Effect of Fe-metabolizing bacteria and humic substances on magnetite nanoparticle reactivity towards arsenic and chromium.

Magnetite is a magnetic, Fe(II)-Fe(III)-mineral formed through abiogenic and biogenic pathways. It constitutes an attractive material for remediation due to its reactivity, large surface-area-to-volume ratio when present as nanoparticles, and magnetic recoverability. Magnetite can be repeatedly microbially oxidized or reduced, but it is unclear how this influences the reactivity of magnetite towards toxic metal or metalloid contaminants. In this study, magnetite (both abiogenic and biogenic) was exposed to microbial Fe(II) oxidation and Fe(III) reduction, before reacted with hexavalent chromium (Cr(VI)) or pentavalent arsenic (As(V)). Results showed microbial reduction of both magnetite types improved the removal rate of Cr(VI) from solution, though surprisingly microbial Fe(II)-oxidation also showed enhanced reactivity towards Cr(VI) compared to un-treated magnetite. Synchrotron based analysis confirmed the formation of Cr(III) at the surface of the magnetite. Reactivity with As was less dramatic and showed un-treated material was able to remove As(V) from solution faster than microbially Fe(III)-reduced and Fe(II)-oxidized magnetite. The presence of humic substances was also shown to lead to a decreased reactivity of biogenic and abiogenic magnetite towards As(V) and Cr(VI). Our results imply that Fe-metabolizing bacteria influence the immobilization of contaminants and should be considered when evaluating remediation schemes, especially where Fe-metabolizing bacteria are active.

Cryptic Cycling of Complexes Containing Fe(III) and Organic Matter by Phototrophic Fe(II)-Oxidizing Bacteria.

Fe-organic matter (Fe-OM) complexes are abundant in the environment and, due to their mobility, reactivity, and bioavailability, play a significant role in the biogeochemical Fe cycle. In photic zones of aquatic environments, Fe-OM complexes can potentially be reduced and oxidized, and thus cycled, by light-dependent processes, including abiotic photoreduction of Fe(III)-OM complexes and microbial oxidation of Fe(II)-OM complexes, by anoxygenic phototrophic bacteria. This could lead to a cryptic iron cycle in which continuous oxidation and rereduction of Fe could result in a low and steady-state Fe(II) concentration despite rapid Fe turnover. However, the coupling of these processes has never been demonstrated experimentally. In this study, we grew a model anoxygenic phototrophic Fe(II) oxidizer, Rhodobacter ferrooxidans SW2, with either citrate, Fe(II)-citrate, or Fe(III)-citrate. We found that strain SW2 was capable of reoxidizing Fe(II)-citrate produced by photochemical reduction of Fe(III)-citrate, which kept the dissolved Fe(II)-citrate concentration at low (<10 µM) and stable concentrations, with a concomitant increase in cell numbers. Cell suspension incubations with strain SW2 showed that it can also oxidize Fe(II)-EDTA, Fe(II)-humic acid, and Fe(II)-fulvic acid complexes. This work demonstrates the potential for active cryptic Fe cycling in the photic zone of anoxic aquatic environments, despite low measurable Fe(II) concentrations which are controlled by the rate of microbial Fe(II) oxidation and the identity of the Fe-OM complexes.IMPORTANCE Iron cycling, including reduction of Fe(III) and oxidation of Fe(II), involves the formation, transformation, and dissolution of minerals and dissolved iron-organic matter compounds. It has been shown previously that Fe can be cycled so rapidly that no measurable changes in Fe(II) and Fe(III) concentrations occur, leading to a so-called cryptic cycle. Cryptic Fe cycles have been shown to be driven either abiotically by a combination of photochemical reduction of Fe(III)-OM complexes and reoxidation of Fe(II) by O2, or microbially by a combination of Fe(III)-reducing and Fe(II)-oxidizing bacteria. Our study demonstrates a new type of light-driven cryptic Fe cycle that is relevant for the photic zone of aquatic habitats involving abiotic photochemical reduction of Fe(III)-OM complexes and microbial phototrophic Fe(II) oxidation. This new type of cryptic Fe cycle has important implications for biogeochemical cycling of iron, carbon, nutrients, and heavy metals and can also influence the composition and activity of microbial communities.

A case study for late Archean and Proterozoic biogeochemical iron- and sulphur cycling in a modern habitat-the Arvadi Spring.

As a consequence of Earth's surface oxygenation, ocean geochemistry changed from ferruginous (iron(II)-rich) into more complex ferro-euxinic (iron(II)-sulphide-rich) conditions during the Paleoproterozoic. This transition must have had profound implications for the Proterozoic microbial community that existed within the ocean water and bottom sediment; in particular, iron-oxidizing bacteria likely had to compete with emerging sulphur-metabolizers. However, the nature of their coexistence and interaction remains speculative. Here, we present geochemical and microbiological data from the Arvadi Spring in the eastern Swiss Alps, a modern model habitat for ferro-euxinic transition zones in late Archean and Proterozoic oceans during high-oxygen intervals, which enables us to reconstruct the microbial community structure in respective settings for this geological era. The spring water is oxygen-saturated but still contains relatively elevated concentrations of dissolved iron(II) (17.2 ± 2.8 µM) and sulphide (2.5 ± 0.2 µM) with simultaneously high concentrations of sulphate (8.3 ± 0.04 mM). Solids consisting of quartz, calcite, dolomite and iron(III) oxyhydroxide minerals as well as sulphur-containing particles, presumably elemental S0 , cover the spring sediment. Cultivation-based most probable number counts revealed microaerophilic iron(II)-oxidizers and sulphide-oxidizers to represent the largest fraction of iron- and sulphur-metabolizers in the spring, coexisting with less abundant iron(III)-reducers, sulphate-reducers and phototrophic and nitrate-reducing iron(II)-oxidizers. 16S rRNA gene 454 pyrosequencing showed sulphide-oxidizing Thiothrix species to be the dominating genus, supporting the results from our cultivation-based assessment. Collectively, our results suggest that anaerobic and microaerophilic iron- and sulphur-metabolizers could have coexisted in oxygenated ferro-sulphidic transition zones of late Archean and Proterozoic oceans, where they would have sustained continuous cycling of iron and sulphur compounds.

