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Article

Preferential Elimination of Ba2+ through Irreversible Biogenic Manganese Oxide Sequestration

1
Department of Environmental and Life Sciences, School of Food and Nutritional Sciences, University of Shizuoka, 52-1 Yada, Shizuoka 422-8526, Japan
2
Department of Environmental Health Sciences, Graduate School of Nutritional and Environmental Sciences, University of Shizuoka, 52-1 Yada, Shizuoka 422-8526, Japan
3
Advanced Science Research Center, Japan Atomic Energy Agency, Tokai, Ibaraki 319-1195, Japan
4
Department of Biological Environment, Akita Prefectural University, Shimoshinjo-Nakano, Akita 010-0195, Japan
*
Author to whom correspondence should be addressed.
Minerals 2021, 11(1), 53; https://doi.org/10.3390/min11010053
Submission received: 23 December 2020 / Revised: 5 January 2021 / Accepted: 6 January 2021 / Published: 7 January 2021
(This article belongs to the Special Issue Biogenic Metal Compounds for Hazardous Waste Remediation)

Abstract

:
Biogenic manganese oxides (BMOs) formed in a culture of the Mn(II)-oxidizing fungus Acremonium strictum strain KR21-2 are known to retain enzymatic Mn(II) oxidation activity. Consequently, these are increasingly attracting attention as a substrate for eliminating toxic elements from contaminated wastewaters. In this study, we examined the Ba2+ sequestration potential of enzymatically active BMOs with and without exogenous Mn2+. The BMOs readily oxidized exogenous Mn2+ to produce another BMO phase, and subsequently sequestered Ba2+ at a pH of 7.0, with irreversible Ba2+ sequestration as the dominant pathway. Extended X-ray absorption fine structure spectroscopy and X-ray diffraction analyses demonstrated alteration from turbostratic to tightly stacked birnessite through possible Ba2+ incorporation into the interlayer. The irreversible sequestration of Sr2+, Ca2+, and Mg2+ was insignificant, and the turbostratic birnessite structure was preserved. Results from competitive sequestration experiments revealed that the BMOs favored Ba2+ over Sr2+, Ca2+, and Mg2+. These results explain the preferential accumulation of Ba2+ in natural Mn oxide phases produced by microbes under circumneutral environmental conditions. These findings highlight the potential for applying enzymatically active BMOs for eliminating Ba2+ from contaminated wastewaters.

1. Introduction

Barium is a toxic alkaline earth metal [1,2], and Ba2+ levels have been elevated in many aquatic environments by anthropogenic activities such as mining [3], coal seam gas utilization [4], and shale gas extraction [5,6]. These enhanced Ba levels threaten humans and ecosystems worldwide. Therefore, developing a cost-effective Ba2+ remediation systems requires urgent attention.
In aquatic and terrestrial environments, manganese (Mn) oxide phases readily accumulate Ba2+ and other heavy metal ions such as Ni2+, Co2+, and Zn2+. The preferential accommodation of Ba2+ in the tunnels of tectomanganates such as hollandite (2 × 2) and romanechite (2 × 3) partly explains Ba2+ accumulation in natural Mn oxide phases [7,8,9]. Phyllomanganates such as birnessite and buserite (vernadite) also accumulate Ba2+ under certain environmental conditions [10,11,12,13,14,15], although the underlying mechanisms for Ba2+ accumulation in manganese oxide phases remain uncertain.
Under circumneutral pH conditions, bacterial and fungal Mn oxide formation enzymatically proceeds faster than heterogeneous Mn(II) oxidation catalyzed by mineral surfaces [16,17,18]. The formation of biogenic Mn oxides (BMOs) serves in scavenging heavy metal cations including Zn2+, Ni2+, Co2+, and Pb2+ from aquatic environments because of the high sequestration affinity and capacity of BMOs [19,20,21,22,23,24,25,26,27,28].
According to previous studies [29,30,31], fungal BMOs produced by Acremonium strictum KR21-2 maintain the activity of an Mn(II)-oxidizing enzyme in the oxide phase, and effectively oxidize exogenous Mn2+ to form another BMO phase. This process significantly enhances the efficiency of heavy metal [32,33,34,35] and rare-earth metal [36,37] sequestration by providing new sorption sites and minimizing competition for exogenous Mn2+ sorption. In addition, enzymatically active BMOs improve the indirect oxidation efficiencies of As(III) to As(V) [30], Co(II) to Co(III) [33], and Cr(III) to Cr(VI) [38] through continuous reoxidation of reduced Mn2+, which is one of the causes of surface passivation. Consequently, in addition to the high sequestration capacity and oxidizing ability, enzymatically active BMOs exhibit a potential for a continuous remediation of contaminated wastewaters as well as metal recovery.
The aims of this study were to examine the Ba2+ sequestration process associated with enzymatic BMO formation and to elucidate factors for the preferential accumulation of this ion in Mn oxide phases in the environment. The BMO alteration linked to the Ba2+ sequestration is also discussed relative to the sequestration reversibility and selectivity for alkali earth metal ions such as Sr2+, Ca2+, and Mg2+. The results of this study demonstrate the potential application of enzymatically active BMOs for Ba2+ removal from contaminated wastewaters.

