Carolyn I. Pearce

Microbial engineering of nanoheterostructures: Biological synthesis of a magnetically recoverable palladium nanocatalyst

Precious metals supported on ferrimagnetic particles have a diverse range of uses in catalysis. However, fabrication using synthetic methods results in potentially high environmental and economic costs. Here we show a novel biotechnological route for the synthesis of a heterogeneous catalyst consisting of reactive palladium nanoparticles arrayed on a nanoscale biomagnetite support. The magnetic support was synthesized at ambient temperature by the Fe(III)-reducing bacterium, Geobacter sulfurreducens , and facilitated ease of recovery of the catalyst with superior performance due to reduced agglomeration (versus conventional colloidal Pd nanoparticles). Surface arrays of palladium nanoparticles were deposited on the nanomagnetite using a simple one-step method without the need to modify the biomineral surface, most likely due to an organic coating priming the surface for Pd adsorption, which was produced by the bacterial culture during the formation of the nanoparticles. A combination of EXAFS and XPS showed the Pd nanoparticles on the magnetite to be predominantly metallic in nature. The Pd(0)-biomagnetite was tested for catalytic activity in the Heck reaction coupling iodobenzene to ethyl acrylate or styrene. Rates of reaction were equal to or superior to those obtained with an equimolar amount of a commercial colloidal palladium catalyst, and near complete conversion to ethyl cinnamate or stilbene was achieved within 90 and 180 min, respectively.

Microbial manufacture of chalcogenide-based nanoparticles via the reduction of selenite using Veillonella atypica: an in situ EXAFS study.

The ability of metal-reducing bacteria to produce nanoparticles, and their precursors, can be harnessed for the biological manufacture of fluorescent, semiconducting nanomaterials. The anaerobic bacterium Veillonella atypica can reduce selenium oxyanions to form nanospheres of elemental selenium. These selenium nanospheres are then further reduced by the bacterium to form reactive selenide which could be precipitated with a suitable metal cation to produce nanoscale chalcogenide precipitates, such as zinc selenide, with optical and semiconducting properties. The whole cells used hydrogen as the electron donor for selenite reduction and an enhancement of the reduction rate was observed with the addition of a redox mediator (anthraquinone disulfonic acid). A novel synchrotron-based in situ time-resolved x-ray absorption spectroscopy technique was used, in conjunction with ion chromatography and inductively coupled plasma-atomic emission spectroscopy, to study the mechanisms and kinetics of the microbial reduction of selenite to selenide. The products of this biotransformation were also assessed using electron microscopy, energy-dispersive spectroscopy, x-ray diffraction and fluorescence spectroscopy. This process offers the potential to prepare chalcogenide-based nanocrystals, for application in optoelectronic devices and biological labelling, from more environmentally benign precursors than those used in conventional organometallic synthesis.

Redox cycling of Fe(II) and Fe(III) in magnetite by Fe-metabolizing bacteria

Building a biogeochemical battery Iron acts as both a source and sink of electrons for microorganisms in the environment. Some anaerobic bacteria use oxidized Fe(III) as an electron acceptor, whereas phototrophic bacteria can use reduced Fe(II) as an electron donor. Byrne et al. show that the iron-bearing mineral magnetite, which contains both Fe(II) and Fe(III), can serve as both an electron acceptor and donor. Cocultures of iron-reducing and iron-oxidizing bacteria exposed to simulated day/night cycles or changes in organic matter altered the ratio of Fe(II) to Fe(III) in magnetite particles. Science, this issue p. 1473 Magnetite can serve as both an electron donor and acceptor for cocultures of iron-metabolizing bacteria. Microorganisms are a primary control on the redox-induced cycling of iron in the environment. Despite the ability of bacteria to grow using both Fe(II) and Fe(III) bound in solid-phase iron minerals, it is currently unknown whether changing environmental conditions enable the sharing of electrons in mixed-valent iron oxides between bacteria with different metabolisms. We show through magnetic and spectroscopic measurements that the phototrophic Fe(II)-oxidizing bacterium Rhodopseudomonas palustris TIE-1 oxidizes magnetite (Fe3O4) nanoparticles using light energy. This process is reversible in co-cultures by the anaerobic Fe(III)-reducing bacterium Geobacter sulfurreducens. These results demonstrate that Fe ions bound in the highly crystalline mineral magnetite are bioavailable as electron sinks and electron sources under varying environmental conditions, effectively rendering magnetite a naturally occurring battery.

