Nitrite Reduction by Biogenic Hydroxycarbonate Green Rusts

Article pubs.acs.org/est

Nitrite Reduction by Biogenic Hydroxycarbonate Green Rusts: Evidence for Hydroxy-nitrite Green Rust Formation as an Intermediate Reaction Product Delphine Guerbois,† Georges Ona-Nguema,*,† Guillaume Morin,† Mustapha Abdelmoula,‡ Anniet M. Laverman,§ Jean-Marie Mouchel,§ Kevin Barthelemy,‡ Fabien Maillot,† and Jessica Brest† †

Institut de Minéralogie, de Physique des Matériaux, et de Cosmochimie (IMPMC), Sorbonne Universités−UPMC Univ Paris 06, UMR 7590 CNRS, Muséum National d’Histoire Naturelle, IRD UMR 206, 4 place Jussieu, F-75005 Paris, France. ‡ Laboratoire de Chimie Physique et Microbiologie pour l’Environnement (LCPME), UMR 7564 CNRS−Université de Lorraine, 405 rue de Vandoeuvre, 54600 Villers-les-Nancy, France § Sisyphe UMR 7619, CNRS−Université Pierre & Marie Curie (UPMC Paris-6) Sorbonne-Universités, 4 place Jussieu, F-75005 Paris, France S Supporting Information *

ABSTRACT: The present study investigates for the first time the reduction of nitrite by biogenic hydroxycarbonate green rusts, bio-GR(CO3), produced from the bioreduction of ferric oxyhydroxycarbonate (Fohc), a poorly crystalline solid phase, and of lepidocrocite, a well-crystallized Fe(III)oxyhydroxide mineral. Results show a fast Fe(II) production from Fohc, which leads to the precipitation of bio-GR(CO3) particles that were roughly 2-fold smaller (2.3 ± 0.4 μm) than those obtained from the bioreduction of lepidocrocite (5.0 ± 0.4 μm). The study reveals that both bio-GR(CO3) are capable of reducing nitrite ions into gaseous nitrogen species such as NO, N2O, or N2 without ammonium production at neutral initial pH and that nitrite reduction proceeded to a larger extent with smaller particles than with larger ones. On the basis of the identification of intermediates and endreaction products using X-ray diffraction and X-ray absorption fine structure (XAFS) spectroscopy at the Fe K-edge, our study shows the formation of hydroxy-nitrite green rust, GR(NO2), a new type of green rust 1, and suggests that the reduction of nitrite by biogenic GR(CO3) involves both external and internal reaction sites and that such a mechanism could explain the higher reactivity of green rust with respect to nitrite, compared to other mineral substrates possessing only external reactive sites.

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INTRODUCTION Intensive agriculture,1 animal farming,2 as well as industrial and domestic wastewater discharges in surface waters3 are responsible for increased nitrogen loading in rivers, lakes, groundwater, and coastal waters.4,5 The use of fertilizers in agriculture has increased the presence of nitrate (NO3−), nitrite (NO2−), and ammonium (NH4+) in surface waters. In the environment, nitrogen exist in different oxidation states: NO3−(+V), NO2−(+III), NO(+II), N2O(+I), N2(0), and NH4+(−III),6 and cycling between those nitrogen species is driven by microbial activities. Denitrification, for instance, corresponds to the sequential biological reduction of nitrate into N2 gas through the production of various nitrogen species, including aqueous nitrite and gaseous nitric oxide (NO) and nitrous oxide (N2O), as follows: NO3− → NO2− → NO → N2O → N2. Denitrification, as well as anammox, which couples ammonium oxidation to nitrite reduction into N2, are consequently the main processes responsible for nitrogen loss as gaseous forms in natural environments.7−10 Another pathway of nitrate reduction is its conversion to ammonium. Indeed, © 2014 American Chemical Society

nitrate is usually converted into nitrite prior to the formation of ammonium by dissimilatory or assimilatory reduction.11 The assimilatory nitrate reduction pathway is used to incorporate ammonium in biomass, while the dissimilatory nitrate reduction (DNRA) is an alternative pathway of nitrate respiration releasing ammonium in natural systems.10 In addition to this, nitrate can be produced via nitrite by nitrification that involves the oxidation of ammonium in the presence of molecular oxygen.10 The excess of aqueous nitrogen in the form of ammonium, nitrate, and nitrite in the environment leads to eutrophication, characterized in part by an increased growth of many species of seagrasses,12 which is responsible for macroalgal blooms commonly found worldwide.13 It is thus imperative to limit and reduce dissolved nitrogen species in waters. As a consequence, the European Union has established Received: Revised: Accepted: Published: 4505

September 9, 2013 February 12, 2014 March 19, 2014 April 7, 2014 dx.doi.org/10.1021/es404009k | Environ. Sci. Technol. 2014, 48, 4505−4514

Environmental Science & Technology

Article

Table 1. Overview of Nitrite Reduction Involving Fe(II)-Bearing Minerals, Fe(II)-Sorbed FeOOH and Fe2+ Ions Which Have Been Previously Published, and the End-Products Obtained from These Reactions substrate

initial [NO2−] (mM)

initial pH

bio-GR(CO3)F bio-GR(CO3)L GR(SO4) siderite FeCO3 siderite FeCO3 siderite FeCO3 Fe(II)/γFeOOH Fe(II)/HFO Fe2+ ions

