1991;Sussman et al., 1989;Correll et al., 1992;Jacobson et al., 1993) showing that the iron atoms are coordinated by four cysteines and are bridged by a pair of acid-labile sulfur atoms. For the Rieske centers, no x-ray structure has been solved yet. The model of the cluster suggesting a coordination via two cysteines and two histidines is supported by 15 N Q band EN-DOR experiments on the terminal oxygenase of the phthalate dioxygenase from Pseudomonas cepacia (Gurbiel et al., 1989). Resonances in the frequency range below 10 MHz were attributed to two slightly inequivalent nitrogen nuclei from histidines interacting with one of the iron ions. The hyperfine coupling constants were claimed to be too high for only dipolar interaction postulating a covalent binding between the iron atom and the histidines. Further ENDOR, ESEEM, and extended x-ray absorption fine structure studies as well as results obtained from site-specific mutagenesis were interpreted in favor of this model (Gurbiel et al., 1991;Britt et al., 1991;Shergill and Cammack, 1994a;Powers et al., 1989;Tsang et al., 1989;Davidson et al., 1992).During recent years, the discovery of several "odd" systems weakened the clearcut E m distinction between the g av ϭ 1.91 and g av ϭ 1.96 clusters. (a) 2Fe2S clusters contained in cytochrome bc complexes involved in oxidation ...

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“…More recently, we found that the b-type cytochrome is in the upstream of the a-type cytochromes of the archaeal respiratory chain, and its partially-denatured form to be copurified with the cytochrome a 583 -aa 3 subcomplex, which, however, did not retain any caldariellaquinol oxidase activity. 2 In addition, the complexity of the archaeal aerobic respiratory chain is further empathized by the recent findings that the Sulfolobus membranes in fact contain the respiratory Rieske-type FeS clusters (37,38).…”

mentioning

confidence: 99%

Resolution of the Aerobic Respiratory System of the Thermoacidophilic Archaeon, Sulfolobus sp. Strain 7:

Iwasaki¹,

Matsuura

Oshima³

1995

Journal of Biological Chemistry

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The aerobic respiratory system of the thermoacidophilic archaeon, Sulfolobus sp. strain 7, is unusual in that it consists of only a-and b-type cytochromes but no c-type cytochromes. In previous studies, a novel cytochrome oxidase a 583 -aa 3 subcomplex has been purified, which showed a ferrocytochrome c oxidase but no caldariellaquinol oxidase activity (Wakagi, T., Yamauchi, T., Oshima, T., Mü ller, M., Azzi, A., and Sone, N. (1989) Biochem. Biophys. Res. Commun. 165, 1110 -1114). We show here that the cytochrome subcomplex could be copurified with a non-CO-reactive cytochrome b 562 as a novel terminal oxidase "supercomplex," which also contained a Rieske-type FeS cluster at g y ‫؍‬ 1.89. It contained one copper and all four heme centers detectable in the archaeal membranes by the low temperature spectrophotometry and the potentiometric titration: cytochromes b 562 (؉146 mV), a 583 (؉270 mV), and aa 3 (؉117 and ؉325 mV). The presence of one copper atom indicates that it contains the conventional heme a 3 -Cu B binuclear center for reducing molecular oxygen. In conjunction with the presence of a Rieske-type FeS center, inhibitor studies suggest that the terminal oxidase segment of the respiratory chain of Sulfolobus sp. strain 7 is a functional fusion of respiratory complexes III and IV, where cytochrome b 562 and the Rieske-type FeS center probably play a central role in the oxidation of caldariellaquinol. This archaeal terminal oxidase supercomplex reconstitutes the in vitro succinate oxidase respiratory chain for the first time together with caldariellaquinone and the purified cognate succinate:caldariellaquinone oxidoreductase complex. The reconstitution system requires caldariellaquinone for the activity, and is highly sensitive to cyanide and 2-heptyl-4-hydroxy-quinoline-N-oxide. These results are also discussed in terms of the evolutionary considerations.

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Evidence for a Rieske‐type FeS center in the thermoacidophilic archaebacterium Sulfolobus acidocaldarius

Cited by 31 publications

References 13 publications

Sulredoxin: a novel iron-sulfur protein of the thermoacidophilic archaeon Sulfolobus sp. strain 7 with a Rieske-type [2Fe-2S] center

Sulredoxin: a novel iron-sulfur protein of the thermoacidophilic archaeon Sulfolobus sp. strain 7 with a Rieske-type [2Fe-2S] center

EPR, Electron Spin Echo Envelope Modulation, and Electron Nuclear Double Resonance Studies of the 2Fe2S Centers of the 2-Halobenzoate 1,2-Dioxygenase from Burkholderia (Pseudomonas) cepacia 2CBS

Resolution of the Aerobic Respiratory System of the Thermoacidophilic Archaeon, Sulfolobus sp. Strain 7:

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