Long-range Electron Transfer Research Articles

Radical Transport Facilitated by a Proton Transfer Network at the Subunit Interface of Ribonucleotide Reductase.

Ribonucleotide reductases (RNRs) play an essential role in the conversion of nucleotides to deoxynucleotides in all organisms. The Escherichia coli class Ia RNR requires two homodimeric subunits, α and β. The active form is an asymmetric αα'ββ' complex. The α subunit houses the site for nucleotide reduction initiated by a thiyl radical (C439•), and the β subunit houses the diferric-tyrosyl radical (Y122•) that is essential for C439• formation. The reactions require a highly regulated and reversible long-range proton-coupled electron transfer pathway involving Y122•[β] ↔ W48?[β] ↔ Y356[β] ↔ Y731[α] ↔ Y730[α] ↔ C439[α]. In a recent cryo-EM structure, Y356[β] was revealed for the first time and it, along with Y731[α], spans the asymmetric α/β interface. An E52[β] residue, which is essential for Y356 oxidation, allows access to the interface and resides at the head of a polar region comprising R331[α], E326[α], and E326[α'] residues. Mutagenesis studies with canonical and unnatural amino acid substitutions now suggest that these ionizable residues are important in enzyme activity. To gain further insights into the roles of these residues, Y356• was photochemically generated using a photosensitizer covalently attached adjacent to Y356[β]. Mutagenesis studies, transient absorption spectroscopy, and photochemical assays monitoring deoxynucleotide formation collectively indicate that the E52[β], R331[α], E326[α], and E326[α'] network plays the essential role of shuttling protons associated with Y356 oxidation from the interface to bulk solvent.

Ru Monoimines with Extended Excited-State Lifetimes and Geometrical Modulation of Photoinduced Mixed-Valence Interactions.

The photophysical properties of monodentate-imine ruthenium complexes do not usually fulfil the requirements for supramolecular solar energy conversion schemes. Their short excited-state lifetimes, like the 5.2 ps metal-to-ligand charge transfer (MLCT) lifetime of [Ru(py)4Cl(L)]+ with L = pz (pyrazine), preclude bimolecular or long-range photoinduced energy or electron transfer reactions. Here, we explore two strategies to extend the excited-state lifetime, based on the chemical modification of the distal N atom of pyrazine. On one hand, we used L = pzH+, where protonation stabilized MLCT states, rendering thermal population of MC states less favorable. On the other hand, we prepared a symmetric bimetallic arrangement in which L = {(μ-pz)Ru(py)4Cl} to enable hole delocalization via photoinduced mixed-valence interactions. A lifetime extension of 2 orders of magnitude is accomplished, with charge transfer excited states living 580 ps and 1.6 ns, respectively, reaching compatibility with bimolecular or long-range photoinduced reactivity. These results are similar to those obtained with Ru pentaammine analogues, suggesting that the strategy employed is of general applicability. In this context, the photoinduced mixed-valence properties of the charge transfer excited states are analyzed and compared with those of different analogues of the Creutz-Taube ion, demonstrating a geometrical modulation of the photoinduced mixed-valence properties.

Effect of Water Deuteration on Protein Electron Transfer

Traditional theories of long-range protein electron transfer describe the reaction rate in terms of the tunneling distance and the reaction free energy. They do not recognize two physical effects: (i) local wetting of the active site by hydration water and (ii) protein identity affecting the rate through dynamics and flexibility. We find, by molecular dynamics simulations, a significant, ∼25 times, slowing down of the rate of protein electron transfer upon deuteration. H/D substitution changes the rate constant pre-exponential factor in the regime of electron transfer controlled by medium dynamics. Switching from light to heavy water increases the effective medium relaxation time. The effect is caused by both a global change in the flexibility of the protein backbone and locally stronger hydrogen bonds to charged residues.