Direct determination of cation site occupancies in natural ferrite spinels by L2,3 X-ray absorption spectroscopy and X-ray magnetic circular dichroism

Abstract Cation distributions in natural ferrite spinels, some containing large amounts of Mg, Ti, Mn, and Zn, have been investigated using the element-, site-, and symmetry-selective spectroscopic techniques of L2,3 X-ray absorption spectroscopy (XAS) and X-ray magnetic circular dichroism (XMCD). By comparing XMCD data with calculated spectra, the site occupancies of the Fe cations have been determined. From the analysis of natural ferrite spinels with formulae very close to that of pure magnetite (Fe3O4), a standard XMCD spectrum for natural magnetite is proposed. Magnetites with small numbers of cation vacancies due to oxidation (solid solutions with maghemite, γ-Fe2O3) show that all the vacancies occur in octahedral sites. Ti L2,3 XAS of oxidized Ti-bearing magnetites (hereafter referred to titanomagnetites) shows that Ti is tetravalent occurring on the octahedral site with 10Dq ~2eV; Fe L2,3 XMCD spectra indicate that the vacancies occur in both tetrahedral and octahedral sites. Mn L2,3 XAS of the Mn-rich ferrite spinels shows that Mn is predominantly ordered onto the tetrahedral site with an Mn2+:Mn3+ ratio of 0.85:0.15. Mn- and Zn-rich ferrite spinels have an excess of cations over 3.0 per 4-oxygen formula unit. The sign of the XMCD for Mn corresponds to a parallel alignment of the Mn moments with the Fe3+ moments in the tetrahedral sublattice. This work demonstrates clearly that combined XAS and XMCD provides direct information on the distribution of multivalent cations in chemically complex magnetic spinels.

Investigating different mechanisms for biogenic selenite transformations: Geobacter sulfurreducens, Shewanella oneidensis and Veillonella atypica

The metal‐reducing bacteria Geobacter sulfurreducens, Shewanella oneidensis and Veillonella atypica, use different mechanisms to transform toxic, bioavailable sodium selenite to less toxic, non‐mobile elemental selenium and then to selenide in anaerobic environments, offering the potential for in situ and ex situ bioremediation of contaminated soils, sediments, industrial effluents, and agricultural drainage waters. The products of these reductive transformations depend on both the organism involved and the reduction conditions employed, in terms of electron donor and exogenous extracellular redox mediator. The intermediary phase involves the precipitation of elemental selenium nanospheres and the potential role of proteins in the formation of these structures is discussed. The bionanomineral phases produced during these transformations, including both elemental selenium nanospheres and metal selenide nanoparticles, have catalytic, semiconducting and light‐emitting properties, which may have unique applications in the realm of nanophotonics. This research offers the potential to combine remediation of contaminants with the development of environmentally friendly manufacturing pathways for novel bionanominerals.

Probing the site occupancies of Co-, Ni-, and Mn-substituted biogenic magnetite using XAS and XMCD

Abstract Ferrimagnetic nanoparticles have many uses in industry including in magnetic recording media and transformers, however these particles are often expensive to synthesize. In this study, the Fe3+- reducing bacteria Geobacter sulfurreducens and Shewanella oneidensis were used to synthesize spinel ferrite nanoparticles of the general chemical formula MxFe3-xO4, where M is either Co, Ni, Mn, Zn, or a combination of Mn and Zn. This was done at ambient temperatures through the dissimilatory reduction of Fe3+-oxyhydroxides containing the appropriate substitutional cations. A combination of L-edge and K-edge X-ray absorption spectroscopy (XAS) and L-edge X-ray magnetic circular dichroism (XMCD) was used to determine the site occupancies, valence, and local structure of the Fe and substitutional cations within the spinels. The Ni and Co ferrites produced using each bacterium were very similar and therefore this study concludes that, despite the difference in reduction mechanism of the bacteria used, the end-product is remarkably unaltered. Nickel ferrites contained only Ni2+, with at least 80% in Oh coordination. Cobalt ferrites contained only Co2+ but with a significant proportion (up to 45%) in Td coordination, showing a slight preference for Td sites. The Mn-ferrites contained Mn2+ only on the Oh sites but a mixture of Mn2+ and Mn3+ on Td sites when the amount of Mn exceeded 3% (compared to the amount of Fe) or some Zn was also present. This study successfully produced a range of nanoparticulate ferrites that could be produced industrially using relatively environmentally benign methodologies.

Cation site occupancy of biogenic magnetite compared to polygenic ferrite spinels determined by X-ray magnetic circular dichroism

Ferrite spinels, especially magnetite (Fe3O4), can be formed either by geological, biological or chemical processes leading to chemically similar phases that show different physical characteristics. We compare, for the first time, magnetite produced by these three different methods using X-ray magnetic circular dichroism (XMCD), a synchrotron radiation based technique able to determine the site occupancy of Fe cations in the ferrite spinels. Extracellular nanoscale magnetite produced by different Fe(Ill)reducing bacteria was shown to have different degrees of stoichiometry depending on the bacteria and the method of formation, but all were oxygen deficient due to formation under anoxic conditions. Intracellular nano-magnetite synthesized in the magnetosomes of magnetotactic bacteria was found to have a Fe cation site occupancy ratio most similar to stoichiometric magnetite, possibly due to the tight physiological controls exerted by the magnetosome membrane. Chemically-synthesised nano-magnetite and bulk magnetite produced as a result of geological processes were both found to be cation deficient with a composition between magnetite and maghemite (oxidised magnetite).