2. Materials and Methods

A. strictum KR21-2, which enzymatically oxidizes Mn(II) to BMOs [39,40,41], was incubated at 25 °C in a HAY liquid medium (pH of 7.0) supplemented with 1 mM Mn2+, as described previously [29,32,33,34], slightly modified by using Mn(NO3)2 instead of MnSO4. After 72 h of incubation, BMOs with fungal mycelia were harvested and washed thrice with 20 mM 4-(2-hydroxyethyl)–1–piperazineethanesulphonic acid (HEPES) buffer (pH of 7.0 adjusted using NaOH). These served as the “newly formed BMOs” for Ba2+ sequestration experiments within 1 h of washing (denoted as “newly formed BMO”).
In the sequestration experiments, all metal ions involved (Mn2+, Ba2+, Sr2+, Ca2+, and Mg2+) were as nitrate salts because Ba2+ readily precipitates with SO42− (the solubility product, Ksp, of BaSO4 is 10−9.97 [42]). The enzymatically active newly formed BMOs (1 mM as Mn) were mixed with 0–10 mM Ba(NO3)2 with or without 1 mM Mn(NO3)2 in 20 mM HEPES buffer (50 mL) at a pH of 7.0 (adjusted using NaOH) under air-equilibrated (aerobic) conditions at 25 °C on a reciprocal shaker at 105 strokes·min−1 (NR–10, Taitec, Nagoya, Aichi, Japan). To maintain aerobic conditions, we used 100 mL Erlenmeyer flasks with cotton stoppers. This procedure was performed thrice, with the bathing solution renewed every 24 h. To elucidate the effects of the Mn(II) oxidase activity in the BMOs, we inactivated the associated Mn(II) oxidase by heating the newly formed BMOs for 2 h in a water bath (Thermo Minder Mini-80, Taitec, Nagoya, Aichi, Japan) at 85 °C [29], followed by cooling of the samples to room temperature at around 20 °C (denoted as “heated BMO” hereafter). These cooled samples were collected, washed thrice with a 20 mM HEPES buffer at pH of 7.0, and used in the Ba2+ sequestration experiments under aerobic conditions. To compare the sequestration properties of the alkaline earth metal ions, we also conducted experiments with solutions of Sr2+, Ca2+, and Mg2+ in the 20 mM HEPES buffer. For competitive sequestration experiments, newly formed BMOs were treated thrice in mixed solutions of Ba2+ with Sr2+, Ca2+, or Mg2+, and with or without exogenous Mn2+. In all sequestration experiments, supernatants were sampled at 0, 2, 8, 16, and 24 h for each treatment and separated using a centrifugal filter unit (Durapore PVDF 0.1 μm, Merk Millipore, Burlington, MA, USA; 12,000× g for 2 min). The dissolved metal concentrations of the supernatants were measured using a 730-ES inductivity coupled plasma atomic emission spectrometer (ICP-AES, Agilent Technology, Santa Clara, CA, USA).
The two-step extraction protocol in this study involved using aqueous 10 mM Cu(NO3)2 (pH of 4.8) and 50 mM hydroxylamine hydrochloride for speciation of the Ba2+ and Mn2+ sequestered by the BMOs, as described previously [29,32,33,34]. This extraction sequence commonly serves for fractionating adsorbed Mn(II) and oxidized Mn from BMOs [43,44,45]. The Ba2+ and other alkaline earth metal ion fractions dissolved in aqueous Cu(NO3)2, and the subsequent hydroxylamine hydrochloride extracts were termed as exchangeable (reversible) and reducible (irreversible) fractions, respectively. The metal concentrations in the extracts were also determined using ICP-AES after dilution with 1.0 M HNO3. The total metal ions extracted via this two-step extraction sequence is hereafter referred to as “solid”. All the sequestration and extraction experiments were conducted in triplicate (n = 3), and data in the figures and tables are shown as mean ± standard deviation.
X-ray diffraction (XRD) measurements were performed for the BMOs using a Rigaku Rint2500 diffractometer (Akishima, Tokyo, Japan) involving CuKα radiation at 26 mA and 40 kV. Lyophilized BMO samples were placed on a glass holder and scanned over a 2θ range of 5–70° at 1.0° min−1 using a 0.02° step interval. The diffractograms were smoothed using a 10-point moving average to enhance the display of broad peaks.
Manganese K-edge extended X-ray absorption fine structure (EXAFS) data for the BMO samples were obtained at the BL12C in the Photon Factory, KEK (Tsukuba, Japan). Lyophilized BMO samples were diluted and adequately mixed with boron nitride (BN). After homogenization, the mixed BMO–BN powders were pressed into discs of appropriate thicknesses for EXAFS measurements in the transmission mode. The intensities of the incident and transmitted X-rays were monitored at room temperature using ionization chambers. Conversely, Barium K-edge EXAFS data for the BMOs treated with Ba2+ were measured at the BL01B1 in the SPring-8 facility (Hyogo, Japan). The lyophilized samples for the Ba-edge EXAFS were also pressed to form discs, without BN dilution. The EXAFS data were also generated in the transmission mode using ionization chambers and analyzed using ver. 2.5.9 of REX2000 (Rigaku Co. Ltd., Akishima, Tokyo, Japan).

