Bioinorganic Systems Research Articles

Porous Hollow Fiber Nickel Electrodes for Effective Supply and Reduction of Carbon Dioxide to Methane through Microbial Electrosynthesis

AbstractMicrobial electrochemical reduction of CO2 gas to value‐added chemical products requires the development of an electrode architecture with a three‐phase interface for efficient mass transport. A hybrid bioinorganic system for CO2 reduction to CH4 is developed by coupling a new electrode architecture with enriched methanogenic community. The novel electrode design consists of porous nickel hollow fibers, which act as an inorganic electrocatalyst for hydrogen generation from proton reduction and as a gas‐transfer membrane for direct CO2 delivery to CO2‐fixing hydrogenotrophic methanogens (biological catalyst) on the cathode through the pores of the hollow fibers. These unique features of the electrode create a suitable environment for the enrichment of methanogens, which utilize the hydrogen as a source of reducing equivalents for the conversion of CO2 to CH4. The performance of the nickel electrode is tested in microbial electrosynthesis cells operated at cathode potential of −1 V versus Ag/AgCl, achieving high faradaic efficiency of 77% for CH4. The superior performance of the hybrid bioinorganic system is attributed to the electrode architecture, which provides a three‐phase boundary for gas–liquid reactions, with the reactions supported by the inorganic and biological catalysts.

Nanoparticles Self-Assembly within Lipid Bilayers.

Coarse-grained molecular dynamics simulations are used to model the self-assembly of small hydrophobic nanoparticles (NPs) within the interior of lipid bilayers. The simulation results reveal the conditions under which NPs form clusters and lattices within lipid bilayers of planar and spherical shapes, depending on the NP–lipid coupling strengths. The formation of nanopores within spherical bilayers with self-assembled planar NPs is also described. These observations can provide guidance in the preparation of functional bio-inorganic systems.

A surface-display biohybrid approach to light-driven hydrogen production in air.

Solar-to-chemical production by artificial and bioinspired photosynthetic systems is of tremendous interest to help solve current global energy and environmental problems. We developed a bioinorganic hybrid system for photocatalytic hydrogen production under aerobic conditions by combining light-harvesting semiconductors, hydrogenase catalysis, and self-aggregation of whole bacterial cells. We induced hydrogen production via self-photosynthesis in engineered Escherichia coli cells, which were originally designed for bioremediation, with in situ biosynthesis of biocompatible cadmium sulfide nanoparticles using a surface-display system. We also introduced a biomimetic silica encapsulation strategy into the engineered E. coli cells, enabling this hybrid system to continuously produce hydrogen for 96 hours, even under natural aerobic conditions. This biohybrid catalytic approach may serve as a general strategy for solar-to-chemical production.

Using porphyrin-amino acid pairs to model the electrochemistry of heme proteins: experimental and theoretical investigations.

Quasi reversibility in electrochemical cycling between different oxidation states of iron is an often seen characteristic of iron containing heme proteins that bind dioxygen. Surprisingly, the system becomes fully reversible in the bare iron-porphyrin complex: hemin. This leads to the speculation that the polypeptide bulk (globin) around the iron-porphyrin active site in these heme proteins is probably responsible for the electrochemical quasi reversibility. To understand the effect of such polypeptide bulk on iron-porphyrin, we study the interaction of specific amino acids with the hemin center in solution. We choose three representative amino acids-histidine (a well-known iron coordinator in bio-inorganic systems), tryptophan (a well-known fluoroprobe for proteins), and cysteine (a redox-active organic molecule). The interactions of these amino acids with hemin are studied using electrochemistry, spectroscopy, and density functional theory. The results indicate that among these three, the interaction of histidine with the iron center is strongest. Further, histidine maintains the electrochemical reversibility of iron. On the other hand, tryptophan and cysteine interact weakly with the iron center but disturb the electrochemical reversibility by contributing their own redox active processes to the system. Put together, this study attempts to understand the molecular interactions that can control electrochemical reversibility in heme proteins. The results obtained here from the three representative amino acids can be scaled up to build a heme-amino acid interaction database that may predict the electrochemical properties of any protein with a defined polypeptide sequence.