5.4 5.4 5.5 4.6 4.6 4.6 0.2 0.26−1.1 4−43

7.3 ± 0.2 7.7 ± 0.4 7.0 7.9 6.5 5.5 8.0 6.8 6.6

end reaction products of nitrite reduction

end reaction products of GR oxidation

gaseous nitrogen species gaseous nitrogen species

ferric oxyhydroxides ferric oxyhydroxides goethite + magnetite

N2Oa N2Ob gaseous nitrogen species NO, N2Oc

lepidocrocite + goethite magnetite n.d.d

references this study this study Hansen et al.21 Rakshit et al. 20 Rakshit et al. 20 Rakshit et al. 20 Sorensen and Thorling18 Tai and Dempsey19 Kampschreur et al.47

a

N2O was measured in the headspace of capped using a Varian 3700 gas chromatograph. bN2O was performed on a Packard model 427 gas chromatograph with 63Ni electron capture detection (320 °C). cNO was measured by Rosemount Chem-iluminescence NOx analyzer and N2O was determined in the off-gas chromatograph. dThe orange color of end oxidation product was not identified in experiment by Kampschreur et al.47 GR means green rust. bio-GR(CO3)L and bio-GR(CO3)F correspond to biogenic hydroxycarbonate green rusts obtained upon bioreduction of either lepidocrocite (Lp) or ferric oxyhydroxycarbonate (Fohc). GR(SO4) corresponds to hydroxysulphate green rust.

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regulatory measures to limit nitrogen release in water, and has imposed a limit of 10−15 mg/L of total nitrogen including N− NO3−, N−NO2−, N−NH4+ and N-organic species in urban wastewater treatments output.14 Among these nitrogen forms, nitrite is an obligatory intermediate in denitrification, DNRA, and nitrification processes as described above; it is also a final reaction product for some nitrate-respiring bacteria, leading to its accumulation in water under high nitrate concentration conditions.15 The occurrence of high nitrite concentrations is an important water quality concern, as it is highly toxic to human and fauna. Moreover, the toxicity of nitrite is related to its transformation into carcinogenic N-nitroso compounds, which are suspected to be responsible for some gastric cancers, and to its ability to convert the hemoglobin to methemoglobin that is then unable to fix oxygen and to transport it to the tissues, leading to hypoxia and the blue-baby syndrome.16 To reduce the adverse effects of nitrite on human health and on macroalgal blooms, any process enhancing the transformation of nitrite ions to nitrogen gas is of interest for the remediation of natural environments. Previous studies conducted with Fe(II)-sorbed on lepidocrocite,17 on hydrous ferric oxide,18 or with Fe(II)-bearing minerals such as siderite19 and hydroxysulfate green rust20 have reported the reduction of nitrite to the greenhouse gas, N2O. Consequently, the use of processes involving Fe(II)-containing minerals could be considered as an interesting and efficient option. Among these Fe(II)-bearing minerals, green rusts which are layered Fe(II,III) hydroxysalts are commonly found in hydromorphic soils21 with variable Fe(II)/Fe(III) ratios typical of those obtained from ferric oxyhydroxides bioreduction by dissimilatory iron-reducing bacteria or during Fe(II) oxidation by nitrate reducers.22−24 Despite the potential importance of green rusts in the nitrogen cycle, the reactivity of these mineral phases with respect to nitrite is still scarcely documented20 (Table 1). The present study investigates for the first time the reduction of nitrite by biogenic hydroxycarbonate green rusts. A mechanism is proposed for this reaction, based on the identification of mineral intermediates and end-products using X-ray diffraction (XRD) and X-ray absorption fine structure (XAFS) spectroscopy at the Fe K-edge.

MATERIALS AND METHODS

Inoculum Preparation and Biogenic FeII−III Hydroxycarbonate Green Rust Synthesis and Characterization. Shewanella putrefaciens CIP 59.28 inoculums, equivalent to the American Type Culture Collection (ATCC) 12099, were prepared with the method described by Ona-Nguema et al.26 Frozen cells from a stock (frozen in 20% glycerol at −80 °C) were revived under aerobic conditions on trypticase soy agar (TSA, BioMérieux, 51044). They were transferred two times to remove glycerol, and subsequently the colonies were used to prepare a suspension with a target absorbance of 1.5 (λ = 600 nm) in NaCl 0.9%. Then, a volume of 30 mL of this suspension was inoculated in 600 mL of trypticase soy broth (TSB, BioMérieux, 51019) in order to initiate the liquid preculture. Cells were grown to a stationary growth phase (14 h) and harvested by centrifugation (12 000g at 20 °C for 15 min), washed twice with NaCl 0.9% sterilized by autoclave (121 °C, 20 min), and concentrated in 30 mL of sterile NaCl 0.9%. The cell density of each inoculum was determined by the number of colony-forming units (CFU). Two samples of Fe II−III hydroxycarbonate green rust, FeII6‑xFeIIIx(OH)12CO3·3H2O (referred to as “GR(CO3)” hereafter), were prepared by bioreduction of either ferric oxyhydroxycarbonate, FeIII6O12H8 CO3·3H2O, or lepidocrocite, γ-FeOOH, at pH 7.5 ± 0.2, with the same inoculum of S. putrefaciens. Ferric oxyhydroxycarbonate (referred to as “Fohc” hereafter) corresponds to the socalled “ferric green rust” layered compound and was synthesized by oxidation of a synthetic GR(CO3) with H2O2.27 Lepidocrocite (Lp) was synthesized and reduced following the procedures described in ref 25 with 80 mM Lp and a bacterial density of 5.7 × 109 CFU/mL. Sterilization of FeOOH suspensions was performed by autoclaving (20 min 120 °C) prior to the addition of the cell suspension. Samples were collected during the reaction monitoring Fe(II) production. Solids were centrifuged in a glovebox under N2 atmosphere, washed twice with O2-free Milli-Q water, dried under vacuum in the glovebox and characterized by X-ray diffraction (XRD), Transmission Mössbauer Spectroscopy (TMS), and Transmission Electronic Microscopy (TEM). Green rust samples produced upon reduction of Fohc and of Lp are referred to as “bio-GR(CO3)F” and “bio-GR(CO3)L”, respectively. 4506