3. Results and Discussion

3.1. Exogenous Mn2+ Oxidation by Newly Formed BMOs

Under aerated (air-equilibrated) conditions, the newly formed BMOs (1 mM Mn) readily converted 1 mM exogenous Mn2+ to solid phase Mn in 20 mM HEPES at a pH of 7.0 (cumulative sequestration efficiency > 98.7 ± 0.1%) and subsequently produced another solid phase (Figure S1A and Table S1). Two-step extraction experiments confirmed that these solid phases mainly comprised reducible (oxidized) Mn (>84.2 ± 0.1%) with minor (<15.8 ± 0.1%) exchangeable Mn2+ after every 24 h in the repeated treatment (Figure S1B). The XRD patterns of the newly formed BMOs are characterized by broad peaks for the (001) and (002) basal reflections at ~7.4 and ~3.6 Å, respectively (Figure S2a), indicating a turbostratic birnessite structure [45]. These patterns were maintained even after repeated exogenous Mn2+ oxidation (Figure S2b–d).

3.2. Ba2+ Sequestration by Newly Formed or Heated BMOs with Exogenous Mn2+

After adding newly formed BMOs (1 mM as Mn) to a mixture of 1 mM Mn(NO3)2 and 1 mM Ba(NO3)2 (20 mM HEPES at a pH of 7.0), the exogenous Mn2+ concentrations decreased over time, with >99% subsequently converted to solid Mn upon termination of each treatment (Figure 1A and Table S1). Two-step extraction data also revealed that oxidized (reducible) Mn dominated the solid Mn phase throughout the repeated treatment (93.4 ± 0.1% to 94.7 ± 0.5%) (Figure 1D), indicating active Mn oxide formation by the newly formed BMOs. In fact, dissolved Ba2+ was efficiently sequestered, with the content reducing from 27.0 ± 0.5% upon the initial treatment to 10.0 ± 0.3% after the third treatment (Figure 1A). The cumulative Ba2+ concentration increased by up to 0.45 ± 0.00 mM (Figure 1C) (the cumulative efficiency was 16.1 ± 0.0%, Table S1). The molar ratio of the sequestered Ba2+ relative to the oxidized Mn (Ba2+seq/Mnoxide) was 11.9 ± 0.1 mol % at the end of the repeated treatment.
In contrast, upon treatment with heated BMOs, the exogenous Mn2+ slightly reduced (Figure 1B), thereby minimally increasing the solid Mn phase (Figure 1D). This behavior is attributed to the lack of enzymatic Mn(II) oxidation ability of the heated BMOs [29]. The dissolved Ba2+ concentration also slightly decreased, producing a minor cumulative Ba2+ sequestration of 0.04 ± 0.01 mM (efficiency ≈ 1.4%; Figure 1C). Here, a significantly lower Ba2+seq/Mnoxide ratio (3.7 ± 0.5 mol %) was obtained, indicating competitive sorption of unreacted exogenous Mn2+ (Figure 1B) and Ba2+ on the BMO surface, as previously demonstrated for heavy metal ion sequestration [32,34]. Consequently, the enzymatic Mn2+ oxidation ability enhanced the Ba2+ sequestration efficiency not only by preparing new accommodation sites, for example, a new BMO phase, but also by minimizing the impact of exogenous Mn2+ as a sorption competitor. In fact, newly formed BMOs without exogenous Mn2+ produced the highest Ba2+seq/Mnoxide ratio of 19.5 ± 0.9 mol %, with the cumulative sequestered Ba2+ concentration limited to 0.19 ± 0.01 mM (Figure S3 and Table S1), which is significantly lower than that with 1 mM exogenous Mn2+ (0.45 ± 0.00 mM; Figure 1C).
Interestingly, the two-step extraction data revealed Ba2+ sequestration reversibility differences between the newly formed and heated BMOs. In the newly formed BMOs, the total sequestered Ba2+ contained up to 40.7 ± 0.1% irreversible Ba2+ (extracted as the reducible phase) (Figure 1D and Table S1), whereas for the heated BMOs, the sequestered Ba2+ was mainly extracted as exchangeable Ba2+ (90.3 ± 0.9 to 83.6 ± 0.0%) during the repeated treatment (Figure 1D). Similar trends were observed for initial Ba2+ concentrations ranging from 0.15 to 10 mM and 1 mM exogenous Mn2+ (Figure 2). In fact, at initial Ba2+ concentrations of 0.15, 3, and 10 mM, irreversible Ba2+ represents 58.3 ± 1.2%, 44.1 ± 0.6%, and 44.4 ± 0.6% sequestration on the newly formed BMOs, respectively (Figure 2 and Table S1). However, for the Ba2+ sequestered by the heated BMOs, exchangeable Ba2+ makes up 76.3 ± 0.5%, 82.1 ± 0.5%, and 82.5 ± 0.4% for corresponding initial Ba2+ concentrations (Figure 2 and Table S1). In addition, even for the newly formed BMOs, irreversible Ba2+ incorporation is scarce without exogenous Mn2+ addition, with >93% of the sequestered Ba2+ as exchangeable Ba2+ (Figure S3D).
Linear correlations between the amounts of irreversible Ba2+ and reducible (oxidized) Mn in the solid phase (R2 > 0.97) were observed throughout the repeated treatments (Figure 2D). From the slopes of the linear relationship curves, molar ratios of the irreversible Ba2+ to the additional oxidized Mn phase from the exogenous Mn2+ increased from 0.062, 0.080, and 0.107 to 0.127 as the initial Ba2+ concentrations increased from 0.15, 1, and 3 to 10 mM, respectively (Figure 2D inset). Considering the incorporation of irreversible Ba2+ into the additional Mn oxide phase, 16.2, 12.5, 9.4, and 7.9 moles of oxidized Mn accommodated 1 mole of irreversible Ba2+, on average, as the initial Ba2+ concentrations changed from 0.15, 1, and 3 to 10 mM, respectively. Although isomorphic substitution with structural Mn4+ is reported to cause irreversible sequestration of Ni2+ [34], this is impossible for Ba2+ because of its significantly higher ionic radius (1.49–1.75 Å [46]) compared to that of Mn4+ (0.53–0.67 Å [46]).

