Cluster-Dependent Charge-Transfer Dynamics in Iron–Sulfur Proteins

Mao, Ziliang; Liou, Shu-Hao; Khadka, Nimesh; Jenney, Francis E.; Goodin, David B.; Seefeldt, Lance C.; Adams, Michael W. W.; Cramer, Stephen P.; Larsen, Delmar S.

doi:10.1021/acs.biochem.7b01159

Cited by 12 publications

(15 citation statements)

References 67 publications

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“…The data is consistent with photoinduced electron transfer (ET) from the [4Fe–4S] + cluster to SAM, 48 providing the EPR-silent [4Fe–4S] 2+ cluster and a SAM-derived organic cryo-trapped radical to study; such photoinduced ET has not previously been reported for RS enzymes. On the basis of known RS enzyme chemistry, the most likely identity of the new radical species would be the 5′-dAdo· radical, resulting from reductive cleavage of SAM.…”

Section: Resultssupporting

confidence: 81%

The Elusive 5′-Deoxyadenosyl Radical: Captured and Characterized by Electron Paramagnetic Resonance and Electron Nuclear Double Resonance Spectroscopies

et al. 2019

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The 5′-deoxyadenosyl radical (5′-dAdo·) abstracts a substrate H atom as the first step in radical-based transformations catalyzed by adenosylcobalamin-dependent and radical S-adenosyl-L-methionine (RS) enzymes. Notwithstanding its central biological role, 5′-dAdo· has eluded characterization despite efforts spanning more than a half-century. Here, we report generation of 5′-dAdo· in a RS enzyme active site at 12 K using a novel approach involving cryogenic photoinduced electron transfer from the [4Fe–4S]+ cluster to the coordinated S-adenosylmethionine (SAM) to induce homolytic S–C5′ bond cleavage. We unequivocally reveal the structure of this long-sought radical species through the use of electron paramagnetic resonance (EPR) and electron nuclear double resonance (ENDOR) spectroscopies with isotopic labeling, complemented by density-functional computations: a planar C5′ (2pπ) radical (~70% spin occupancy); the C5′(H)2 plane is rotated by ~37° (experiment)/39° (DFT) relative to the C5′–C4′–(C4′–H) plane, placing a C5′–H antiperiplanar to the ribose-ring oxygen, which helps stabilize the radical against elimination of the 4′–H. The agreement between φ from experiment and in vacuo DFT indicates that the conformation is intrinsic to 5-dAdo· itself, and not determined by its environment.

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Section: Resultssupporting

confidence: 81%

The Elusive 5′-Deoxyadenosyl Radical: Captured and Characterized by Electron Paramagnetic Resonance and Electron Nuclear Double Resonance Spectroscopies

et al. 2019

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“…The spectrum associated with the long-lived photoproduct of the (Fe-S)ox state of the Rieske protein (Fig. 3B) is similar to those observed on the picosecond-nanosecond timescale in other oxidized 2Fe-2S proteins [8,9] and comprises both positive and negative (440-500 nm and around 580 nm) absorption changes. As indicated before, the similarity of the extrema with those of the steady-state reduced-minus-oxidized spectrum (Fig.…”

Section: Discussionsupporting

confidence: 68%

“…The observed lifetimes are much shorter (~1.5 ps for Fe-Sox, ~25 ps for Fe-Sred), an observation that we assign to quenching by charge transfer reactions. Indeed, the number of Fe-S proteins [8,9]. Also, we have previously suggested photo-oxidation of the Rieske 2Fe-2S cluster in the Rhodobacter capsulatus bc1 complex, but this assessment was complicated by the dominant absorption of the hemes in this complex [7].…”

Section: Discussionmentioning

confidence: 99%

“…Here, states with lifetimes in the nanosecond range were assigned to photo-reduction products populated from excited states decaying within a few picoseconds. These studies were then extended to different types of Fe-S centers [9]. On the other hand, very recently a reaction intermediate in pyruvate formate-lyase activating enzyme observed by EPR after prolonged illumination was suggested to be initiated by electron transfer from the reduced [4Fe-4S] center [10].…”

