Electron tunneling pathways in ruthenated proteins

Beratan, David N.; Onuchic, José N.; Betts, Jonathan N.; Bowler, Bruce E.; Gray, Harry B.

doi:10.1021/ja00178a011

Cited by 227 publications

(174 citation statements)

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“…ET Pathways. Ligand-metal covalency plays an important role in activating ET pathways and increasing k ET through increased donor-acceptor coupling (H DA ) (33,(39)(40)(41). The nature of the ET pathways coupling the Cu A active site with its donor and acceptor has been the subject of much research.…”

Section: Discussionmentioning

confidence: 99%

Axial interactions in the mixed-valent Cu _A active site and role of the axial methionine in electron transfer

Tsai

Hadt

Marshall

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Within Cu-containing electron transfer active sites, the role of the axial ligand in type 1 sites is well defined, yet its role in the binuclear mixed-valent Cu A sites is less clear. Recently, the mutation of the axial Met to Leu in a Cu A site engineered into azurin (Cu A Az) was found to have a limited effect on E 0 relative to this mutation in blue copper (BC). Detailed low-temperature absorption and magnetic circular dichroism, resonance Raman, and electron paramagnetic resonance studies on Cu A Az (WT) and its M123X (X = Q, L, H) axial ligand variants indicated stronger axial ligation in M123L/H. Spectroscopically validated density functional theory calculations show that the smaller ΔE 0 is attributed to H 2 O coordination to the Cu center in the M123L mutant in Cu A but not in the equivalent BC variant. The comparable stabilization energy of the oxidized over the reduced state in Cu A and BC (Cu A ∼ 180 mV; BC ∼ 250 mV) indicates that the S(Met) influences E 0 similarly in both. Electron delocalization over two Cu centers in Cu A was found to minimize the Jahn-Teller distortion induced by the axial Met ligand and lower the inner-sphere reorganization energy. The Cu-S(Met) bond in oxidized Cu A is weak (5.2 kcal/ mol) but energetically similar to that of BC, which demonstrates that the protein matrix also serves an entatic role in keeping the Met bound to the active site to tune down E 0 while maintaining a low reorganization energy required for rapid electron transfer under physiological conditions. spectroscopy | reduction potential | energy transduction pathway L ong-range electron transfer (ET) is vital to a wide range of biological processes, including two key energy transduction pathways essential for life: H 2 O oxidation in photosynthesis and O 2 reduction in respiration (1, 2). Nature has adapted a conserved cupredoxin fold motif (i.e., the Greek-key β barrel) to construct two evolutionarily linked, but structurally distinct Cucontaining ET proteins (3-5). These are the mononuclear type 1 (T1) or blue copper (BC) and binuclear purple Cu A proteins. The first coordination sphere of the classic BC sites [e.g., plastocyanin (Pc) and azurin (Az)] consists of a trigonally distorted tetrahedral environment where Cu resides in an equatorial plane formed by one S(Cys) and two N(His) ligands and has an axial S (Met) ligand (Fig. 1A) (Fig. 1B) (8-11). Both sites carry out rapid, efficient longrange ET with rates on the order of 10 3 -10 5 s −1 (12, 13).Although BC proteins use a Cu + /Cu 2+ redox couple, the binuclear Cu A sites use a (Cu 1+ -Cu 1+ )/(Cu 1.5+ -Cu 1.5+ ) redox cycle. The oxidized form of Cu A is mixed-valent (MV), with a highly covalent Cu 2 S 2 core that gives rise to its unique spectroscopic features. The unpaired electron is fully delocalized over the two Cu centers and exhibits a characteristic seven-line 63,65 Cu hyperfine splitting pattern in electron paramagnetic resonance (EPR) spectroscopy (14, 15). Maintaining valence delocalization even in the presence of a low symmetry protein ...

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Section: Discussionmentioning

confidence: 99%

Axial interactions in the mixed-valent Cu _A active site and role of the axial methionine in electron transfer

Tsai

Hadt

Marshall

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…However, in the latter three systems, the closest approach between prosthetic groups is 8-9 A , whereas in the ternary complex the closest copper-to-heme distance is about 21 A. It has been postulated that the dynamics of electron transfer between prosthetic groups may depend not so much on the through space distance as on the through bond pathways between the groups (Beratan et al, 1990). Analysis of such pathways in the ternary complex must be postponed until the structure is completed.…”

Section: Discussionmentioning

confidence: 99%

Preliminary crystal structure studies of a ternary electron transfer complex between a quinoprotein, a blue copper protein, and a c‐type cytochrome

et al. 1993

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A ternary electron transfer protein complex has been crystallized and a preliminary structure investigation has been carried out. The complex is composed of a quinoprotein, methylamine dehydrogenase (MADH), a blue copper protein, amicyanin, and a C-type cytochrome All three proteins were isolated from Paracoccus denitrificans. The crystals of the complex are orthorhombic, space group C2221 with cell dimensions a = 148.81 A , b = 68.85 A, and c = 187.18 A . Two types of isomorphous crystals were prepared: one using native amicyanin and the other copper-free apo-amicyanin. The diffraction data were collected at 2.75 A resolution from the former and at 2.4 A resolution from the latter. The location of the MADH portion was determined by molecular replacement. The copper site of the amicyanin molecule was located in an isomorphous difference Fourier while the iron site of the cytochrome was found in an anomalous difference Fourier. The MADH from P. denitrificans (PD-MADH) is an H,L, hetero-tetramer with the H subunit containing 373 residues and the L subunit 131 residues, the latter containing a novel redox cofactor, tryptophan tryptophylquinone (TTQ). The amicyanin of P. denitrificans contains 105 residues and the cytochrome cg5li contains 155 residues. The ternary complex consists of one MADH tetramer with two molecules of amicyanin and two of Cssli, forming a hetero-octamer; the octamer is located on a crystallographic diad. The relative positions of the three redox centers-i.e., the TTQ of MADH, the copper of amicyanin, and the heme group of are presented. ., 1983). The crystal structures of MADH from both Thiobucillus versutus (Vellieux et al., 1989) and P. denitrifcuns (Chen et al., 1992b) have been determined, based on an X-ray sequence for the former. The structure of the latter has recently been rebuilt using the DNA-derived amino acid sequence (Chistoserdov et al., 1992) and refined at 1.75 A resolution (Chen et al., in prep.).The nature of the redox cofactor of MADH has been a challenging topic over the last decade. Recently a cofactor model was proposed for MADH based on biophysical studies and on the gene sequence of the L subunit of MADH. This new cofactor, 147