3.3. BMO Alteration from Turbostratic to Tightly Stacked Birnessite

The Mn K-edge EXAFS data for the newly formed BMOs (untreated) were similar to those of chemically synthesized δ-MnO2 (Figure 3). This is consistent with the fact that the original BMOs were turbostratic analogues of birnessite [47]. Even after adding the exogenous Mn2+, the newly formed BMOs maintained the EXAFS oscillations throughout the repeated treatment in 10 mM Ba2+ (Figure 3). This indicated no remarkable alteration in the structural alignment of Mn in the resultant BMOs, although the Ba2+ sequestration reversibility largely became irreversible. This behavior is inconsistent with the formation of tectomanganates such as hollandite (2 × 2) and romanechite (2 × 3). These naturally occurring Mn oxides are considered the most suitable for accommodating Ba2+ because of their tunnel structures [7,9,11,28]. Therefore, we inferred that under the experimental conditions in this study, the coexisting Ba2+ failed to directly stimulate tectomanganate formation through enzymatic Mn(II) oxidation. However, some studies have reported direct tectomanganate formation from biogenic Mn oxide processes. Webb et al. [48], for example, reported pseudo-tunnel structures (todorokite-like), with UVIO22+ serving as a template ion, during Mn oxide biogenesis by Bacillus sp. SG-1. In addition, Saratovsky et al. [49] reported todorokite-like biogenic Mn oxides from Acremonium KR21-2 in solid agar media.
The XRD patterns of the newly formed BMOs repeatedly treated in Ba2+ and exogenous Mn2+ are typical of birnessite (Figure 4). As the initial Ba2+ concentration increased, the peak intensities for the (001) and (002) basal reflections also significantly increased, especially the (002) reflection peak. The full width at half maximum (FWHM) of basal reflections for the resulting BMOs narrowed in comparison to those of the newly formed BMOs treated with exogenous Mn2+ without Ba2+, indicating tighter layer stacking as the irreversible Ba2+ content increased. In addition to Mn K-edge EXAFS results (see above), the XRD results confirmed minor alteration from turbostratic to tightly stacked (well-ordered along the c-axis) birnessite, with subsequent irreversible Ba2+ accommodation, possibly into the interlayer space. This observation is consistent with the absence of alteration in the diffractogram for exchangeable Ba2+ removal using the Cu(II) procedure (Figure S4).
Without exogenous Mn2+, the repeated treatment in Ba2+ solutions at 1 and 10 mM significantly weakened the (001) and (002) basal reflection peaks (Figure S5), suggesting that Ba2+ sequestration on the “preformed” BMOs increased the disorder in its turbostratic structure along the c-axis hosting most reversible Ba2+. Xhaxhiu [50] demonstrated that a chemically synthesized turbostratic Na+–birnessite readily changes to phyllomanganate with disorder along the c-axis after treatment in a Ba2+ solution. In addition to the loss of the (001) and (002) peaks by the heated (enzymatically inactivated) BMOs upon treatment in Ba2+, even with exogenous Mn2+ (Figure 4), we conclude that active Mn oxide formation and coexistence with Ba2+ are prerequisites for producing tightly stacked birnessite sheets, with irreversible Ba2+ incorporation in the interlayer.
Analysis of the Ba K-edge EXAFS data strongly supports the irreversible Ba2+ incorporation into the interlayer of the tight birnessite structure. The newly formed BMOs treated thrice in 10 mM Ba2+ with and without exogenous Mn2+ (1 mM) displayed similar EXAFS oscillations (Figure 5), with their radial structural functions (RSFs) indicating Ba–O shells at R + ∆R = 2.1 Å. The newly formed BMOs treated with Ba2+ and exogenous Mn2+ also exhibited small peaks attributed to the Ba–Mn scattering path at R + ∆R = 3.6 Å. The second shell of Ba–Mn scattering was clearer after the extraction using a 10 mM Cu(NO3)2 solution for removing exchangeable (reversible) Ba2+. This indicates that the irreversible Ba2+ on the BMOs created an inner-sphere complex in association with dehydration. The complex suggests covalent bonding of Ba2+ to the oxygen atoms of the MnO6 octahedra at interlayer sites. This strong Ba2+ bonding is probably irreversible, and it stimulated the structure development of tightly stacked birnessite. Further studies are needed to clarify the atomic-level Ba2+ incorporation mechanism during enzymatic Mn(II) oxide formation.