Microbial population properties in the hierarchically structured aerobic granular sludge: Phenotype and genotype

Aerobic granular sludge (AGS) is a layered microbial aggregate formed by the ordered self-assembly of different microbial populations. In this study, the outer layer (OL), middle layer (ML), and the inner layer (IL) of matured AGS were obtained by circular cutting. The adhesion of microorganisms in IL was significantly higher than that in OL and ML during the famine period, while the adhesion of microorganisms in ML and OL was significantly higher than that in IL during the feast period, confirming that the formation of AGS started in the famine period, and the feast period promoted the increase of particle size. Microorganisms in the three-layer structure were highly diverse and rich in genes for cytochrome c oxidase synthesis with oxygen as the electron acceptor. G_Pseudoxanthomonas was the dominant bacterium in OL. Its spatial distribution increased gradually from the inside to the outside. G_Rhodanobacter was the dominant bacterium in IL. Its spatial distribution gradually decreased from the inside to the outside. The microorganisms in IL contained abundant pili genes. During the self-assembly process of particle formation, G_ Rhodanobaker adhered stronger than G_ Pseudoxanthomonas. The interface between aerobic and anoxic was about 0.6 mm away from the granule surface. Combined with the electron mediator properties of the extracellular polymeric substance (EPS) in granules, it was speculated that the degradation of organic substrates located in the anoxic layer relied on EPS as a mediator for long-range electron transfer, and finally transferred electrons to O2. This study provides a new viewpoint on the formation mechanism of AGS from the perspective of the ordered self-assembly of microorganisms, offering a theoretical basis for the optimal selection of culture conditions and the application of AGS technology.

Enhancing energy transfer by regulating electron transport pathways in semiconductor metal–organic frameworks

Fe-MOF with short-range and long-range photo-induce electron transfer exhibits highly efficient photon utilization, which is validated by excellent degradation of tetracycline hydrochloride.

Selective incorporation of 5-hydroxytryptophan blocks long range electron transfer in oxalate decarboxylase.

Oxalate decarboxylase from Bacillus subtilis is a binuclear Mn-dependent acid stress response enzyme that converts the mono-anion of oxalic acid into formate and carbon dioxide in a redox neutral unimolecular disproportionation reaction. A π-stacked tryptophan dimer, W96 and W274, at the interface between two monomer subunits facilitates long-range electron transfer between the two Mn ions and plays an important role in the catalytic mechanism. Substitution of W96 with the unnatural amino acid 5-hydroxytryptophan leads to a persistent EPR signal which can be traced back to the neutral radical of 5-hydroxytryptophan with its hydroxyl proton removed. 5-Hydroxytryptophan acts as a hole sink preventing the formation of Mn(III) at the N-terminal active site and strongly suppresses enzymatic activity. The lower boundary of the standard reduction potential for the active site Mn(II)/Mn(III) couple can therefore be estimated as 740 mV against the normal hydrogen electrode at pH4, the pH of maximum catalytic efficiency. Our results support the catalytic importance of long-range electron transfer in oxalate decarboxylase while at the same time highlighting the utility of unnatural amino acid incorporation and specifically the use of 5-hydroxytryptophan as an energetic sink for hole hopping to probe electron transfer in redox proteins.

Metavalent Bonding Origins of Unusual Properties of Group IV Chalcogenides.

A distinct type of metavalent bonding (MVB) is recently proposed to explain an unusual combination of anomalous functional properties of group IV chalcogenide crystals, whose electronic mechanisms and origin remain controversial. Through theoretical analysis of evolution of bonding along continuous paths in structural and chemical composition space, emergence of MVB in rocksalt chalcogenides is demonstrated as a consequence of weakly broken symmetry of parent simple-cubic crystals of Group V metalloids. High electronic degeneracy at the nested Fermi surface of parent metal drives spontaneous breaking of its translational symmetry with structural and chemical fields, which open up a small energy gap and mediate strong coupling between conduction and valence bands making metavalent crystals highly polarizable, conductive, and sensitive to bond-lengths. Stronger symmetry-breaking structural and chemical fields, however, transform them discontinuously to covalent and ionic semiconducting states. MVB involves bonding-antibonding pairwise interactions alternating along linear chains of at least five atoms, which facilitate long-range electron transfer in response to polar fields causing unusual properties. The precise picture of MVB predicts anomalous second-order Raman scattering as an addition to set off their unusual properties, and will guide in design of new metavalent materials with improved thermoelectric, ferroelectric and nontrivial electronic topological properties.

