Structural Conservation of the Isolated Zinc Site in Archaeal Zinc-containing Ferredoxins as Revealed by X-ray Absorption Spectroscopic Analysis and Its Evolutionary Implications

Cosper, Nathaniel J.; Stålhandske, Claes; Iwasaki, Hideo; Oshima, Tairo; Scott, Robert A.; Iwasaki, Toshio

doi:10.1074/jbc.274.33.23160

Cited by 10 publications

(16 citation statements)

References 72 publications

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“…1998) C N/O ligands only Carbonic anhydrase (Liljas et al, 1972;Yachandra et al, 1983) Methanosarcina carbonic anhydrase (Alber et al, 1999) Thermolysin (Colman et al, 1972) Superoxide dismutase (Richardson et al, 1975;Blackburn et al, 1983;Murphy et al, 1996) Carboxypeptidase (Rees et al, 1981) Zn-containing ferredoxin (Cosper et al, 1999) Fe(III)±Zn(II) purple acid phosphatase (Priggemeyer et al, 1995;Stra È ter et al, 1995;Klabunde et al, 1996) al., 1998), we observe a major peak at $2.0±2.3 A Ê that shows clear evidence of its mixed character with N and S contributions at 2.0 A Ê and 2.3 A Ê , respectively, and relative intensities that are in agreement with equivalent numbers of N and S ligands when the difference in backscattering amplitude (Feiters et al, 1990) is taken into account. Minor shells at 3 A Ê and 4 A Ê are also observed, which give evidence for imidazole coordination.…”

Section: Type Characteristic Examplesmentioning

confidence: 99%

“…There have been various studies of zinc-®nger-type proteins Summers et al, 1992), and recent examples of Zn XAS studies include carbonic anhydrase (Bracey et al, 1994;Alber et al, 1999), metallothionein (Jiang et al, 1994) and the related neuronal growth inhibitory factor (Bogumil et al, 1998), ferric uptake regulator protein (Fur;Jaquamet et al, 1998), methionine synthase (Gonza Â lez et al, 1996;Peariso et al, 1998;Zhou et al, 1999), other methyl transferases (Gencic et al, 2001;Kru È er et al, 2002), and Zncontaining ferredoxin (Cosper et al, 1999). The XANES (X-ray absorption near-edge structure) part of the spectrum provides information on valence state and coordination geometry, while the extended X-ray absorption ®ne structure (EXAFS) part provides ligand distances and coordination numbers with relatively high (AE0.02 A Ê ) and low (AE20%) accuracy, respectively.…”

Section: Introductionmentioning

confidence: 99%

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X-ray absorption spectroscopic studies of zinc in the N-terminal domain of HIV-2 integrase and model compounds

et al. 2002

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X-ray absorption spectroscopy (XAS), including extended X-ray absorption fine structure (EXAFS) and X-ray absorption near-edge structure (XANES) analysis, has been carried out at the ZnKedge of the N-terminal part of the integrase protein of the human immunodeficiency virus, type 2 (HIV-2), and of some zinc coordination compounds. In the presence of excess β-mercaptoethanol, which was present in the NMR structure elucidation of the protein [Eijkelenboomet al.(1997),Curr. Biol.7, 739–746; (2000),J. Biomol. NMR,18, 119–28], the protein spectrum was nearly identical to that recorded in its absence. Comparison of the XANES of the protein with that of model compounds and literature data permits the conclusion that the Zn ion is four-coordinated. The major shell of the EXAFS provides evidence for a mixed (N or O as well as S) coordination sphere, while the minor shells indicate imidazole coordination. Our approach to the analysis of the EXAFS, including quantification of the imidazole by multiple scattering simulations withEXCURV92, was validated on the model compounds. An important result is that with multiple scattering simulations using restraints on the parameters of the imidazole rings the number of imidazoles and their orientation could be determined. The integrase spectra can be fitted with two sulfur ligands at 2.26 Å (Debye–Waller-type factor 0.009 Å2) and two imidazole ligands with the N atoms at 1.99 Å (Debye–Waller-type factor 0.005 Å2). The XAS-derived geometry is fully consistent with that found in the NMR structure determination and, allowing for the volume contraction due to the temperature difference between the experiments, justifies the restraints applied in the structure calculation (Zn—S and Zn—N distances of 2.3 Å and 2.0 Å, respectively).