Inhibition of Multimolecular RNA-Protein Interactions Using Multitarget-Directed Nanohybrid System.

Multitarget-directed ligands (MTDLs) are hybrid ligands obtained by covalently linking active pharmacophores that can act on different targets. We envision that the concept of MTDLs can also be applied to supramolecular bioinorganic nanohybrid systems. Here, we report the inhibition of multimolecular RNA-protein complexes using multitarget-directed peptide-carbon nanotube hybrids (SPCHs). One of the most well-characterized and important RNA-protein interactions, a Rev-response element (RRE) RNA:Rev protein:Crm1 protein interaction system in human immunodeficiency virus type-1, was used as a model of multimolecular RNA-protein interactions. Although all previous studies have targeted only one of the interaction interfaces, that is, either the RRE:Rev interface or the RRE-Rev complex:Crm1 interface, we here have developed multitarget-directed SPCHs that could target both interfaces because the supramolecular nanosystem could be best suited for inhibiting multimolecular RNA-protein complexes that are characterized by large and complex molecular interfaces. The results showed that the single target-directed SPCHs were inhibitory to the single interface comprised only of RNA and protein in vitro, whereas multitarget-directed SPCHs were inhibitory to the multimolecular RNA-protein interfaces both in vitro and in cellulo. The MTDL nanohybrids represent a novel nanotherapeutic system that could be used to treat complex disease targets.

Synthesis of New Bioinorganic Systems Based on Nitrilium Derivatives of closo-Decaborate Anion and meso-Arylporphyrins with Pendant Amino Groups

Synthesis of New Bioinorganic Systems Based on Nitrilium Derivatives of closo-Decaborate Anion and meso-Arylporphyrins with Pendant Amino Groups

Implications of Guanidine Substitution on Copper Complexes as Entatic‐State Models

AbstractInvited for the cover of this issue is the group of Sonja Herres‐Pawlis from RWTH Aachen University, Germany. The cover image shows our entatic‐state model. The research described in the article is the result of strongly collaborative work of four groups within the interdisciplinary DFG Research Unit FOR1405 (“Dynamics of Electron Transfer Processes within Transition Metal Sites in Biological and Bioinorganic Systems”).

Computational approaches to the prediction of the redox potentials of iron and copper bioinorganic systems

AbstractAim of this contribution is to review some recent quantum mechanical approaches used to compute the redox potentials of transition metal complexes, with the emphasis on copper and iron species, which are particularly relevant in inorganic biochemistry and in synthetic chemistry of bio‐mimetic compounds. The paper presents also new DFT results obtained on Cu and Fe aquo ions in the framework of the Thermodynamic Integration and Grand Canonical Ensemble approaches. Such results show that without explicit inclusion of water molecules in the external solvation shells (even using a continuum solvation model) also very advanced methodologies fail to predict the redox potential in an acceptable manner. This is a confirmation of some previous studies which however never addressed this specific problem along the aforementioned approaches. Better results are obtained, on the contrary, on a series of Cu(II) complexes with Gly, Ala, en, Im, and water ligands with coordination type or N4. In this case, the complexes are surrounded by nine water molecules which may partially alleviate the inadequacy of the continuum solvent models, especially in the case of highly positively charged species.

Decoupling and elucidation of surface-driven processes during inorganic mineralization on virus templates

There is a lack of fundamental information about the molecular processes governing biomineralization of inorganic materials to produce nanostructures on biological templates. This information is essential for the directed synthesis of high quality nanomaterials via biotemplating. We characterized palladium (Pd) mineralization via the individual adsorption, reduction, and nanocrystal growth processes, which simultaneously occur during the hydrothermal synthesis on the Tobacco mosaic virus (TMV). The adsorption of precursor and reduction of palladium were decoupled through UV–vis Spectroscopy and in situ X-ray absorption spectroscopy studies. The role of additional cysteine (Cys) residues, ionic strength, and coating density on the fundamental parameters describing these processes were quantitatively evaluated. Primary nanocrystal growth and structural orientation of Pd nanoparticles was characterized using in situ small angle X-ray scattering. The adsorption, reduction of Pd species, and nanocrystal sizes were significantly changed on addition of Cys residues to the amino terminus of the TMV coat protein. Reduction of Pd on an already coated virion was dependent on the Pd surface area, and was hindered by the presence of residual salt. Furthermore, trends in Pd adsorption intensity and capacity suggested that chloride ions affected the adsorption equilibrium. Application of this fundamental approach with further optimization of parameters dictating biomineralization would facilitate directed synthesis and scale up of bioinorganic systems.