New Perspective on Electron Transfer through Molecules.

Motivated by experiments which display unusual length and temperature effects for electron transfer in the nanometer length regime, we propose a new approach for describing long-range electron transfer (ET) processes through molecules. We posit that the electron reorganization in the molecules (e.g., the electronic polarization of a macromolecule or organic film by an applied electric potential, or the injected charge generating a dipole moment) should be included in the description. We numerically solve a one-dimensional model for the electron transport, which includes electron-electron interactions explicitly, and we show that it generates a power law distance dependence for electron transport similar to that observed in experiments. The model does not include vibrations explicitly and should be consistent with the weak temperature dependences observed experimentally. This approach emphasizes the need to treat the electronic changes in the molecule(s) more explicitly to understand the behavior.

Phosphorylation disrupts long-distance electron transport in cytochrome c

It has been recently shown that electron transfer between mitochondrial cytochrome c and the cytochrome c1 subunit of the cytochrome bc1 can proceed at long-distance through the aqueous solution. Cytochrome c is thought to adjust its activity by changing the affinity for its partners via Tyr48 phosphorylation, but it is unknown how it impacts the nanoscopic environment, interaction forces, and long-range electron transfer. Here, we constrain the orientation and separation between cytochrome c1 and cytochrome c or the phosphomimetic Y48pCMF cytochrome c, and deploy an array of single-molecule, bulk, and computational methods to investigate the molecular mechanism of electron transfer regulation by cytochrome c phosphorylation. We demonstrate that phosphorylation impairs long-range electron transfer, shortens the long-distance charge conduit between the partners, strengthens their interaction, and departs it from equilibrium. These results unveil a nanoscopic view of the interaction between redox protein partners in electron transport chains and its mechanisms of regulation.

Reconstructing bridging carbon atoms (from sp3-C to sp2-C) of pyrolytic N-doped carbon to enhance oxygen reduction reaction

The development of new regulation strategy for constructing functional carbon skeletons is a standing challenge for oxygen reduction reaction (ORR). Herein, the locally ordered graphene microcrystals with suitable N-sites derived from glucose are synthesized under the assistance of low melting point zinc molten salt. Utilizing the structural features of graphene microcrystals (“house of cards” model), the work function of carbon skeleton is reduced after inducing the conversion of bridging sp3-C to bridging sp2-C (ratio of sp2-C to sp3-C increases from 3.75 to 7.41). The lower work function of locally ordered microarchitectures decreases the long-range electron transfer barrier in outer-Helmholtz plane. And the synergy between pyridinic N and graphitic N is beneficial for enhancing short-range electron transfer process in inner-Helmholtz plane. After rearrangement of carbon skeletons, the half-wave potential can increase from 0.846 V to 0.874 V, and the HO2– by-product yield decreases from 31.5 % to 6.9 %. Furthermore, the discharge voltage of locally ordered microarchitecture (1.31 V) at 10 mA cm−2 can surpass the commercial Pt/C (1.25 V) in Zn-air battery devices. In brief, it provides a new direction of structure design for carbonaceous catalysts.

Analysis Method for Rotating Disk Voltammograms of Electrocatalytic Reaction —Oxygen Reduction Reaction—

Rotating disk voltammograms of electrocatalytic reactions were often analyzed on a model of the totally irreversible reaction. The problem with the conventional method is pointed out, and the validity of an analysis method on a model of the electrocatalytic reaction is demonstrated for oxygen-reduction reaction (ORR) as an example. Rotating disk voltammograms of ORRs sometimes show gradual change in the limiting current region called residual slope. The phenomenon has been explained on a random distribution model in which the catalytic sites communicate in long-range electron transfer with the electronic conductors that locate at distances (z), and are uniformly distributed with respect to z. Observed data of an ORR were well reproduced by non-linear least squares analysis on the random distribution model. The result of the analysis is briefly discussed.