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“…One intermediate is identified with hemes I and III largely oxidized and heme IV essentially reduced in accordance with the order of reduction potentials of the unmodified protein. Although no information is available on the intramolecular electron-transfer pathway, it is tempting to propose that heme IV provides the electron to chromium, because they are so close to one another, and hemes I and III reestablish the thermodynamic conditions by electron tunneling to heme IV (41)(42)(43)(44)(45)(46)(47)(48). As far as chromium is concerned, it is reasonable that the three electrons provided by the protein reduce chromate(VI) stepwise (49,50).…”

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The metal reductase activity of some multiheme cytochromes c : NMR structural characterization of the reduction of chromium(VI) to chromium(III) by cytochrome c ₇

Assfalg

Bertini

Bruschi

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

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The redox reaction between CrO 4 2Ϫ and the fully reduced threeheme cytochrome c 7 from Desulfuromonas acetoxidans to give chromium(III) and the fully oxidized protein has been followed by NMR spectroscopy. The hyperfine coupling between the oxidized protein protons and chromium(III), which remains bound to the protein, gives rise to line-broadening effects on the NMR resonances that can be transformed into proton-metal distance restraints. Structure calculations based on these unconventional constraints allowed us to demonstrate that chromium(III) binds at a unique site and to locate it on the protein surface. The metal ion is located 7.9 ؎ 0. S ulfur-and sulfate-reducing bacteria constitute a group of anaerobic organisms, the common feature of which is the use of sulfur and its oxidized forms as electron acceptors. Thiosulfate, sulfur, sulfite, or sulfate ''respiration'' produces sulfide. The end product of the reaction, hydrogen sulfide, can react with heavy metal ions to form less toxic insoluble metal sulfides (1). These bacteria are also able to enzymatically reduce and precipitate heavy metals (2-8). They therefore are important for the geochemical cycle of metals and become particularly relevant for possible applications in the decontamination of environments polluted by toxic heavy metals through bioreduction coupled with precipitation as insoluble sulfides. Among the metals that can be reduced by these bacteria, chromium(VI) is particularly relevant from the technological and environmental point of view, because it represents one of the most common polluting metals and is highly soluble and toxic. § The three heme-containing cytochrome c 7 from the sulfurreducing bacterium Desulfuromonas acetoxidans (Cyt c 7 hereafter) has been proposed to have a role as electron-transfer protein in the sulfur metabolism of this bacterium, acting as a terminal reductase in the metabolic pathway by directly reducing elemental sulfur to sulfide (9); it has been suggested also that it could be involved in the reduction of iron(III) and manganese(IV) (10). The solution structures of the fully oxidized and fully reduced species are available, followed by the x-ray structure of the oxidized species (11)(12)(13)(14). The availability of the assigned NMR spectra and the nuclear Overhauser effects (NOEs; refs. 11 and 15) prompted us to study by NMR the reaction between CrO 4 2Ϫ and fully reduced Cyt c 7 . The products of the reaction are chromium(III) and the oxidized protein with three iron(III) hemes. Because chromium(III) is kinetically inert with respect to ligand exchange, it remains bound to protein residues through which electron transfer occurs. The hyperfine coupling between the unpaired electrons of chromium(III) and the proton nuclei of the protein gives rise to particular features in the NMR spectra (16) that could be used to obtain structural information about the chromium(III) binding site. The redox-inert MoO 4 2Ϫ was used to map the binding site of the anion. NMR has allowed us to obtain a clear picture of the...

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Electron tunneling pathways in ruthenated proteins

Cited by 227 publications

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Axial interactions in the mixed-valent Cu _A active site and role of the axial methionine in electron transfer

Axial interactions in the mixed-valent Cu _A active site and role of the axial methionine in electron transfer

Preliminary crystal structure studies of a ternary electron transfer complex between a quinoprotein, a blue copper protein, and a c‐type cytochrome

The metal reductase activity of some multiheme cytochromes c : NMR structural characterization of the reduction of chromium(VI) to chromium(III) by cytochrome c ₇

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Electron tunneling pathways in ruthenated proteins

Cited by 227 publications

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Axial interactions in the mixed-valent Cu A active site and role of the axial methionine in electron transfer

Axial interactions in the mixed-valent Cu A active site and role of the axial methionine in electron transfer

Preliminary crystal structure studies of a ternary electron transfer complex between a quinoprotein, a blue copper protein, and a c‐type cytochrome

The metal reductase activity of some multiheme cytochromes c : NMR structural characterization of the reduction of chromium(VI) to chromium(III) by cytochrome c 7

Contact Info

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Axial interactions in the mixed-valent Cu _A active site and role of the axial methionine in electron transfer

Axial interactions in the mixed-valent Cu _A active site and role of the axial methionine in electron transfer

The metal reductase activity of some multiheme cytochromes c : NMR structural characterization of the reduction of chromium(VI) to chromium(III) by cytochrome c ₇