3.4. Sr2+, Ca2+, and Mg2+ Sequestration by Newly Formed or Heated BMOs Involving Exogenous Mn2+

To determine if irreversible sequestration during active Mn oxide formation is specific for Ba2+ or if it is possible for other alkaline earth metal ions, we treated newly formed BMOs (1 mM Mn) thrice in 10 mM Sr2+, Ca2+, or Mg2+, including exogenous 1 mM Mn2+ (20 mM HEPES at pH of 7.0). For all alkaline earth metal ions, the exogenous Mn2+ was converted to solid Mn with an efficiency > 97% after every 24 h, with reducible Mn exceeding 89%, confirming retention of the Mn(II) oxidation efficiency (Figure 6). The Sr2+ sequestered was 0.31 ± 0.01, 0.40 ± 0.05, and 0.48 ± 0.05 mM after the first, second, and third treatments, respectively, with exchangeable (reversible) Sr2+ exceeding 98% (Figure 6 and Table S2). Exchangeable Ca2+ also dominated the sequestered Ca2+ (>94.5%) with the totals (0.28 ± 0.05, 0.37 ± 0.01, and 0.51 ± 0.03 mM) close to those for Sr2+ (Figure 6 and Table S2). However, the sequestered quantities of Mg2+ (0.18 ± 0.03, 0.37 ± 0.02, and 0.41 ± 0.01 mM, respectively) were lower, with a higher exchangeable fraction of >82% (Figure 6 and Table S2). These results indicate that the sequestration of these ions on the newly formed BMOs is controlled primarily by reversible sorption, even with simultaneous exogenous Mn2+ oxidation. In addition, all BMOs produce XRD patterns typical of turbostratic birnessite, with the (001) and (002) basal peaks broader than those of the tightly stacked birnessite-type BMOs involving irreversible Ba2+ (Figure 7). Therefore, the high irreversible sequestration appears to be limited to Ba2+.