The Selective Function of Quantum Biological Electron Transfer between DNA Bases and Metal Ions in DNA Replication.

Metal ions play vital roles in the electron transfer between biological molecules in humans, animals, and plants. However, the electron transfer between metal ions and nucleic acids and its impact on DNA-ion binding during DNA replication has been ignored. Here, we present a long-range quantum biological electron transfer (QBET) between DNA bases and metal ions and its selective function of DNA-ion binding in DNA replication. We discover biophysical DNA-ion binding and create biological filters that allow selective DNA replication by dual modulators of the valence and concentration of metal ions. QBET-based DNA replication filters provide powerful tools for ultrasensitive polymerase chain reaction (PCR) to selectively amplify target sequences with a discrete concentration window of metal ions; for example, Au3+ exhibits a concentration window that is approximately 3 orders of magnitude lower than that of Na+. DNA-ion filters provide new perspectives into metal ion-mediated QBET in DNA replication and hold great potential in life sciences and medical applications.

Iron Mobilization from Ferritin in Yeast Cell Lysate and Physiological Implications.

Most in vitro iron mobilization studies from ferritin have been performed in aqueous buffered solutions using a variety of reducing substances. The kinetics of iron mobilization from ferritin in a medium that resembles the complex milieu of cells could dramatically differ from those in aqueous solutions, and to our knowledge, no such studies have been performed. Here, we have studied the kinetics of iron release from ferritin in fresh yeast cell lysates and examined the effect of cellular metabolites on this process. Our results show that iron release from ferritin in buffer is extremely slow compared to cell lysate under identical experimental conditions, suggesting that certain cellular metabolites present in yeast cell lysate facilitate the reductive release of ferric iron from the ferritin core. Using filtration membranes with different molecular weight cut-offs (3, 10, 30, 50, and 100 kDa), we demonstrate that a cellular component >50 kDa is implicated in the reductive release of iron. When the cell lysate was washed three times with buffer, or when NADPH was omitted from the solution, a dramatic decrease in iron mobilization rates was observed. The addition of physiological concentrations of free flavins, such as FMN, FAD, and riboflavin showed about a two-fold increase in the amount of released iron. Notably, all iron release kinetics occurred while the solution oxygen level was still high. Altogether, our results indicate that in addition to ferritin proteolysis, there exists an auxiliary iron reductive mechanism that involves long-range electron transfer reactions facilitated by the ferritin shell. The physiological implications of such iron reductive mechanisms are discussed.

The Intriguing Role of Iron-Sulfur Clusters in the CIAPIN1 Protein Family

Iron-sulfur (Fe/S) clusters are protein cofactors that play a crucial role in essential cellular functions. Their ability to rapidly exchange electrons with several redox active acceptors makes them an efficient system for fulfilling diverse cellular needs. They include the formation of a relay for long-range electron transfer in enzymes, the biosynthesis of small molecules required for several metabolic pathways and the sensing of cellular levels of reactive oxygen or nitrogen species to activate appropriate cellular responses. An emerging family of iron-sulfur cluster binding proteins is CIAPIN1, which is characterized by a C-terminal domain of about 100 residues. This domain contains two highly conserved cysteine-rich motifs, which are both involved in Fe/S cluster binding. The CIAPIN1 proteins have been described so far to be involved in electron transfer pathways, providing electrons required for the biosynthesis of important protein cofactors, such as Fe/S clusters and the diferric-tyrosyl radical, as well as in the regulation of cell death. Here, we have first investigated the occurrence of CIAPIN1 proteins in different organisms spanning the entire tree of life. Then, we discussed the function of this family of proteins, focusing specifically on the role that the Fe/S clusters play. Finally, we describe the nature of the Fe/S clusters bound to CIAPIN1 proteins and which are the cellular pathways inserting the Fe/S clusters in the two cysteine-rich motifs.

