Samuel M. Webb

A Bacterium That Can Grow by Using Arsenic Instead of Phosphorus

Evidence is offered for arsenate replacing phosphate as a molecular building block in a Mono Lake, California, bacterium. Life is mostly composed of the elements carbon, hydrogen, nitrogen, oxygen, sulfur, and phosphorus. Although these six elements make up nucleic acids, proteins, and lipids and thus the bulk of living matter, it is theoretically possible that some other elements in the periodic table could serve the same functions. Here, we describe a bacterium, strain GFAJ-1 of the Halomonadaceae, isolated from Mono Lake, California, that is able to substitute arsenic for phosphorus to sustain its growth. Our data show evidence for arsenate in macromolecules that normally contain phosphate, most notably nucleic acids and proteins. Exchange of one of the major bio-elements may have profound evolutionary and geochemical importance.

In Situ X-ray Absorption Spectroscopy Investigation of a Bifunctional Manganese Oxide Catalyst with High Activity for Electrochemical Water Oxidation and Oxygen Reduction

In situ X-ray absorption spectroscopy (XAS) is a powerful technique that can be applied to electrochemical systems, with the ability to elucidate the chemical nature of electrocatalysts under reaction conditions. In this study, we perform in situ XAS measurements on a bifunctional manganese oxide (MnOx) catalyst with high electrochemical activity for the oxygen reduction reaction (ORR) and the oxygen evolution reaction (OER). Using X-ray absorption near edge structure (XANES) and extended X-ray absorption fine structure (EXAFS), we find that exposure to an ORR-relevant potential of 0.7 V vs RHE produces a disordered Mn3(II,III,III)O4 phase with negligible contributions from other phases. After the potential is increased to a highly anodic value of 1.8 V vs RHE, relevant to the OER, we observe an oxidation of approximately 80% of the catalytic thin film to form a mixed Mn(III,IV) oxide, while the remaining 20% of the film consists of a less oxidized phase, likely corresponding to unchanged Mn3(II,III,III)O4. XAS and electrochemical characterization of two thin film catalysts with different MnOx thicknesses reveals no significant influence of thickness on the measured oxidation states, at either ORR or OER potentials, but demonstrates that the OER activity scales with film thickness. This result suggests that the films have porous structure, which does not restrict electrocatalysis to the top geometric layer of the film. As the portion of the catalyst film that is most likely to be oxidized at the high potentials necessary for the OER is that which is closest to the electrolyte interface, we hypothesize that the Mn(III,IV) oxide, rather than Mn3(II,III,III)O4, is the phase pertinent to the observed OER activity.

Structural characterization of biogenic Mn oxides produced in seawater by the marine bacillus sp. strain SG-1

Abstract Natural Mn-oxide nanoparticles and grain coatings are ubiquitous in the environment and profoundly impact the water quality and quality of sediments through their ability to degrade and sequester contaminants. These oxides, which are believed to form dominantly via oxidation of Mn2+ by marine and freshwater bacteria, have extremely high sorptive capacities for heavy metals. We have used XANES, EXAFS, and synchrotron (SR)-XRD techniques to study biogenic Mn oxides produced by spores of the marine Bacillus sp. strain SG-1 in seawater as a function of reaction time under in-situ conditions. An EXAFS model was developed to fully account for the structure and features in the data, providing realistic structural information. The first observed biogenic solid-phase Mn-oxide product is a layered phyllomanganate with hexagonal sheet symmetry and an Mn-oxidation state similar to that in δ-MnO2, between 3.7 and 4.0. XRD and SEM-EDS data show the biooxides to have a phyllomanganate 10 Å basal plane spacing and an interlayer containing Ca. With time, a phyllomanganate oxide with pseudo-orthogonal sheet symmetry appears. Fits to these EXAFS spectra suggest the octahedral layers have relatively few Mn octahedral site vacancies in the lattice and the layers bend to accommodate Jahn-Teller distortions creating the change in symmetry. A reaction mechanism is proposed to account for the observed products. The phyllomanganate oxides observed in this study may be the same as the most abundant Mn-oxide phases suspended in the oxic and sub-oxic zones of the oceanic water column that are of global importance in trace metal and nutrient cycling

Biotic and abiotic products of Mn(II) oxidation by spores of the marine Bacillus sp. strain SG-1