dx.doi.org/10.1021/es404009k | Environ. Sci. Technol. 2014, 48, 4505−4514


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Figure 1. (a) Fe(II) production as a function of time during the formation of hydroxycarbonate green rusts {bio-GR(CO3)} upon bioreduction of either lepidocrocite (Lp) or ferric oxyhydroxycarbonate (Fohc). Concentration values are averaged for n independent experiments. Initial rates of Fe(II) production are calculated according to a second-order kinetic models displayed as solid lines. TEM images of the bio-GR(CO3) samples obtained after bioreduction of (b) Fohc or (c) Lp. Inserts corresponds to SAED patterns along the [001] direction.

X-ray Diffraction. Mineralogical compositions of the solid samples from experiment #1 and #2 conducted with bioGR(CO3)F and from experiment #9 conducted with bioGR(CO3)L were determined by X-ray powder diffraction (XRD). CoKα radiation (λ = 0.178 89 nm) was used in order to minimize the X-ray absorption of Fe. In order to avoid any changes in the mineralogy related to possible redox reaction with air, powder samples were mounted on low background Si single crystal sample holders within the glovebox and transferred into an anoxic sample chamber designed by the IMPMC project team for XRD data collection under anoxic conditions. Data were collected in Bragg−Brentano geometry using a Panalytical X’Pert Pro diffractometer equipped with an X’celerator detector. A continuous collection mode was applied over the 5−80° 2θ range with a 0.016° 2θ step and counting 1 h for each sample. XAFS Data Collection and Analysis. Iron K-edge XAS data for samples 0.5, 1, 7, 48, and 72 h from bio-GR(CO3)F interaction with NO2− were recorded at 77 K in transmission detection mode on the XAFS beamline at ELETTRA, Trieste, Italy. Data for the Fohc model compound were recorded at 40 K in transmission detection mode on BM23 beamline at ESRF, Grenoble, France. Absorption spectra were merged and normalized using the Athena program29 and Extended X-ray Absorption Fine Structure (EXAFS) spectra were extracted using the XAFS program.30 In order to identify and to quantify the products of bio-GR(CO3)F oxidation after reaction with nitrite, EXAFS data were analyzed by Linear Combination Fitting (LCF) as described in refs 24 and 31 for similar iron compounds. For this purpose, our set of iron model compounds spectra included bio-GR(CO3)F, ferric oxyhydroxycarbonate,32 Fe(OH)2,26 ferrihydrite, goethite, akaganeite, maghemite,33 magnetite,34 and lepidocrocite.30 The oxidation state of iron was determined by linear combination fitting (LCF) of X-ray Absorption Near Edge Structure (XANES) data using the XANES spectra of bio-GR(CO3)F and of Fohc as fitting components.

Interactions between Green Rust and Nitrite. The reactivity of biogenic hydroxycarbonate green rust with respect to nitrite ions was investigated under anoxic conditions using samples of bio-GR(CO3)L and bio-GR(CO3)F. Time-course experiments were conducted to determine kinetics of nitrite reduction and Fe(II) oxidation. Experiments were carried out in a glovebox under an argon atmosphere to preserve green rust from oxidation by O2. Suspensions of 1.7 g/L of bio-GR(CO3)F or bio-GR(CO3)L were prepared in O2-free Milli-Q water. The suspensions were then sonicated for 15 min and the pH was adjusted to 7.5 ± 0.2 with 1 M HCl. Appropriate volumes of an O2-free sodium nitrite stock solution (0.3 M) were added in all experiments to start the reaction with 5.4 mM NO2−. Experiments were performed under anoxic conditions in closed 100-mL flasks with sealed rubber stoppers. Suspensions were sampled over the reaction time using syringes and needles and treated either by acid extraction for total Fe(II) analysis, or by filtration for dissolved NO2− and NH4+ analyses. Solid samples were collected by centrifugation and vacuum-dried within the glovebox. All aqueous and solid samples were kept under anoxic conditions prior to analysis. Eight independent assays (experiments #1−8) were carried out with bio-GR(CO3)F at initial pH values around 7.4 ± 0.2, and five assays (experiments #9−14) were performed with bio-GR(CO3)L at pH 7.7 ± 0.4 (Supporting Information, SI, Table SI-1). Solution Analyses. The total Fe(II) concentration, including the aqueous and solid phases, was estimated as 0.5 M HCl-extractable Fe(II). To this end, 0.5 mL of unfiltered sample suspension was mixed with 0.5 mL of 1 M HCl, and with 2 mL of a 11 mM 1,10-phenanthroline, 227 mM Glycocoll, and 9 mM nitrilacetic acid solution.28 These colored solutions were stored under anoxic conditions for at least one hour before photometric analysis (Novaspec Plus visible spectrophotometer). Initial dissolved Fe(II) concentrations, prior to nitrite addition were measured using the same colorimetric method, after 0.22 μm filtration. Dissolved NO2− and NH4+ were measured by ionic chromatography DIONEX ISC 3000 after 0.22 μm filtration with detection limits of 0.1 mg/L. 4507



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Figure 2. Nitrite reduction by (a) bio-GR(CO3)F and by (b) bio-GR(CO3)L. Error bars for nitrite correspond to standard deviation calculated from 7 and 3 independent experiments carried out with bio-GR(CO3)F and bio-GR(CO3)L, respectively. Total Fe(II) concentrations in the solid phase were measured using XANES spectroscopy in experiment #1 (see text and Table SI-2), while dissolved Fe(II) concentrations were determined by the phenanthroline assay.