Oxidation of Fe(II)-Organic Matter Complexes in the Presence of the Mixotrophic Nitrate-Reducing Fe(II)-Oxidizing Bacterium Acidovorax sp. BoFeN1.

Fe(II)-organic matter (Fe(II)-OM) complexes are abundant in the environment and may play a key role for the behavior of Fe and pollutants. Mixotrophic nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOx) reduce nitrate coupled to the oxidation of organic compounds and Fe(II). Fe(II) oxidation may occur enzymatically or abiotically by reaction with nitrite that forms during heterotrophic denitrification. However, it is unknown whether Fe(II)-OM complexes can be oxidized by NRFeOx. We used cell-suspension experiments with the mixotrophic nitrate-reducing Fe(II)-oxidizing bacterium Acidovorax sp. strain BoFeN1 to reveal the role of nonorganically bound Fe(II) (aqueous Fe(II)) and nitrite for the rates and extent of oxidation of Fe(II)-OM complexes (Fe(II)-citrate, Fe(II)-EDTA, Fe(II)-humic acid, and Fe(II)-fulvic acid). We found that Fe(II)-OM complexation inhibited microbial nitrate-reducing Fe(II) oxidation; large colloidal and negatively charged complexes showed lower oxidation rates than aqueous Fe(II). Accumulation of nitrite and fast abiotic oxidation of Fe(II)-OM complexes only happened in the presence of aqueous Fe(II) that probably interacted with (nitrite-reducing) enzymes in the periplasm causing nitrite accumulation in the periplasm and outside of the cells, whereas Fe(II)-OM complexes probably could not enter the periplasm and cause nitrite accumulation. These results suggest that Fe(II) oxidation by mixotrophic nitrate reducers in the environment depends on Fe(II) speciation, and that aqueous Fe(II) potentially plays a critical role in regulating microbial denitrification processes.

Interactions between magnetite and humic substances: redox reactions and dissolution processes.

Humic substances (HS) are redox-active compounds that are ubiquitous in the environment and can serve as electron shuttles during microbial Fe(III) reduction thus reducing a variety of Fe(III) minerals. However, not much is known about redox reactions between HS and the mixed-valent mineral magnetite (Fe3O4) that can potentially lead to changes in Fe(II)/Fe(III) stoichiometry and even dissolve the magnetite. To address this knowledge gap, we incubated non-reduced (native) and reduced HS with four types of magnetite that varied in particle size and solid-phase Fe(II)/Fe(III) stoichiometry. We followed dissolved and solid-phase Fe(II) and Fe(III) concentrations over time to quantify redox reactions between HS and magnetite. Magnetite redox reactions and dissolution processes with HS varied depending on the initial magnetite and HS properties. The interaction between biogenic magnetite and reduced HS resulted in dissolution of the solid magnetite mineral, as well as an overall reduction of the magnetite. In contrast, a slight oxidation and no dissolution was observed when native and reduced HS interacted with 500 nm magnetite. This variability in the solubility and electron accepting and donating capacity of the different types of magnetite is likely an effect of differences in their reduction potential that is correlated to the magnetite Fe(II)/Fe(III) stoichiometry, particle size, and crystallinity. Our study suggests that redox-active HS play an important role for Fe redox speciation within minerals such as magnetite and thereby influence the reactivity of these Fe minerals and their role in biogeochemical Fe cycling. Furthermore, such processes are also likely to have an effect on the fate of other elements bound to the surface of Fe minerals.

An experimental protocol for structural characterization of Fe in dilute natural waters.

The properties of iron (Fe) complexes and compounds in the environment influence several central processes, e.g., iron uptake, adsorption/desorption of contaminants and nutrients, and redox transformations, as well as the fate of of natural organic matter (NOM). It is thus important to characterize Fe species in environmental samples. Synchrotron-based extended X-ray absorption fine structure (EXAFS) spectroscopy has been used in several studies on soils and sediments, but literature is scarce on investigations of natural waters because of low Fe concentrations. In this study we have described a gentle and noninvasive preconcentration method, based on electrostatic adsorption onto ion-exchange resins, suitable for EXAFS analysis of Fe species in dilute stream water samples. The EXAFS results of metal-organic model complexes showed that no significant local structural distortions were induced by the method. We also demonstrated the feasibility for an 8 µM Fe stream water sample. The Fe heterogeneity in this stream water was investigated via a gradient series at 28%, 42%, 77%, 84%, and 100% adsorption of total iron. The EXAFS results showed that Fe(III) in this stream water was divided into Fe(III)-NOM complexes and Fe(III) (oxyhydr)oxides associated with NOM, and that each class consisted of several subspecies.