Abstract Bacterial Mn(II) oxidization by spores of Bacillus, sp. strain SG-1 has been systematically probed over the time scale 0.22 to 77 days under in-situ conditions and at differing Mn(II) concentrations. Three complementary techniques, K-edge X-ray absorption near-edge spectroscopy (XANES), X-ray emission spectroscopy (XES), and in-situ synchrotron radiation-based X-ray diffraction (SR-XRD), have been utilized to examine time-dependent changes in Mn oxidation state, local-, and long-range structure in amorphous, crystalline, cell-bound, and solute Mn species. The primary solid biogenic product of Mn(II) oxidation is an X-ray amorphous oxide similar to δ-MnO2, which has a Mn oxidation state between 3.7 and 4.0. Reaction of Mn(II) with the primary biogenic oxide results in the production of abiotic secondary products, feitknechtite or a 10 Å Na phyllomanganate. The identity of the secondary product depends upon the Mn(II) concentration as described by thermodynamic relations. A decrease in the dissolved Mn(II) concentration is followed by mineralogic transformation of the secondary products. Thus, Mn(II) appears to act as a reductant toward the biogenic oxide and to control the stability of secondary reaction products. Mineralogic changes similar to these are likely to be commonplace in natural settings where bacterial Mn(II) oxidation is occurring and may liberate sorbed metal ions or alter the rates of important Mn oxide surface-mediated processes such as the degradation of organic molecules. It is plausible that microbes may exploit such mineral transformation reactions to indirectly control specific chemical conditions in the vicinity of the cell.

Uranium redox transition pathways in acetate-amended sediments

Redox transitions of uranium [from U(VI) to U(IV)] in low-temperature sediments govern the mobility of uranium in the environment and the accumulation of uranium in ore bodies, and inform our understanding of Earth’s geochemical history. The molecular-scale mechanistic pathways of these transitions determine the U(IV) products formed, thus influencing uranium isotope fractionation, reoxidation, and transport in sediments. Studies that improve our understanding of these pathways have the potential to substantially advance process understanding across a number of earth sciences disciplines. Detailed mechanistic information regarding uranium redox transitions in field sediments is largely nonexistent, owing to the difficulty of directly observing molecular-scale processes in the subsurface and the compositional/physical complexity of subsurface systems. Here, we present results from an in situ study of uranium redox transitions occurring in aquifer sediments under sulfate-reducing conditions. Based on molecular-scale spectroscopic, pore-scale geochemical, and macroscale aqueous evidence, we propose a biotic–abiotic transition pathway in which biomass-hosted mackinawite (FeS) is an electron source to reduce U(VI) to U(IV), which subsequently reacts with biomass to produce monomeric U(IV) species. A species resembling nanoscale uraninite is also present, implying the operation of at least two redox transition pathways. The presence of multiple pathways in low-temperature sediments unifies apparently contrasting prior observations and helps to explain sustained uranium reduction under disparate biogeochemical conditions. These findings have direct implications for our understanding of uranium bioremediation, ore formation, and global geochemical processes.

Trace Metals as Biomarkers for Eumelanin Pigment in the Fossil Record

X-ray maps of fossil feather pigments reveal color patterning in extinct bird species. Well-preserved fossils of pivotal early bird and nonavian theropod species have provided unequivocal evidence for feathers and/or downlike integuments. Recent studies have reconstructed color on the basis of melanosome structure; however, the chemistry of these proposed melanosomes has remained unknown. We applied synchrotron x-ray techniques to several fossil and extant organisms, including Confuciusornis sanctus, in order to map and characterize possible chemical residues of melanin pigments. Results show that trace metals, such as copper, are present in fossils as organometallic compounds most likely derived from original eumelanin. The distribution of these compounds provides a long-lived biomarker of melanin presence and density within a range of fossilized organisms. Metal zoning patterns may be preserved long after melanosome structures have been destroyed.

Manganese-oxidizing photosynthesis before the rise of cyanobacteria

The emergence of oxygen-producing (oxygenic) photosynthesis fundamentally transformed our planet; however, the processes that led to the evolution of biological water splitting have remained largely unknown. To illuminate this history, we examined the behavior of the ancient Mn cycle using newly obtained scientific drill cores through an early Paleoproterozoic succession (2.415 Ga) preserved in South Africa. These strata contain substantial Mn enrichments (up to ∼17 wt %) well before those associated with the rise of oxygen such as the ∼2.2 Ga Kalahari Mn deposit. Using microscale X-ray spectroscopic techniques coupled to optical and electron microscopy and carbon isotope ratios, we demonstrate that the Mn is hosted exclusively in carbonate mineral phases derived from reduction of Mn oxides during diagenesis of primary sediments. Additional observations of independent proxies for O2—multiple S isotopes (measured by isotope-ratio mass spectrometry and secondary ion mass spectrometry) and redox-sensitive detrital grains—reveal that the original Mn-oxide phases were not produced by reactions with O2, which points to a different high-potential oxidant. These results show that the oxidative branch of the Mn cycle predates the rise of oxygen, and provide strong support for the hypothesis that the water-oxidizing complex of photosystem II evolved from a former transitional photosystem capable of single-electron oxidation reactions of Mn.