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Section: Type Characteristic Examplesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

X-ray absorption spectroscopic studies of zinc in the N-terminal domain of HIV-2 integrase and model compounds

et al. 2002

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“…Extended X-ray absorption fine structure (EXAFS) data analysis and curve fitting were performed by using EXAFSPAK (http://ssrl.slac.stanford.edu/exafspak.html) and Feff v7.0 (5, 44). Multiple-scattering contributions from outer-shell atoms of histidine ligands were quantified as described previously (15), with parameters derived from tetra(imidazole) zinc(II) perchlorate (7).…”

Section: Methodsmentioning

confidence: 99%

Structural and Kinetic Characterization of an Archaeal β-Class Carbonic Anhydrase

et al. 2000

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The ␤-class carbonic anhydrase from the archaeon Methanobacterium thermoautotrophicum (Cab) was structurally and kinetically characterized. Analytical ultracentrifugation experiments show that Cab is a tetramer. Circular dichroism studies of Cab and the Spinacia oleracea (spinach) ␤-class carbonic anhydrase indicate that the secondary structure of the ␤-class enzymes is predominantly ␣-helical, unlike that of the ␣-or ␥-class enzymes. Extended X-ray absorption fine structure results indicate the active zinc site of Cab is coordinated by two sulfur and two O/N ligands, with the possibility that one of the O/N ligands is derived from histidine and the other from water. Both the steady-state parameters k cat and k cat /K m for CO 2 hydration are pH dependent. The steady-state parameter k cat is buffer-dependent in a saturable manner at both pH 8.5 and 6.5, and the analysis suggested a ping-pong mechanism in which buffer is the second substrate. At saturating buffer conditions and pH 8.5, k cat is 2.1-fold higher in H 2 O than in D 2 O, consistent with an intramolecular proton transfer step being rate contributing. The steady-state parameter k cat /K m is not dependent on buffer, and no solvent hydrogen isotope effect was observed. The results suggest a zinc hydroxide mechanism for Cab. The overall results indicate that prokaryotic ␤-class carbonic anhydrases have fundamental characteristics similar to the eukaryotic ␤-class enzymes and firmly establish that the ␣-, ␤-, and ␥-classes are convergently evolved enzymes that, although structurally distinct, are functionally equivalent.The thermophilic archaeon Methanobacterium thermoautotrophicum obtains energy for growth by the reduction of CO 2 to CH 4 and is also an obligate chemolithoautotroph; thus, this organism has a high demand for CO 2 . Carbonic anhydrase, a zinc-containing enzyme catalyzing the reversible hydration of carbon dioxide (equation 1)is expected to play an important role in the growth of M. thermoautotrophicum and may have several functions, including transporting HCO 3 Ϫ into the cell and providing CO 2 or HCO 3 Ϫ to enzymes that utilize these substrates. Based on sequence comparisons, carbonic anhydrases belong to three genetically distinct classes (␣, ␤, and ␥) which appear to have independent origins (24). The most extensively studied enzymes are those from the ␣-class, which is composed primarily of mammalian carbonic anhydrases, but also includes enzymes from the green alga Chlamydomonas reinhardtii (19,20) and the prokaryote Neisseria gonorrhoeae (13). The ␤-class enzymes are abundant in C 3 and C 4 monocotyledenous and dicotyledenous plants and green unicellular algae (24, 43), where they are essential for photosynthetic CO 2 fixation (6). The most recently identified class of carbonic anhydrase, the ␥-class (24), is represented by the prototype Cam from the archaeon Methanosarcina thermophila (2). Even though sequences encoding putative ␥-class carbonic anhydrases have been found in prokaryotes from both the Bacteria and Archaea domains (2...