Photosynthetic conversion of CO2 to acetic acid by an inorganic-biological hybrid system

Recent work by Sakimoto et al. has adopted such an approach by inducing the bacterium Moorella thermoacetica (M. thermoacetica) to precipitate and decorate itself with cadmium sulfide nanoparticles. This cyborgian bacteria, M. thermoacetica-CdS, when illuminated by sunlight, is able to use the photogenerated electrons to reduce CO2 into acetic acid with exceedingly high quantum efficiencies. While many synthetic CO2 reducing catalysts can achieve high efficiencies in converting to C1 products (such as methane, carbon monoxide, formic acid, etc.), this C2 product holds great promise as a non-volatile, non-toxic intermediate that could serve as a biofeedstock commodity chemical, ready to be upgraded to a variety of biofuels, biopolymers, and pharmaceutical precursors. This first generation system opens up a new parameter space to investigate such bio-inorganic hybrid systems: biosynthesizing smaller band gap semiconductors to increase light absorption and energy conversion efficiency, genetic engineering to produce more complicated organic molecules, and more.

Scalable improvement of SPME multipolar electrostatics in anisotropic polarizable molecular mechanics using a general short-range penetration correction up to quadrupoles.

We propose a general coupling of the Smooth Particle Mesh Ewald SPME approach for distributed multipoles to a short-range charge penetration correction modifying the charge-charge, charge-dipole and charge-quadrupole energies. Such an approach significantly improves electrostatics when compared to ab initio values and has been calibrated on Symmetry-Adapted Perturbation Theory reference data. Various neutral molecular dimers have been tested and results on the complexes of mono- and divalent cations with a water ligand are also provided. Transferability of the correction is adressed in the context of the implementation of the AMOEBA and SIBFA polarizable force fields in the TINKER-HP software. As the choices of the multipolar distribution are discussed, conclusions are drawn for the future penetration-corrected polarizable force fields highlighting the mandatory need of non-spurious procedures for the obtention of well balanced and physically meaningful distributed moments. Finally, scalability and parallelism of the short-range corrected SPME approach are addressed, demonstrating that the damping function is computationally affordable and accurate for molecular dynamics simulations of complex bio- or bioinorganic systems in periodic boundary conditions.

Thermodynamic and Structural Investigation of Synthetic Actinide-Peptide Scaffolds.

The complexation of uranium and europium, in oxidation states +VI and +III, respectively, was investigated with pertinent bio-inorganic systems. Three aspartate-rich pentapeptides with different structural properties were selected for study to rationalize the structure-affinity relationships. Thermodynamic results, crosschecked by both isothermal titration calorimetry and time-resolved laser fluorescence spectroscopy, showed different affinity depending on the peptide for both Eu(III) and U(VI). The thermodynamic aspects were correlated to structural predictions, which were acquired by density functional theory quantum chemical calculations and from IR and extended X-ray absorption fine structure experiments. The combination of these microscopic properties revealed that carbonyl-metal interactions affected the entropy in the case of europium, while the larger uranyl cation was mostly affected by preorganization and steric effects, so that the affinity was enhanced through enthalpy. The approach described here revealed various microscopic aspects governing peptide actinide affinity. Highlighting these mechanisms should certainly contribute to the rational synthesis of higher affinity biomimetic aspartic ligands.

Cobalt Kβ valence-to-core X-ray emission spectroscopy: a study of low-spin octahedral cobalt(iii) complexes.