Figure 3. Linear Combination Fitting results for the Fe K-edge XANES and EXAFS spectra of the reaction products from time course experiment #1 conducted with bio-GR(CO3)F and nitrite (Table SI-2). Experimental spectra and LCF fit curves are displayed as black and red solid lines, respectively. (a) XANES data indicate progressive oxidation of bio-GR(CO3)F into Fohc (Table SI-3); (b−d) EXAFS data confirm this trend and the evolution of solid phases proportions showing the oxidation of bio-GR(CO3)F and the production of Fohc, and Lp in the 72 h sample; these proportions resulted from the LCF fit analysis of Fe K-edge XANES spectra (Table SI-5).

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RESULTS

(Figure SI-1). During these bioreduction experiments, solid phases were characterized over time by X-ray diffraction (XRD) (Figure SI-2) and each bacterial culture was stopped when the ferric precursor was fully reduced and when green rust was the sole mineral product. XRD analysis indicated the formation of pure FeII−III hydroxycarbonate green rust 1, GR(CO3), after 14 and 33 days of incubation in the experiments with Fohc and with Lp, respectively (Figure SI-2). The GR(CO3) mineral species was characterized by predominant Bragg peaks at d003 = 7.55 Å, d006 = 3.78 Å, d012 = 2.67 Å, d015 = 2.35 Å, and d018 = 1.97 Å.23,25,35 TEM micrographs of bio-GR(CO3)F and bio-GR(CO3)L samples showed isolated hexagonal crystals typical of green

Production and Characterization of the Biogenic FeII−III Hydroxycarbonate Green Rust Samples. Fe(II) production was monitored as a function of time during the preparation of the bio-GR(CO3)F and bio-GR(CO3)L samples (Figures 1a and SI-1). The rate of microbial Fe(III) reduction was faster when Fohc was used as an electron acceptor instead of Lp (Figure 1). Initial rates calculated according to a secondorder kinetic model on the first five days were 5.3 and 3.2 mM/ h in experiments with Fohc and with Lp, respectively. After 5 days of incubation, Fe(II) production continued at lower rates and reaching a value of 40 mM in both experiments, after 11 and 26 days, in the Fohc and Lp experiments, respectively 4508



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Figure 4. XRD patterns of samples collected at different reaction times during interaction of bio-GR(CO3)F with nitrite ions in experiment #1 (Table SI-2). The unindexed peaks on the low angle side of the 003 and 006 Bragg peaks of GR(CO3) (labeled as GR) are interpreted as basal spacing Bragg reflection of a NO2− intercalated green rust phase (see text). (a) Diffractograms are presented between 10 and 30° in 2-θ range; red and blue rectangles correspond to (b) a zoom of the 003 reflections between 12.5° and 15°, and (c) a zoom of the 006 reflections.

rust (Figure 1b,c) with a unit cell parameter a value of 0.04 nm in hexagonal R3m ̅ space group that is consistent with those of GR(CO3).25 Crystal diameters averaged for 8−10 isolated particles were twice as large for sample bio-GR(CO3)F (2.3 ± 0.4 μm) than for sample bio-GR(CO3)L(5.0 ± 0.4 μm). Mössbauer spectra of these samples exhibit three paramagnetic quadrupole doublets D1, D2 and D3 at 77 K (Figure SI-3). The doublets D1 and D2 with large center shift and quadrupole splitting values are typical of Fe2+ in GR(CO3) at 77 or 10 K, while the doublet D3 with small center shift and quadrupole splitting values is characteristic of paramagnetic Fe3+ in GR(CO3) (Table SI-2).35,36 These Mössbauer analyses indicate that Fe(II)/Fe(III) ratios are equal to 1.0:1 and 1.2:1 for samples bio-GR(CO3)F and bio-GR(CO3)L, respectively. Interactions of Biogenic Hydroxycarbonate Green Rust with Nitrite. During the first five hours of nitrite interaction with bio-GR(CO3)F, and with bio-GR(CO3)L, nitrite concentration decreased from 5.5 ± 0.2 mM to 3.7 ± 0.8 mM (Figure 2a), and from 5.4 mM to 4.3 ± 0.2 mM (Figure 2b), respectively. This decrease of nitrite concentration corresponds to 33% of nitrite reduced by bio-GR(CO3)F and 20% by bio-GR(CO3)L. After 48 h of interactions with bioGR(CO3)F and bio-GR(CO3)L, 60% and 30% of the initial nitrite was consumed, respectively (Table SI-1), indicating that the reaction was faster with bio-GR(CO3)F than with bioGR(CO3)L. However, the overall reaction was slowed down between two days and five days with both green rusts (Figure 2). Ammonium concentrations were under detection limit in all of the experiments, suggesting that nitrite was reduced into gaseous nitrogen species after reaction with both bio-GR(CO3)F and bio-GR(CO3)L samples. After one hour of reaction with both GR(CO3) samples, total Fe(II) concentrations, measured by the colorimetric analysis after 0.5 N HCl extraction, decreased down to ∼30% of the initial Fe(II) content (Figure SI-4). However, these total Fe(II) concentration values may have been underestimated since, under strong acidic conditions, dissolved Fe(II) ions react rapidly with nitrite ions, as recently reported by Klueglein and Kappler.37 According to these authors, using sulfamic acid