Mn(II) oxidation by an ascomycete fungus is linked to superoxide production during asexual reproduction

Manganese (Mn) oxides are among the most reactive minerals within the environment, where they control the bioavailability of carbon, nutrients, and numerous metals. Although the ability of microorganisms to oxidize Mn(II) to Mn(III/IV) oxides is scattered throughout the bacterial and fungal domains of life, the mechanism and physiological basis for Mn(II) oxidation remains an enigma. Here, we use a combination of compound-specific chemical assays, microspectroscopy, and electron microscopy to show that a common Ascomycete filamentous fungus, Stilbella aciculosa, oxidizes Mn(II) to Mn oxides by producing extracellular superoxide during cell differentiation. The reactive Mn oxide phase birnessite and the reactive oxygen species superoxide and hydrogen peroxide are colocalized at the base of asexual reproductive structures. Mn oxide formation is not observed in the presence of superoxide scavengers (e.g., Cu) and inhibitors of NADPH oxidases (e.g., diphenylene iodonium chloride), enzymes responsible for superoxide production and cell differentiation in fungi. Considering the recent identification of Mn(II) oxidation by NADH oxidase-based superoxide production by a common marine bacterium (Roseobacter sp.), these results introduce a surprising homology between some prokaryotic and eukaryotic organisms in the mechanisms responsible for Mn(II) oxidation, where oxidation appears to be a side reaction of extracellular superoxide production. Given the versatility of superoxide as a redox reactant and the widespread ability of fungi to produce superoxide, this microbial extracellular superoxide production may play a central role in the cycling and bioavailability of metals (e.g., Hg, Fe, Mn) and carbon in natural systems.

Nonreductive Biomineralization of Uranium(VI) Phosphate Via Microbial Phosphatase Activity in Anaerobic Conditions

The remediation of uranium from soils and groundwater at Department of Energy (DOE) sites across the United States represents a major environmental issue, and bioremediation has exhibited great potential as a strategy to immobilize U in the subsurface. The bioreduction of U(VI) to insoluble U(IV) uraninite has been proposed to be an effective bioremediation process in anaerobic conditions. However, high concentrations of nitrate and low pH found in some contaminated areas have been shown to limit the efficiency of microbial reduction of uranium. In the present study, nonreductive uranium biomineralization promoted by microbial phosphatase activity was investigated in anaerobic conditions in the presence of high nitrate and low pH as an alternative approach to the bioreduction of U(VI). A facultative anaerobe, Rahnella sp. Y9602, isolated from soils at DOEs Oak Ridge Field Research Center (ORFRC), was able to respire anaerobically on nitrate as a terminal electron acceptor in the presence of glycerol-3-phosphate (G3P) as the sole carbon and phosphorus source and hydrolyzed sufficient phosphate to precipitate 95% total uranium after 120 hours in synthetic groundwater at pH 5.5. Synchrotron X-ray diffraction and X-ray absorption spectroscopy identified the mineral formed as chernikovite, a U(VI) autunite-type mineral. The results of this study suggest that in contaminated subsurfaces, such as at the ORFRC, where high concentrations of nitrate and low pH may limit uranium bioreduction, the biomineralization of U(VI) phosphate minerals may be a more attractive approach for in situ remediation providing that a source of organophosphate is supplied for bioremediation.

Site Specific X-ray Anomalous Dispersion of the Geometrically Frustrated Kagomé Magnet, Herbertsmithite, ZnCu3(OH)6Cl2

Structural characterization, exploiting X-ray scattering differences at elemental absorption edges, is developed to quantitatively determine crystallographic site-specific metal disorder. We apply this technique to the problem of Zn-Cu chemical disorder in ZnCu(3)(OH)(6)Cl(2). This geometrically frustrated kagomé antiferromagnet is one of the best candidates for a spin-liquid ground state, but chemical disorder has been suggested as a mundane explanation for its magnetic properties. Using anomalous scattering at the Zn and Cu edges, we determine that there is no Zn occupation of the intralayer Cu sites within the kagomé layer; however there is Cu present on the Zn intersite, leading to a structural formula of (Zn(0.85)Cu(0.15))Cu(3)(OH)(6)Cl(2). The lack of Zn mixing onto the kagomé lattice sites lends support to the idea that the electronic ground state in ZnCu(3)(OH)(6)Cl(2) and its relatives is nontrivial.