Kβ valence-to-core (V2C) X-emission spectroscopy (XES) has gained prominence as a tool for molecular inorganic chemists to probe the occupied valence orbitals of coordination complexes, as illustrated by recent evaluation of Kβ V2C XES ranging from titanium to iron. However, cobalt Kβ V2C XES has not been studied in detail, limiting the application of this technique to probe cobalt coordination in molecular catalysts and bioinorganic systems. In addition, the community still lacks a complete understanding of all factors that dictate the V2C peak area. In this manuscript, we report experimental cobalt Kβ V2C XES spectra of low-spin octahedral Co(iii) complexes with different ligand donors, in conjunction with DFT calculations. Cobalt Kβ V2C XES was demonstrated to be sensitive to cobalt-ligand coordination environments. Notably, we recognize here for the first time that there is a linear correlation between the V2C area and the spectrochemical series for low-spin octahedral cobalt(iii) complexes, with strong field π acceptor ligands giving rise to the largest V2C area. This unprecedented correlation is explained by invoking different levels of π-interaction between cobalt p orbitals and ligand orbitals that modulate the percentage of cobalt p orbital character in donor MOs, in combination with changes in the average cobalt-ligand distance.

Novel biohybrids of layered double hydroxide and lactate dehydrogenase enzyme: Synthesis, characterization and catalytic activity studies

The present work introduces new biohybrid materials involving layered double hydroxides (LDH) and biomolecule such as enzyme to produce bioinorganic system. Lactate dehydrogenase (Lac Deh) has been chosen as a model enzyme, being immobilized onto MgAl and ZnAl LDH materials via direct ion-exchange (adsorption) and co-precipitation methods. The immobilization efficiency was largely dependent upon the immobilization methods. A comparative study shows that the co-precipitation method favors the immobilization of great and tunable amount of enzyme. The structural behavior, chemical bonding composition and morphology of the resulting biohybrids were determined by X-ray diffraction (XRD) study, Fourier transform infrared (FTIR) spectroscopy and transmission electron microscopy (TEM), respectively. The free and immobilized enzyme activity and kinetic parameters were also reported using UV–Visible spectroscopy. However, the modified LDH materials showed a decrease in crystallinity as compared to the unmodified LDH. The change in activity of the immobilized lactate dehydrogenase was considered to be due, to the reduced accessibility of substrate molecules to the active sites of the enzyme and the partial conformational change of the Lac Deh molecules as a result of the immobilization way. Finally, it was proven that there is a correlation between structure/microstructure and enzyme activity dependent on the immobilization process.

Reactivity of the binuclear non-heme iron active site of Δ⁹ desaturase studied by large-scale multireference ab initio calculations.

The results of density matrix renormalization group complete active space self-consistent field (DMRG-CASSCF) and second-order perturbation theory (DMRG-CASPT2) calculations are presented on various structural alternatives for the O-O and first C-H activating step of the catalytic cycle of the binuclear nonheme iron enzyme Δ(9) desaturase. This enzyme is capable of inserting a double bond into an alkyl chain by double hydrogen (H) atom abstraction using molecular O2. The reaction step studied here is presumably associated with the highest activation barrier along the full pathway; therefore, its quantitative assessment is of key importance to the understanding of the catalysis. The DMRG approach allows unprecedentedly large active spaces for the explicit correlation of electrons in the large part of the chemically important valence space, which is apparently conditio sine qua non for obtaining well-converged reaction energetics. The derived reaction mechanism involves protonation of the previously characterized 1,2-μ peroxy Fe(III)Fe(III) (P) intermediate to a 1,1-μ hydroperoxy species, which abstracts an H atom from the C10 site of the substrate. An Fe(IV)-oxo unit is generated concomitantly, supposedly capable of the second H atom abstraction from C9. In addition, several popular DFT functionals were compared to the computed DMRG-CASPT2 data. Notably, many of these show a preference for heterolytic C-H cleavage, erroneously predicting substrate hydroxylation. This study shows that, despite its limitations, DMRG-CASPT2 is a significant methodological advancement toward the accurate computational treatment of complex bioinorganic systems, such as those with the highly open-shell diiron active sites.

Study of iron dimers reveals angular dependence of valence-to-core X-ray emission spectra.