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“…A similar zinc site was also found in ferredoxin from Thermoplasma acidophilum strain HO-62 that also contained one 1ϩ,0 cluster, and one [4Fe- 4S] 2ϩ,1ϩ cluster (7). This site was analyzed by zinc K-edge x-ray absorption spectroscopy (XAS) (8) and was found to be essentially identical to the zinc site in Sulfolobus sp. ferredoxin.…”

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confidence: 95%

“…The number and type of FeS clusters in this structure are inconsistent with our previous spectroscopic analysis of the purified protein, which suggested one 1ϩ,0 cluster (cluster I; E 1 ⁄2 ϭ Ϫ280 mV) and one 2ϩ,1ϩ cluster (cluster II; E 1 ⁄2 ϭ Ϫ530 mV) (5). Other archaeal zinc-containing ferredoxins from T. acidophilum (7,8) (Fig. 1).…”

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confidence: 99%

Spectroscopic Investigation of Selective Cluster Conversion of Archaeal Zinc-containing Ferredoxin fromSulfolobus sp. Strain 7

Iwasaki¹,

Watanabe²,

Ohmori³

et al. 2000

Journal of Biological Chemistry

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Ferredoxins, small iron-sulfur (FeS) proteins in archaea, serve as water-soluble electron acceptors of acyl-coenzyme A forming 2-oxoacid:ferredoxin oxidoreductase, a key enzyme involved in the central archaeal metabolic pathways (1-5). The 2.0-Å resolution x-ray crystal structure (PDB 1 entry 1XER ; Ref. 6) of ferredoxin from Sulfolobus sp. strain 7 (JCM 10545; optimal growth conditions, pH 2.5-3 and 80°C) showed the presence of an unexpected isolated zinc center, tetrahedrally coordinated by three nitrogen atoms from histidine residues in the N-terminal extension region (N␦1 of His 16 , N⑀2 of His 19 , and N␦1 of His 34 ) and one O␦1 atom from Asp 76 in the FeS cluster-binding core fold (Fig. 1). A similar zinc site was also found in ferredoxin from Thermoplasma acidophilum strain HO-62 that also contained one 1ϩ,0 cluster, and one [4Fe-4S] 2ϩ,1ϩ cluster (7). This site was analyzed by zinc K-edge x-ray absorption spectroscopy (XAS) (8) and was found to be essentially identical to the zinc site in Sulfolobus sp. ferredoxin. Thus, these unusual ferredoxins contain both the conventional FeS clusters and a structurally conserved, isolated zinc center. This new class of bacterial type ferredoxin, isolated from phylogenetically diverse members of several aerobic and thermoacidophilic archaea, are thus called "zinc-containing ferredoxins" (2, 6 -10).Another unexpected result of the crystal structure of airoxidized Sulfolobus sp. zinc-containing ferredoxin was the presence of two [3Fe-4S] clusters beside one isolated zinc center (9) (Fig. 1). The number and type of FeS clusters in this structure are inconsistent with our previous spectroscopic analysis of the purified protein, which suggested one 1ϩ,0 cluster (cluster I; E 1 ⁄2 ϭ Ϫ280 mV) and one 2ϩ,1ϩ cluster (cluster II; E 1 ⁄2 ϭ Ϫ530 mV) (5). Other archaeal zinc-containing ferredoxins from T. acidophilum (7,8) (Fig. 1).Because FeS clusters have a remarkable facility for interconversion under protein-bound conditions (reviewed in Ref. 14), the significant discrepancy of the types of FeS clusters of Sulfolobus sp. zinc-containing ferredoxin in the crystalline and as-isolated states may represent selective degradation of the cluster II to a [3Fe-4S] form in vitro. Although the [4Fe-4S] 7 [3Fe-4S] cluster interconversion is well known in some bacterial type ferredoxins (14 -25) and aconitase (26 -29), there is no conclusive report demonstrating the selective cluster conversion at the cluster II site in bacterial type dicluster ferredoxins. The most extensive spectroscopic analyses of oxidative degra-

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Structural Conservation of the Isolated Zinc Site in Archaeal Zinc-containing Ferredoxins as Revealed by X-ray Absorption Spectroscopic Analysis and Its Evolutionary Implications

Cited by 10 publications

References 72 publications

X-ray absorption spectroscopic studies of zinc in the N-terminal domain of HIV-2 integrase and model compounds

X-ray absorption spectroscopic studies of zinc in the N-terminal domain of HIV-2 integrase and model compounds

Structural and Kinetic Characterization of an Archaeal β-Class Carbonic Anhydrase

Spectroscopic Investigation of Selective Cluster Conversion of Archaeal Zinc-containing Ferredoxin fromSulfolobus sp. Strain 7

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