Mechanisms of nickel sorption by a bacteriogenic birnessite

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Abstract

A synergistic experimental–computational approach was used to study the molecular-scale mechanisms of Ni sorption at varying loadings and at pH 6–8 on the biogenic hexagonal birnessite produced by Pseudomonas putida GB-1. We found that Ni is scavenged effectively by bacterial biomass-birnessite assemblages. At surface excess values below 0.18 mol Ni kg−1 sorbent (0.13 mol Ni mol−1 Mn), the biomass component of the sorbent did not interfere with Ni sorption on mineral sites. Extended X-ray absorption fine structure (EXAFS) spectra showed two dominant coordination environments: Ni bound as a triple-corner-sharing (Ni-TCS) complex at vacancy sites and Ni incorporated (Ni-inc) into the MnO2 sheet, with the latter form of Ni favored at high sorptive concentrations and decreased proton activity. In parallel to our spectral analysis, first-principles geometry optimizations based on density functional theory (DFT) were performed to investigate the structure of Ni surface complexes at vacancy sites. Excellent agreement was achieved between EXAFS- and DFT-derived structural parameters for Ni-TCS and Ni-inc. Reaction-path calculations revealed a pH-dependent energy barrier associated with the transition from Ni-TCS to Ni-inc. Our results are consistent with the rate-limited incorporation of Ni at vacancy sites in our sorption samples, but near-equilibrium state of Ni in birnessite phases found in nodule samples. This study thus provides direct and quantitative evidence of the factors governing the occurrence of Ni adsorption versus Ni incorporation in biogenic hexagonal birnessite, a key mineral in the terrestrial manganese cycle.

Introduction

The mobility and bioavailability of Ni in metal-impacted ecosystems is significantly influenced by sorption on Mn(IV) oxide minerals. For example, chemical analysis of sediment samples from Pinal Creek, Arizona, an aquatic ecosystem adversely impacted by copper mining (Fuller and Harvey, 2000, Kay et al., 2001), and field measurements made on biofilms formed in acid rock drainage from a Ni mine in Ontario, Canada, (Haack and Warren, 2003) revealed that Ni was depleted from the water column by sorption to MnO2. Microbial catalysis of Mn(II) oxidation to form MnO2 also was found to be significant at both field sites. Microorganisms have in fact been shown to play a central role in the oxidation of Mn(II) to Mn(IV) in terrestrial and aquatic environments, thereby precipitating nanocrystalline Mn(IV) oxides (Tebo et al., 2004, Hochella et al., 2005, Bargar et al., 2009). There is now consensus that these biogenic MnO2 minerals are widespread, serving as effective sinks for toxicant metal cations such as Ni2+ due to their abundant cation vacancy defects and nanoscale particle size.

The biogenic MnO2 found in field settings, as well as that produced by model bacteria in laboratory culture, is a poorly-crystalline layer-type mineral with hexagonal symmetry (hexagonal birnessite) and significant sheet-stacking disorder along the c-axis (Friedl et al., 1997, Villalobos et al., 2003, Tebo et al., 2004, Webb et al., 2005, Bargar et al., 2009). Villalobos et al. (2006) have proposedHaNa0.15(H2O)0.45Mn2+,3+0.167(H2O)0.50Mn4+0.833W0.167O2as the empirical formula for the nanoparticulate hexagonal birnessite produced by the model bacterium, Pseudomonas putida (Tebo et al., 2004). In Eq. (1), the metal cations to the left of the square brackets are hydrated interlayer species balancing the negative structural charge created by cation vacancy sites (□) and the stoichiometric coefficient of the proton in the formula (a) varies according to the charge of the interlayer metal cations. External (N2 BET) specific surface areas of 100–220 m2 g−1 have been measured by Villalobos et al., 2003, Duckworth and Sposito, 2007 for this mineral. Biogenic birnessite minerals are typically found enmeshed in an organic matrix of bacterial cells and extracellular polymeric substances (Tebo et al., 2004, Tebo et al., 2005, Toner et al., 2005a), thus forming heterogeneous biomass-mineral assemblages that contain a variety of reactive organic functional groups, such as –COOH, –CHOH, –PO4H3, –SH, and –NH2 (Fein et al., 2001, Warren and Haack, 2001, Toner et al., 2005b, Sposito, 2008), as well as mineral sorption sites.

Besides the retention of Ni on birnessite precipitated in soils or sediments of metal-impacted ecosystems, ferromanganese nodules can accumulate up to percent levels of Ni by mass (Manceau et al., 1987, Manceau et al., 2007a, Bodei et al., 2007). In nodules from marine (Bodei et al., 2007, Peacock and Sherman, 2007a), freshwater (Manceau et al., 2007a), and soil environments (Manceau et al., 2002b, Manceau et al., 2003), Ni was present as a divalent cation incorporated into the octahedral sheets of layer-type Mn(IV) oxide minerals (Ni-inc, Fig. 1a). Analysis of the Ni K-edge extended X-ray absorption fine structure (EXAFS) spectra of various nodule samples (Manceau et al., 2002a, Bodei et al., 2007, Peacock and Sherman, 2007a) showed that Ni is in an edge-sharing configuration with respect to Mn(IV) octahedra and has a shell of Mn nearest-neighbors at 2.9 Å.