Critical Roles of Exchange and Superexchange Interactions in Dictating Electron Transfer and Reactivity in Metalloenzymes.

Electron transfer (ET) is a fundamental process in transition-metal-dependent metalloenzymes. In these enzymes, the spin-spin interactions within the same metal center and/or between different metal sites can play a pivotal role in the catalytic cycle and reactivity. This Perspective highlights that the exchange and/or superexchange interactions can intrinsically modulate the inner-sphere and long-range electron transfer, thus controlling the mechanism and activity of metalloenzymes. For mixed-valence diiron oxygenases, the spin-regulated inner-sphere ET can be dictated by exchange interactions, leading to efficient O-O bond activations. Likewise, the spin-regulated inner-sphere ET can be enhanced by both exchange and superexchange interactions in [Fe4S4]-dependent SAM enzymes, which enable the efficient cleavage of the S─C(γ) or S─C5' bond of SAM. In addition to inner-sphere ET, superexchange interactions may modulate the long-range ET between metalloenzymes. We anticipate that the exchange and superexchange enhanced reactivity could be applicable in other important metalloenzymes, such as Photosystem II and nitrogenases.

Lignin peroxidase-catalyzed direct oxidation of trace organic pollutants through a long-range electron transfer mechanism: Using propranolol as an example

In this work, lignin peroxidase (LiP) was extracted for the in vitro degradation of a persistent compound (propranolol, PPN). The results showed that 94.2% of PPN was degraded at 30 U L−1 LiP activity and 10 mg L−1 PPN. The PPN degradation rate increased from 33.5% to 94.2% when the veratryl alcohol (VA) concentration varied from 0 to 180 µM, but decreased to 73.1% with further VA addition. This phenomenon confirmed that VA was indispensable, however, it also acted as a competitive inhibitor of PPN oxidation. Computational analysis revealed that the Trp171…iron porphyrin (TRP-FeP) path was responsible for specific substrate (e.g., VA) transformation, and another long-range electron transfer (LRET) path through His–Asp…FeP (HSP-FeP) was discovered for non-specific substrate (e.g., PPN) degradation. These two electron-transfer routes shared one catalytic center, and VA protected the enzyme from H2O2-dependent inactivation. The HSP-FeP path transformed PPN through single electron transfer or H abstraction mechanisms. In addition, hydroxyl radicals generated in the LiP/H2O2 system were involved in the hydroxylation of the PPN intermediates. Possible degradation pathways were deduced using these degradation mechanisms and mass-spectrometry analysis. The multipath degradation mechanism endowed LiP with a remarkable capacity for removing various recalcitrant pollutants in environmental remediation.

Dissecting the Structural and Conductive Functions of Nanowires in Geobacter sulfurreducens Electroactive Biofilms.

ABSTRACTConductive nanowires are thought to contribute to long-range electron transfer (LET) in Geobacter sulfurreducens anode biofilms. Three types of nanowires have been identified: pili, OmcS, and OmcZ. Previous studies highlighted their conductive function in anode biofilms, yet a structural function also has to be considered. We present here a comprehensive analysis of the function of nanowires in LET by inhibiting the expression of each nanowire. Meanwhile, flagella with poor conductivity were expressed to recover the structural function but not the conductive function of nanowires in the corresponding nanowire mutant strain. The results demonstrated that pili played a structural but not a conductive function in supporting biofilm formation. In contrast, the OmcS nanowire played a conductive but not a structural function in facilitating electron transfer in the biofilm. The OmcZ nanowire played both a structural and a conductive function to contribute to current generation. Expression of the poorly conductive flagellum was shown to enhance biofilm formation, subsequently increasing current generation. These data support a model in which multiheme cytochromes facilitate long-distance electron transfer in G. sulfurreducens biofilms. Our findings also suggest that the formation of a thicker biofilm, which contributed to a higher current generation by G. sulfurreducens, was confined by the biofilm formation deficiency, and this has applications in microbial electrochemical systems.