measurements can significantly limit nitrite reduction by aqueous Fe(II). In the present study, we have used an alternative approach to follow the concentration of Fe(II) during the interaction of green rust particles with nitrite ions. Indeed, XANES spectroscopy at the Fe K-edge was used to estimate the proportions of Fe(II) and Fe(III) in the solid phases over the course of the nitrite reduction by the bioGR(CO3)F sample, in experiment #1 (Figure 3a; Table SI-3). XANES data for samples collected from 1 to 72 h of reaction were fit using only bio-GR(CO3)F and Fohc as fitting components. The fit results indicate a net increase of the proportion of Fohc at the expense of bio-GR(CO3)F. According to the Fe(II)/Fe(III) ratio of 1:1 determined using Mössbauer spectroscopy for the bio-GR(CO3)F samples, the proportion of Fe(II)/FeTotal in the solid phase could be determined as a function of time from the XANES LCF fit results (Table SI-3). The proportion of initial dissolved Fe(II) (0.57 mM) in equilibrium with bio-GR(CO3)F was equal to 7% of the total initial Fe(II) concentration of 8 mM as measured by 0.5 N HCl extraction prior to nitrite addition, and did not increase during interaction with nitrite (Figure 2a). Accordingly, the evolution of the total Fe(II) quantity could be estimated using XANES analyses of the solid phase (Figure 2a). XANES results thus indicate that 26% and 33% of Fe(II) in the solid phase was oxidized after 1 and 7 h of reaction with nitrite, respectively. Between 7 h and 2 days, Fe(II) oxidation stopped as indicated by XANES results, and the nitrite consumption drastically slowed down (Figure 2a). Further Fe(II) oxidation is indicated by XANES results between 2 and 3 days, while no changes in nitrite concentrations are observed within the same period of time (Figure 2a). Such an Fe(II) oxidation could be explained by the reduction of other nitrogen species such as NO or N2O, which could have been produced after nitrite reduction, as discussed in the next section. This Fe(II) oxidation process was accompanied by a significant color change of the iron suspensions from dark green to brownish, suggesting the formation of Fe(III)-containing solid phases. Mineralogical Transformations of bio-GR(CO3) after Interaction with Aqueous Nitrite. XRD data show that 4509



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illustrated in Figure SI-9. This similarity could be explained by the presence of ferrihydrite-like nanosized clusters in Fohc, as suggested by the presence of the main diffusion bands of Fh in the XRD pattern of Fohc, which thus emphasizes the complex structure of this phase (Figure SI-9). Therefore, the presence of ferrihydrite as an oxidation product during the reaction of green rust with nitrite ions cannot be excluded since this component could not be distinguished from Fohc by EXAFS analysis. The presence of Fohc as the main oxidation product of bio-GR(CO3)F between 0.5 and 72 h in experiment #1 is however supported by the fact that this phase is observed, in association with goethite, as a main component after 33 days of reaction with nitrite ions (Figure SI-6b). Overall, EXAFS results showed that 42% of green rust was oxidized during the first 7 h of interaction, leading to the formation of Fohc as a predominant oxidation product (Figure 3d), in possible association with minor components as Gt and Lp (≤10%). Finally, yellow ochre colloids were observed in filtered subsamples taken in the experiments #6, #7, and #8, indicating the presence of Fe(III)-containing compounds that passed through the 0.22 μm pore size of the filters (Figure SI-10), and which could correspond to nanosized Fohc or Fh-like compounds. These Fe(III)-colloids were only observed between 20 min and 1 day of reaction, suggesting that they could have ripen into crystalline phases as Lp and Gt after 1 day of reaction. These latter mineral phases are indeed observed as final oxidation products by XRD (Figure SI-6),