In contrast to the speciation of Ni in ferromanganese nodules, adsorption—not incorporation—was found to be the dominant mechanism of Ni sorption by birnessite-coated sand grains in a groundwater filter (Manceau et al., 2007b), where 65% of the total Ni (0.33 wt%) was bound as a triple-corner-sharing surface complex (Ni-TCS, Fig. 1b) at cation vacancy sites, while 25% was incorporated into the sheet structure, as inferred from EXAFS-derived Ni–Mn interatomic distances of 3.5 and 2.9 Å, respectively. These two coordination environments also were observed by Manceau et al., 2007b, Peacock and Sherman, 2007b, Peacock, 2009 for Ni sorbed by δ-MnO2 and hexagonal birnessite (H+-exchanged hexagonal birnessite prepared by acidifying crystalline triclinic Na-birnessite to pH 2), respectively, at very low Ni:Mn molar ratio (⩽0.01). At pH 4, Ni was bound predominantly as a TCS complex (>90%), whereas at pH 7, variable extents of Ni incorporation (10–45%) were observed in samples with a 0.01 Ni:Mn molar ratio, suggesting that increased pH favors incorporation. Moreover, Peacock (2009) showed that the fraction of Ni-inc increased to 20% when samples initially equilibrated at pH 4 for 24 h were exposed to an electrolyte solution maintained at pH 7 for either 24 or 120 h and that, as the contact time increased from 24 to 408 h in samples prepared at pH 7, the fraction of Ni-inc increased from 10% to 30%. However, even greater Ni incorporation (45%) was observed after the short equilibration time of 12 h in a δ-MnO2 sample prepared at pH 7 and a 0.01 Ni:Mn molar ratio (Manceau et al., 2007b).

The literature reviewed above indicates that, at low Ni:Mn molar ratios, Ni sorbs to hexagonal birnessite either by becoming incorporated into the MnO2 sheet (Ni-inc, Fig. 1a) or by forming triple-corner-sharing surface complexes at vacancy sites (Ni-TCS, Fig. 1b), with the former sorption mechanism found to be dominant in ferromanganese nodules and the latter dominant in laboratory-synthesized hexagonal birnessite samples that are equilibrated with Ni-containing solutions for relatively short times when compared to the timescales over which ferromanganese nodules accrue. Although high pH favors Ni-inc, the extent of Ni-inc observed in chemically-synthesized birnessite samples has been quite variable (10–45% of the total Ni). Thus, besides pH and contact time, the formation of Ni-TCS versus Ni-inc in hexagonal birnessite must be influenced by other variables, e.g., structural disorder in the mineral. Differences between the hexagonal birnessite minerals studied by Manceau et al., 2007b, Peacock, 2009 arise with respect to both specific surface area and structural disorder, with the δ-MnO2 sample employed by Manceau et al. (2007b) having a greater surface area and lacking sheet-stacking order along the c-axis direction. The vacancy content of the two birnessites may also differ, with crystalline hexagonal birnessite having a vacancy content of 16.7% (Lanson et al., 2000), which is near the upper limit for δ-MnO2, whose vacancy content lies between 6% and 18% (Villalobos et al., 2006, Grangeon et al., 2008).

In this paper, we attempt to clarify the mechanisms of Ni sorption by a systematic investigation of a single biogenic hexagonal birnessite using a synergistic experimental–theoretical approach. The bacteriogenic birnessite precipitated by P. putida was selected for study because its structure is well characterized and it can be synthesized with good replication (Villalobos et al., 2003, Villalobos et al., 2006). We performed batch experiments to quantify the Ni sorption characteristics of P. putida biomass-birnessite assemblages. To determine the local coordination environment of sorbed Ni, we applied EXAFS spectroscopy to samples prepared with various Ni loadings and at pH 6–8. From the interatomic distances (R) and coordination numbers (CN) obtained by fitting the EXAFS spectra, we were able to infer the presence of Ni-TCS and/or Ni-inc, as well as determine the influence of Ni concentration and proton activity on the distribution of the two species. Finally, we investigated the two “end-member” sorbed Ni species, Ni-TCS and Ni-inc, using first-principles geometry optimizations based on density functional theory (Koch and Holthausen, 2002, Martin, 2004, Kohanoff, 2006, Kwon et al., 2009) to explore the transition from Ni-TCS to Ni-inc under scenarios of low and high proton activity without the complicating effects of reaction time and structural disorder.

Section snippets

Materials

A.C.S. reagent-grade chemicals were used in all experiments. Solutions were prepared using Milli-Q (MQ) water with a resistivity of 18.2  cm. Birnessite was produced using a P. putida GB-1 culture (Villalobos et al., 2003, Toner et al., 2005a). Microbiological work was carried out in a sterile laminar flow-hood. The bacterial growth medium (Leptothrix medium) was prepared by dissolving solid components in MQ water, autoclaving the solution for 20 min, cooling the autoclaved solution to room

Sorption behavior

Sorption isotherms measured at pH 6 (5.6–6.0) and 7 (6.7–6.9) for the biomass-birnessite assemblage are plotted in Fig. 2. The highest surface excess (q) values measured were 0.32 ± 0.02 mol Ni kg−1 and 0.45 ± 0.01 mol Ni kg−1, at pH 6 and 7, respectively, indicating increasing Ni sorption capacity with increasing pH. Sorption edges measured over the range of pH 6–8 for Ni reacted with the assemblage in both the presence and the absence of its biogenic MnO2 component (Peña, 2009) confirmed the effect of

Acknowledgments

This research was supported by the University of California Toxic Substances Research and Teaching Program as well as by the Director, Office of Energy Research, Office of Basic Energy Sciences of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. Our DFT computations used resources of the National Energy Research Scientific Computing Center, which is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. J. Peña was also

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