Crystalline molybdenum carbide−amorphous molybdenum oxide heterostructures: In situ surface reconfiguration and electronic states modulation for Li−S batteries

Designing heterostructure electrocatalysts synergizing highly polar component and conductive matrix hold great promise to regulate lithium polysulfides (LiPSs) toward high−performance Li−S batteries based on anchoring−diffusion−conversion mechanism. Nevertheless, performance ceiling exists, restrict severely by the significant LiPSs diffusion barrier, which inevitably decrease the conversion efficiency of LiPSs. Amorphization can not only promote the diffusion of LiPSs on catalyst surface but also induce the modulation of surface electronic states and strengthen the adsorption toward LiPSs, in comparison with crystalline counterpart. Herein, crystalline Mo2C−amorphous MoO3 heterostructure grown on nitrogen doped carbon nanosheets is meticulously designed as an efficient sulfur immobilizer and promoter through a facile oxygen plasma treatment strategy. With the integrated advantage of improved adsorption and facilitated diffusion of LiPSs by amorphous MoO3, superior LiPSs redox kinetics by the catalytic effect of conductive Mo2C, and long-range electron transfer network arising from nitrogen doped carbon nanosheets, the assembled battery based on the as-developed modified separator endows excellent electrochemical performance and satisfactory cycling stability. This work provides an easy route to synergistic regulate crystallinity and heterogeneous interfaces of multifunctional catalysts for high energy density Li−S batteries.

Short and long-range electron transfer compete to determine free-charge yield in organic semiconductors.

Understanding how Frenkel excitons efficiently split to form free-charges in low-dielectric constant organic semiconductors has proven challenging, with many different models proposed in recent years to explain this phenomenon. Here, we present evidence that a simple model invoking a modest amount of charge delocalization, a sum over the available microstates, and the Marcus rate constant for electron transfer can explain many seemingly contradictory phenomena reported in the literature. We use an electron-accepting fullerene host matrix dilutely sensitized with a series of electron donor molecules to test this hypothesis. The donor series enables us to tune the driving force for photoinduced electron transfer over a range of 0.7 eV, mapping out normal, optimal, and inverted regimes for free-charge generation efficiency, as measured by time-resolved microwave conductivity. However, the photoluminescence of the donor is rapidly quenched as the driving force increases, with no evidence for inverted behavior, nor the linear relationship between photoluminescence quenching and charge-generation efficiency one would expect in the absence of additional competing loss pathways. This behavior is self-consistently explained by competitive formation of bound charge-transfer states and long-range or delocalized free-charge states, where both rate constants are described by the Marcus rate equation. Moreover, the model predicts a suppression of the inverted regime for high-concentration blends and efficient ultrafast free-charge generation, providing a mechanistic explanation for why Marcus-inverted-behavior is rarely observed in device studies.

Modulation of proton-coupled electron transfer reactions in lysine-containing alpha-helixes: alpha-helixes promoting long-range electron transfer.

The proton-coupled electron transfer (PCET) reaction plays an important role in promoting many biological and chemical reactions. Usually, the rate of the PCET reaction increases with an increase in the electron transfer distance because long-range electron transfer requires more free energy barriers. Our density functional theory calculations here reveal that the mechanism of PCET occurring in lysine-containing alpha(α)-helixes changes with an increasing number of residues in the α-helical structure and the different conformations because of the modulation of the excess electron distribution by the α-helical structures. The rate constants of the corresponding PCET reactions are independent of or substantially shallower dependent on the electron transfer distances along α-helixes. This counter-intuitive behavior can be attributed to the fact that the formation of larger macro-cylindrical dipole moments in longer helixes can promote electron transfer along the α-helix with a low energy barrier. These findings may be useful to gain insights into long-range electron transfer in proteins and design α-helix-based electronics via the regulation of short-range proton transfer.