when bio-GR(CO3)F interacted with nitrite, new diffraction lines appear on the low angle side of the 003 and 006 reflections with d-spacings at d003 = 7.55 Å and d006 = 3.77 Å (Figure 4). These new diffraction peaks are observed between 30 mn and 24 h and disappear after 48 h of reaction (Figure 4b and Table SI-4). The shift in their position with respect to those of GR(CO3) matched with d003 basal spacing of 7.87 and 7.81 Å (Figure 4b), consistent with d006 spacing of 3.93 Å and 3.89 Å (Figure 4c). These interlayer spacing are assigned to the incorporation of nitrite ions in the interlayer space of green rust, suggesting the formation of an hydroxy-nitrite green rust, GR(NO2), a new type of green rust 1. The same d003 and d006 spacing values of 7.8 and 7.9 Å were assigned to nitrite ions incorporation in the interlayer region of MgAl-NO2 and NiAlNO2 LDHs.38 Similar Bragg peaks were observed in experiment #2 performed with the same bio-GR(CO3)F (Figure 4a−c). In contrast, in experiment #9 carried out with bio-GR(CO3)L, no extra Bragg peaks were observed in the XRD patterns after reaction with nitrite (Figure SI-5d,e). During the first 48 h of reaction in experiments #1, #2, and #9, no other solid-phases than green rusts were observed by XRD. Then, goethite formed after six days reaction of bio-GR(CO3)F with nitrite in experiment #1 (Figure SI-6a). In contrast, bio-GR(CO3)L was still the predominant solid phase in experiment #9 after 6 days (Figures SI-5d and SI-6c) and 8 days (Figure SI-5d). These results show that the oxidation of small bio-GR(CO3)F particles was faster than that of large bio-GR(CO3)F particles. Fe−K edge EXAFS spectra of the solid samples from the time course experiment #1 were best fit using linear combinations of bio-GR(CO3)F and Fohc as main fitting components (Figure 3b,c) with the proportions reported in Figure 3d and in Table SI-3. An example of linear decomposition of the EXAFS spectrum is given for the 48 h sample in Figure SI-9. For all samples analyzed, from 0.5 h to 72 h of reaction in experiment #1, the proportions of the fit components determined by EXAFS LCF were fully consistent with those determined by XANES LCF, within an accuracy of ±10% (Table SI-3). Although EXAFS data of samples 0.5, 1, 7, and 48 h could be fit with only the two components bioGR(CO3)F and Fohc, it was necessary to include an additional lepidocrocite component to fit the 72 h sample EXAFS data, which reduced the goodness of fit of 35%, as illustrated in Figure SI-10. This minor component was not included in XANES fitting due to the similarity of the Fohc and Lp XANES spectra. Lepidocrocite is a common product of green rust oxidation and it is observed by XRD analysis in experiment #9 after 6 days and 33 days reaction of bio-GR(CO3)L with nitrite (Figure SI-5d). Addition of a goethite component slightly improved the fits of the EXAFS spectra for samples 1 and 48 h, with a relative decrease of 20% and 30% of the goodness of fit. This goethite component was not retained in the final EXAFS fit solutions for the 0.5−72 h samples (Figure 3; Table SI-3), since the resulting proportions of goethite were lower than 10%, which is the estimated accuracy of our LCF analysis Table SI-3. However, goethite was unambiguously identified by XRD analysis as an oxidation product of bio-GR(CO3)F and of bioGR(CO3)L after longer reaction times with nitrite, i.e., 6 and 33 days (Figure SI-6). Goethite was especially the major oxidation product of bio-GR(CO3)F in experiment #1 after 33 days (Figure SI-6b). Interestingly, replacing the ferric oxyhydroxycarbonate component (Fohc) by a ferrihydrite (Fh) component for fitting the EXAFS data gave similar fit qualities. Indeed, Fohc and Fh exhibit similar EXAFS spectra, as

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DISCUSSION Dissimilatory Reduction of Lepidocrocite and of Ferric Oxyhydroxycarbonate. Previous studies have demonstrated that biogenic hydroxycarbonate green rust can be formed upon reduction of lepidocrocite,23,25,35,39 or of ferric oxyhydroxycarbonate40 by Shewanella putrefaciens. In the present study, we show that the particle size of biogenic hydroxycarbonate green rust produced using a same inoculum of S. putrefaciens strain ATCC 12099 can depend on the nature of the ferric precursor. Moreover, we demonstrate that the bioreduction of Fohc, a poorly crystalline solid phase, is faster than that of lepidocrocite, a crystalline Fe(III)-oxyhydroxide mineral. These findings are consistent with previous studies reporting that the rate and extent of microbial iron(III) oxides reduction are controlled by factors such as particle size,41 degree of crystallinity and surface area,42,43 solubility,44 and surface site concentration of the solid phase.45 Accordingly, the poorly crystalline and nanosized character of the Fohc precursor likely induced a fast Fe(II) production, which led to the precipitation of bio-GR(CO3) particles that were at least twice as small as those obtained from the bioreduction of crystalline lepidocrocite. Such a relationship between green rust (GR) crystal size and kinetics of Fe(II) production has already been raised in a previous laboratory study by Zegeye et al. 46 that compared particle size of GR(SO4) produced abiotically to those bacterially formed, and suggested that the low kinetics of Fe(II) production could allow the germination and nucleation of large GR crystals. Moreover, our results indicate that the Fe(II) production rate did not significantly influence the Fe(II)/Fe(III) ratio, which was in the 1:1−1.2:1 range in the GR(CO3) produced from the Fohc and Lp bioreduction. Such low Fe(II)/Fe(III) ratio in GR(CO3) is unusual compared to GR(CO3) formed in most other studies performed in bacterial cultures, which generally gave values close to 1.735,39 or 2.6.31,39 Similar low ferrous-containing GR(CO3) were however 4510



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obtained for the first time by Legrand et al.47 using an electrochemical procedure, and by Ona-Nguema et al.25 upon bioreduction of lepidocrocite. Reaction Products of the Reduction of Nitrite Ions by Biogenic Hydrocarbonate Green Rust. The present study shows that the reduction of NO2− ions by biogenic GR(CO3) at neutral initial pH proceeded to a larger extent with smaller particles (∼2 μm) than with bigger ones (∼5 μm). However, regardless of particle size, biogenic GR(CO3) are capable of reducing NO2− ions without NH4+ production. These results suggest that NO2− ions were reduced into gaseous nitrogen species such as NO, N2O, or N2 by biogenic GR(CO3). This finding is consistent with previous studies in which NO2− ions were reduced into gaseous nitrogen species by siderite,19 Fe(II)-sorbed lepidocrocite,17 Fe(II)-sorbed hydrous ferric oxide,18 or by Fe2+ ions in sulfate-rich systems.48 In the study by Kampschreur et al.,48 aqueous Fe2+ was first oxidized into a greenish suspension most likely a green rust compound, leading to an increase in NO emission; this latter gaseous species reacted with the supposed green rust compound to form N2O and Fe(III)-minerals. The first study in which a wellcharacterized green rust compound was exposed to nitrite ions was carried out with GR(SO4).20 Although nitrogen products were not measured, these authors proposed the formation of various nitrogen species such as N2O, N2, and NH4+, based on the interpretation of the Fe(II)oxidized/ NO2−reduced molar ratio obtained in their experiments. The following equations correspond to the reduction of NO2− ions into N2O, N2 or NH4+, coupled to the oxidation of hydroxysulfate GR into goethite:

Fe3IIFe3III(OH)10 (OOH) ·CO3 + 1.5N2O ↔ 6FeOOH + 1.5N2 + H+ + HCO−3 + 1.5H 2O

The global Fe(II)oxidized/NO2−reduced molar ratio in our experiments was close to 2:1 after three days of reaction, which corresponds to the reduction of NO2− into N2O according to eq 4. However, the reaction involved in eq 4 usually occurs in two steps with the production of NO gas as an intermediate reaction product (eqs 5 and 6) as previously reported in the study by Kampschreur et al.47 In our experiments, the kinetics of Fe(II) oxidation and NO2− reduction could be consistent with such a two step reaction pathway. Indeed, an equimolar reaction occurred in the first two days of incubation, i.e., 2.4 mM of Fe(II) were oxidized and 2.6 mM of NO2− were reduced. According to eq 5, this equimolar stoichiometry matches the transformation of NO2− to NO gas. Our results indicate a strong oxidation of Fe(II) (i.e., 3.5 mM) between 2 and 3 days of reaction, while the reduction of nitrite was slowed down. Such behavior could suggest that bio-GR(CO3) reacted with NO gas to produce N2O, as reported in eq 6. It cannot be excluded that bioGR(CO3) reduce a part of the N2O gas further into N2, i.e., eq 7. Overall, the present interpretations are consistent with the absence of NH4+ production in our experiments with bioGR(CO3). In contrast, NH4+ production was observed both under circumneutral or slightly alkaline conditions during the reduction of NO2− by more reduced substrates such as wüstite, FeO,49 and zerovalent iron,50,51 and under acidic conditions when the reduction of NO2− was coupled with the oxidation of FeS52 or of zerovalent iron.53 Oxidation Mechanisms of bio-GR(CO3) by Nitrite and Formation of Nitrite Green Rust. Green rusts are Fe(II,III) layered double hydroxysalts that are intermediate compounds between Fe(II)-hydroxides and Fe(III)-(oxyhydr)oxides; their structure consists of [Fe2+(1‑x) Fe3+x (OH)2]x+ positively charged layers, which alternate with [(x/n)An−·(mx/n)H2O]x− negatively charged interlayers that include m water molecules per An− anion.54 Previous studies have suggested that such a layered structure contains external and internal Fe(II) reactive sites.20,55 In addition, Hansen and Koch54 have previously demonstrated that when nitrate ions enter into the interlayer space of GR(SO4), the available surface area for nitrate reduction was increased, and the reaction rate was 40 times higher than when the available surface area was restricted to the outer particle surfaces. Their XRD analysis revealed a decrease of the interlayer spacing from 10.9 to 7.7 Å when GR(SO4) was exposed to nitrate ions; this behavior was assigned to a shrinking of the anion- and water-containing interlayer associated with ion exchange of sulfate for nitrate.54 This former study provides evidence for the intercalation of nitrate in GR(SO4) interlayer by using FTIR analysis, and showed that the ν3 vibration at 1385 cm−1 corresponded to nitrate exchanged into green rust, while the single ν1 + ν4 nitrate combination band at 1767 cm−1 was assigned to free nitrate ions in the interlayer of GR(SO4). Similarly, the incorporation of nitrite in the interlayer of MgAl-NO2 and NiAl-NO2 layered double hydroxides (LDHs) was characterized by a sharp absorption band at 1267 cm−1.37 XRD analysis further indicated that the observed 003 basal spacing were equal to 7.9 and 7.8 Å for MgAl-NO2 and NiAl-NO2 LDHs, respectively; such reflections were assigned to the flat lying orientation of nitrite ions in the interlayer region of MgAl-NO2 and NiAl-NO2

Fe II4 Fe2III(OH)12 SO4 ·3H 2O + 2NO−2 ↔ 6α FeOOH + N2O + SO24 − + 6H 2O

(1)

3Fe II4 Fe2III(OH)12 SO4 ·3H 2O + 4NO−2 + 2OH− ↔ 18α FeOOH + 2N2 + 3SO24 − + 6H 2O

(2)

3Fe II4 Fe2III(OH)12 SO4 ·3H 2O + 2NO−2 + 2OH− ↔ 18α FeOOH + 2NH+4 + 3SO24 − + 15H 2O 20

(3)

Fe(II)oxidized/NO2−reduced

In the study by Hansen et al., the molar ratio was equal to 2.87:1 ± 0.17, and was therefore higher than 2.0:1 as in eq 1 and close to 3:1, as in eq 2, thus suggesting the production of N2 and N2O. The two biogenic GR(CO3) used in our study are capable of reducing NO2− without NH4+ production, suggesting that the resulting nitrogen gas could be NO, N2O, or N2. The following equations correspond to possible reactions coupling the reduction of nitrogen species with the oxidation of GR(CO3) into ferric oxyhydroxide: Fe3IIFe3III(OH)10 (OOH)·CO3 + 1.5NO−2 + 0.5H+ ↔ 6FeOOH + 0.75N2O + HCO−3 + 2.25H 2O

(4)

Fe3IIFe3III(OH)10 (OOH)· CO3 + 3NO−2 + 2H+ ↔ 6FeOOH + 3NO + HCO−3 + 3H 2O

(5)