Fe site occupancy in magnetite-ulvöspinel solid solutions: A new approach using X-ray magnetic circular dichroism

Abstract Ordering of Fe3+ and Fe2+ cations between octahedral and tetrahedral sites in synthetic members of the magnetite-ulvöspinel (Fe3O4-Fe2TiO4) solid-solution series was determined using Fe L2,3-edge X-ray magnetic circular dichroism (XMCD) coupled with electron microprobe and chemical analysis, Ti L2,3-edge and Fe K-edge X-ray absorption spectroscopy (XAS), and unit-cell parameters. Microprobe analyses, cell edges, and chemical FeO determinations showed that bulk compositions were stoichiometric magnetite-ulvöspinel solid solutions. XMCD showed that the surface was sensitive to redox conditions, and samples required re-equilibration with solid-solid buffers. Detailed site-occupancy analysis gave Fe2+/Fe3+ XMCD-intensity ratios close to stoichiometric values. L2,3-edge XAS confirmed that Ti4+ was restricted to octahedral sites. XMCD showed that significant Fe2+ only entered the tetrahedral sites when Ti content was >0.40 atoms per formula unit (apfu), whereas Fe2+ in octahedral sites increased from 1 apfu in magnetite to a maximum of ~1.4 apfu when Ti content was 0.45 apfu. As Ti content increased, a steady increase in Fe2+ in tetrahedral sites was observable in the XMCD spectra, concurrent with a slow decrease in Fe2+ in octahedral sites. Calculated magnetic moments decreased rapidly from magnetite (4.06 μB) to USP45 (1.5 μB), then more slowly toward ulvöspinel (0 μB). Two synthesized samples were maghemitized by re-equilibrating with an oxidizing buffer. XMCD showed that Fe2+ oxidation, with concomitant vacancy formation, was restricted to octahedral sites. Through the direct measurement of Fe oxidation states, XMCD results can be used to rationalize the magnetic properties of titanomagnetites, along with oxidized titanomaghemitized analogs, in Earth’s crustal rocks.

Biomineralization: linking the fossil record to the production of high value functional materials

The microbial cell offers a highly efficient template for the formation of nanoparticles with interesting properties including high catalytic, magnetic and light-emitting activities. Thus biomineralization products are not only important in global biogeochemical cycles, but they also have considerable commercial potential, offering new methods for material synthesis that eliminate toxic organic solvents and minimize expensive high-temperature and pressure processing steps. In this review we describe a range of bacterial processes that can be harnessed to make precious metal catalysts from waste streams, ferrite spinels for biomedicine and catalysis, metal phosphates for environmental remediation and biomedical applications, and biogenic selenides for a range of optical devices. Recent molecular-scale studies have shown that the structure and properties of bionanominerals can be fine-tuned by subtle manipulations to the starting materials and to the genetic makeup of the cell. This review is dedicated to the late Terry Beveridge who contributed much to the field of biomineralization, and provided early models to rationalize the mechanisms of biomineral synthesis, including those of geological and commercial potential.

Synthesis and properties of titanomagnetite (Fe3-xTixO4) nanoparticles: A tunable solid-state Fe(II/III) redox system

Titanomagnetite (Fe(3-x)Ti(x)O(4)) nanoparticles were synthesized by room temperature aqueous precipitation, in which Ti(IV) replaces Fe(III) and is charge compensated by conversion of Fe(III) to Fe(II) in the unit cell. A comprehensive suite of tools was used to probe composition, structure, and magnetic properties down to site-occupancy level, emphasizing distribution and accessibility of Fe(II) as a function of x. Synthesis of nanoparticles in the range 0≤x≤0.6 was attempted; Ti, total Fe and Fe(II) content were verified by chemical analysis. TEM indicated homogeneous spherical 9-12 nm particles. μ-XRD and Mössbauer spectroscopy on anoxic aqueous suspensions verified the inverse spinel structure and Ti(IV) incorporation in the unit cell up to x≤0.38, based on Fe(II)/Fe(III) ratio deduced from the unit cell edge and Mössbauer spectra. Nanoparticles with a higher value of x possessed a minor amorphous secondary Fe(II)/Ti(IV) phase. XANES/EXAFS indicated Ti(IV) incorporation in the octahedral sublattice (B-site) and proportional increases in Fe(II)/Fe(III) ratio. XA/XMCD indicated that increases arise from increasing B-site Fe(II), and that these charge-balancing equivalents segregate to those B-sites near particle surfaces. Dissolution studies showed that this segregation persists after release of Fe(II) into solution, in amounts systematically proportional to x and thus the Fe(II)/Fe(III) ratio. A mechanistic reaction model was developed entailing mobile B-site Fe(II) supplying a highly interactive surface phase that undergoes interfacial electron transfer with oxidants in solution, sustained by outward Fe(II) migration from particle interiors and concurrent inward migration of charge-balancing cationic vacancies in a ratio of 3:1.