Transition-metal Kβ X-ray emission spectroscopy (XES) is a developing technique that probes the occupied molecular orbitals of a metal complex. As an element-specific probe of metal centers, Kβ XES is finding increasing applications in catalytic and, in particular, bioinorganic systems. For the continued development of XES as a probe of these complex systems, however, the full range of factors which contribute to XES spectral modulations must be explored. In this report, an investigation of a series of oxo-bridged iron dimers reveals that the intensity of valence-to-core features is sensitive to the Fe–O–Fe bond angle. The intensity of these features has a well-known dependence on metal–ligand bond distance, but a dependence upon bond angle has not previously been documented. Herein, we explore the angular dependence of valence-to-core XES features both experimentally and computationally. Taken together, these results show that, as the Fe–O–Fe angle decreases, the intensity of the Kβ″ feature increases and that this effect is modulated by increasing amounts of Fe np mixing into the O 2s orbital at smaller bond angles. The relevance of these findings to the identification of oxygenated intermediates in bioinorganic systems is highlighted, with special emphasis given to the case of soluble methane monooxygenase.

Single-Molecule Dynamics and Mechanisms of Metalloregulators and Metallochaperones

Understanding how cells regulate and transport metal ions is an important goal in the field of bioinorganic chemistry, a frontier research area that resides at the interface of chemistry and biology. This Current Topic reviews recent advances from the authors' group in using single-molecule fluorescence imaging techniques to identify the mechanisms of metal homeostatic proteins, including metalloregulators and metallochaperones. It emphasizes the novel mechanistic insights into how dynamic protein-DNA and protein-protein interactions offer efficient pathways via which MerR-family metalloregulators and copper chaperones can fulfill their functions. This work also summarizes other related single-molecule studies of bioinorganic systems and provides an outlook toward single-molecule imaging of metalloprotein functions in living cells.

Quantum chemical study of the catalytic activation of methane by copper oxide and copper hydroxide cations

The activation of methane and its subsequent conversion into more valuable feedstocks under ambient conditions are regarded as one of the major challenges in contemporary catalysis, due to its thermodynamically strong and kinetically inert C-H bond. Several enzymes and synthetic bioinorganic systems perform the activation of C-H bonds in methane and small hydrocarbons, mediated by transition metal mononuclear centers. Among them, monocopper cores and, in particular, CuO(+) and CuOH(+) have been suggested as efficient catalytic centers; this activity has not been experimentally proven until very recently, mainly due to the difficulty to produce sufficient amounts of active species to demonstrate the bond activation processes. The theoretical study presented here provides a thorough quantum chemical description of the activity of both species, together with molecular level insight into the elementary steps of the experimentally observed reactions. Post-HF (CCSD(T), CASPT2) and Density Functional Theory (DFT) methods have been used to unravel detailed electronic and mechanistic aspects of the reaction paths. Our study reveals the decisive role of the oxygen-centered radical in the reactivity of both species, and the improvement of the reactivity as a result of the protonation of the active species.

ChemInform Abstract: Applications of High‐Resolution 1H Solid‐State NMR

AbstractReview: 310 refs.

Theoretical calculations of physico-chemical and spectroscopic properties of bioinorganic systems: current limits and perspectives

In the last decade, we have witnessed substantial progress in the development of quantum chemical methodologies. Simultaneously, robust solvation models and various combined quantum and molecular mechanical (QM/MM) approaches have become an integral part of quantum chemical programs. Along with the steady growth of computer power and, more importantly, the dramatic increase of the computer performance to price ratio, this has led to a situation where computational chemistry, when exercised with the proper amount of diligence and expertise, reproduces, predicts, and complements the experimental data. In this perspective, we review some of the latest achievements in the field of theoretical (quantum) bioinorganic chemistry, concentrating mostly on accurate calculations of the spectroscopic and physico-chemical properties of open-shell bioinorganic systems by wave-function (ab initio) and DFT methods. In our opinion, the one-to-one mapping between the calculated properties and individual molecular structures represents a major advantage of quantum chemical modelling since this type of information is very difficult to obtain experimentally. Once (and only once) the physico-chemical, thermodynamic and spectroscopic properties of complex bioinorganic systems are quantitatively reproduced by theoretical calculations may we consider the outcome of theoretical modelling, such as reaction profiles and the various decompositions of the calculated parameters into individual spatial or physical contributions, to be reliable. In an ideal situation, agreement between theory and experiment may imply that the practical problem at hand, such as the reaction mechanism of the studied metalloprotein, can be considered as essentially solved.