Fe3IIFe3III(OH)10 (OOH) ·CO3 + 3NO ↔ 6FeOOH + 1.5N2O + HCO−3 + H+ + 1.5H 2O

(7)

(6) 4511



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explained by aging of the first oxidation products such as Fohc as proposed by Legrand et al.58 Environmental Implications. The present study conducted with two biogenic GR(CO3) samples demonstrates clearly the reduction of nitrite without ammonium production, in agreement with a previous study conducted with sulfate green rust.21 Moreover, we show that the reduction of nitrite by biogenic GR(CO3) involves both external and internal reactions sites, the latter ones corresponding to nitrite ions intercalated in the interlayer space of the green rust structure. Such a mechanism was proposed as a possible reason to explain the higher reactivity of green rust with respect to nitrite, compared to other mineral substrates possessing only external reactive sites, as siderite20 (Table 1). This reactivity could be however limited to large green rust particles, for which no nitrite intercalation is observed in the present study.

LDHs.37 In the present study, the XRD patterns of bioGR(CO3)F interactions with nitrite ions show the presence of diffraction peaks at d003 = 7.8 Å, d003 = 7.9 Å, and d006 = 3.9 Å mixed with predominant lines of GR(CO3). These new diffraction lines are ascribed to the intercalation of nitrite into the bio-GR(CO3) interlayer, leading to the formation of an hydroxy-nitrite green rust, GR(NO2) as an intermediate reaction product. This is consistent with a previous study by Refait et al.56 that provided evidence for the formation of an hydroxyl-selenate green rust as an intermediate reaction product during the reduction of selenite ions to Se(IV) species by an Fe(II)-containing solid phase.56 Our work indicates the simultaneous presence of two types of green rusts, i.e., GR(CO3) and GR(NO2), as previously observed in a study by Ona-Nguema et al.,34 which showed the competitive formation of bio-GR(CO3) and bio-GR(SO4) depending on the relative ratio of bicarbonate and sulfate concentrations. Moreover, we suggest that d-spacings at d003 = 7.9 Å and d003 = 7.8 Å correspond to two different configurations of nitrite ions in the green rust interlayer during its oxidation, as previously reported in the work by Wang and Wang57 that demonstrated the influence of the layer charge density on the orientation in the interlayer nitrate in MgAl LDHs. Therefore, we suggest that the layer charge density of the green rust used in the present study varies positively as a function of time during its oxidation by nitrite ions, allowing different configurations of nitrite ions in the GR(NO2) interlayer space. The intercalation of nitrite in green rust interlayers exposes nitrite ions to internal Fe(II) reactive sites, leading to an increase of the available surface area of green rusts as previously reported by Hansen and Koch.54 For the oxidation of the bioGR(CO3)L samples, we suggest that only the external Fe(II) sites of the green rust were available since no nitrite intercalation was observed by XRD analysis over the course of the nitrite reduction reaction. This may explain the slower nitrite reduction observed with the bio-GR(CO3)L samples, compared to the bio-GR(CO3)F samples, for which nitrite intercalation was observed. Although the reasons for the absence of observable nitrite intercalation in the bio-GR(CO3)L particles are still unclear, we suggest that it could be related to their larger particle size, which could limit the diffusion of NO2− ions within the interlayer space. Mineralogical Transformations upon GR(CO3) Oxidation by Nitrite Ions. XAS data reveal that the first steps of the reaction of bio-GR(CO3) with nitrite leads to the formation of ferric hydroxycarbonate, with minor amounts of other ferric oxyhydroxides, such as goethite, and lepidocrocite. XRD data of long-term (33 days) oxidation samples show the formation of goethite, lepidocrocite, and Fohc as major mineral phases. Our results also emphasize the difficulty to distinguish between Fohc and Fh using EXAFS spectroscopy, which could be explained by similarities in the local structure of these phases. However, despite some similarities in their XRD patterns, Fohc can be distinguished from Fh by characteristic basal plane reflections in the low angle region of the XRD pattern and by slight shifts of some high angle diffusion bands. Overall, our results are in good agreement with previous studies, especially based on XRD analyses, which reported that the oxidation of synthetic GR(CO3) suspensions by either H2O2 or air leads to the formation of Fohc,27,58−60 lepidocrocite,56,58 and goethite56,57 as major oxidation products. The formation of goethite as a predominant end-reaction product could be

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ASSOCIATED CONTENT

S Supporting Information *

Mö ssbauer spectra of bio-GR(CO3)F and bio-GR(CO3)L samples, EXAFS and XANES fits results, additional chemical data, XRD patterns, LCF fits analysis of Fe K-edge EXAFS, and materials and methods for TEM and TMS analysis. This material is available free of charge via the Internet at http:// pubs.acs.org.

■

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

■

ACKNOWLEDGMENTS This study was funded by the Ecotech program of the “Agence Nationale de la Recherche” (ANR), piloted by ADEME (ECOTECH2009−No. 0994C0103). D.G. expresses her sincere gratitude to SAUR for the Ph.D. position grant. The authors make a special thanks to Ludovic Delbes, Frederic Gélebart, and the IMPMC Cell Project Team for their help for the device used to record XRD data under anoxic conditions. We thank Jaafar Ghanbaja at the Université de Lorraine for his help with the Transmission Electron Microscope analyses. The technical staff Luca Olivi at ELETTRA (Trieste, Italy) and Manuel Muñioz at ESRF (Grenoble, France) are greatly acknowledged for their technical support during the XAFS measurements.

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REFERENCES

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Nitrite Reduction by Biogenic Hydroxycarbonate Green Rusts

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