Section: Introductionmentioning

confidence: 99%

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Fluorescent iron‑sulfur centers: Photochemistry of the PetA Rieske protein from Aquifex aeolicus

Vos

Salman

Ramodiharilafy

et al. 2021

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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Cytochrome bc1 complexes are energy-transducing enzymes and key components of respiratory electron chains. They contain Rieske 2Fe-2S proteins that absorb very weakly in the visible absorption region compared to the heme cofactors of the cytochromes, but are known to yield photoproducts. Here, the photoreactions of isolated Rieske proteins from the hyperthermophilic bacterium Aquifex aeolicus are studied in two redox states using ultrafast transient fluorescence and absorption spectroscopy. We provide evidence, for the first time in iron-sulfur proteins, of very weak fluorescence of the excited state, in the oxidized as well as the reduced state. The excited states of the oxidized and reduced forms decay in 1.5 ps and 30 picoseconds, respectively. In both cases they give rise to product states with lifetimes beyond 1 nanosecond, reflecting photo-reduction of oxidized centers as well as photo-oxidation of reduced centers. Potential reaction partners are discussed and studied using site-directed mutagenesis. For the reduced state, a nearby disulfide bridge is suggested as an electron acceptor. The resulting photoproducts in either state may play a role in photoactivation processes.

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“…The key feature that makes the iron-sulfur clusters efficient electron mediators is the dense ladder of excited states that presumably allows the system to switch between them upon geometry change in a nonadiabatic process [5,6]. Recently, light-induced charge-transfer (CT) pathways were spectroscopically characterized and a presence of longlived CT states was confirmed [7,8]. Based on a classical works on iron-sulfur clusters [9][10][11] that provide the analysis of a symmetry-broken (BS) ground state determinant of the Xα (or related) method, the CT state was attributed to Fe ← S(cysteine) excitation.…”

Section: Introductionmentioning

confidence: 99%

Characterization of charge transfer excited states in [2Fe–2S] iron–sulfur clusters using conventional configuration interaction techniques

Kubas

2020

Theor Chem Acc

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The experimental UV–Vis spectra of the biologically relevant [2Fe–2S] iron–sulfur clusters feature typically three bands in the 300–800 nm range. Based on ground-state orbitals and using the one electron transition picture, these bands are said to be of charge transfer character. The key complication in the electronic structure calculations of these compounds are the antiferromagnetic coupling of the iron centers and high covalency of Fe–S bonds. Thus, the examples of the direct computations of electronically excited states of these systems are rare. Whereas low lying electronic excited states were subject of recent studies, higher energy states computed with many-body theories were never reported. In this work we present, for the first time, calculations of the electronic spectra of [Fe2S2](SMe)42− biomimetic compound. We demonstrate that spin-averaged restricted open-shell Hartree–Fock orbitals are superior to high-spin orbitals and are convenient reference for subsequent configuration interaction calculations. Moreover, the use of conventional configuration interaction methods enabled us to study the nature of the excited states in details with the difference density maps. By systematic extension of the donor orbital space we show that key excitations in the 300–800 nm range are of Fe 3d ← (μ-S) character.

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Cluster-Dependent Charge-Transfer Dynamics in Iron–Sulfur Proteins

Cited by 12 publications

References 67 publications

The Elusive 5′-Deoxyadenosyl Radical: Captured and Characterized by Electron Paramagnetic Resonance and Electron Nuclear Double Resonance Spectroscopies

The Elusive 5′-Deoxyadenosyl Radical: Captured and Characterized by Electron Paramagnetic Resonance and Electron Nuclear Double Resonance Spectroscopies

Fluorescent iron‑sulfur centers: Photochemistry of the PetA Rieske protein from Aquifex aeolicus

Characterization of charge transfer excited states in [2Fe–2S] iron–sulfur clusters using conventional configuration interaction techniques

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