3.5. Active Mn2+ Oxidation Sequestration Selectivity Enhancement for Ba2+

To assess the sequestration selectivity among the alkaline earth metal ions, we conducted competitive sequestration experiments in a solution containing 1 mM Ba2+, 1 mM Sr2+, and 1 mM exogenous Mn2+ (20 mM HEPES at pH 7.0) using the newly formed BMOs (1 mM Mn). After three treatments, with renewal of the bathing solution every 24 h, the exogenous Mn2+ was converted to the solid phase (>99% efficiency), with reducible Mn dominating (>92.0 ± 0.5%; Figure 8), indicating active Mn oxide formation. The sequestration efficiency for Ba2+ was 24.6 ± 1.2%, 12.5 ± 0.3%, and 10.4 ± 0.9% for the first, second, and third treatment (cumulative efficiency 15.8 ± 0.8%), respectively (Table S3). The sequestration efficiencies of 5.5 ± 0.4%, <1%, and <1% (cumulative ~0.7%), respectively, for Sr2+ were significantly lower. The two-step extraction produced Ba2+seq/Sr2+seq molar ratios for the resultant BMO phase ranging from 4.9 to 9.1 (Figure 8D), highlighting a clear increase with renewal of the bathing solution. Similar trends were observed for Ba2+/Ca2+ and Ba2+/Mg2+ with exogenous Mn2+, with Ba2+seq/Ca2+seq and Ba2+seq/Mg2+seq molar ratios increasing from 7.1 to 10.6 and from 13.1 to 31.2, respectively (Figure 8D). Evidently, even in the competitive sequestration experiments, the proportion of irreversible (reducible) Ba2+ significantly increased as the exogenous Mn2+ progressed (Figure 8B), while the coexisting Sr2+, Ca2+, and Mg2+ were sequestered mostly as exchangeable fractions (Figure 8C). For example, the reducible Ba2+ increased from 26.6 ± 1.5% to 40.3 ± 0.3% and then to 46.8 ± 0.3%, while exchangeable Sr2+ dominated the sequestered Sr2+ (>99%) throughout the experiment (Table S3).
Competitive sequestration experiments without exogenous Mn2+ also revealed that exchangeable Ba2+ was dominant in the sequestered Ba2+ (>94.4%) (Figure 9B and Table S3), consistent with the Ba2+ restricted sequestration experiments. Most Sr2+, Ca2+, and Mg2+ sequestered were also in the exchangeable fractions (Figure 9C). The Ba2+seq/Sr2+seq, Ba2+seq/Ca2+seq, and Ba2+seq/Mg2+seq molar ratios were, however, lower than those with exogenous Mn2+, ranging from 4.3 to 5.1, 4.1 to 5.1, and 5.7 to 6.5, respectively (Figure 9D). Consequently, the reversible Ba2+ sequestration by the preformed BMOs caused lower Ba2+ selectivity compared to the irreversible Ba2+ sequestration into tightly stacked birnessite-type BMOs.
The XRD patterns of the newly formed BMOs treated thrice in a mixture of 1 mM Ba2+ and 1 mM Sr2+ resembled those for BMOs treated in the 1 mM Ba2+ solution more than those for BMOs treated in the 1 mM Sr2+ solution (Figure S6). This confirms that only Ba2+ was irreversibly incorporated, even in the competitive sequestration experiments. The biological Ba2+ sequestration process is likely in environments with simultaneous supply of Mn2+ and Ba2+, which subsequently contributes to Ba2+ accumulation in birnessite-type Mn oxides.

4. Conclusions

In this study, we present results showing that irreversible Ba2+ sequestration predominates during simultaneous enzymatic Mn oxidation. This process is a likely pathway for Ba2+ sequestration into naturally occurring Mn oxide phases, with microbial (enzymatic) activity occasionally catalyzing the process in the environment. Irreversible sequestration was limited to Ba2+, with Sr2+, Ca2+, and Mg2+ characterized by reversible sequestration, thereby explaining the preferential accumulation of Ba2+ in Mn oxide phases in the environment. These findings improve understanding of the role of biogenic Mn oxidation in natural Ba2+ cycling, particularly under conditions in which microbial Mn(II) oxidation dominates abiotic processes. The insights from this study also highlight the potential of enzymatically active BMOs for scavenging Ba2+ from contaminated wastewaters.

Supplementary Materials

The following are available online at https://www.mdpi.com/2075-163X/11/1/53/s1: Figure S1: Mn2+ oxidation by newly formed BMOs in Mn(NO3)2. Figure S2: XRD patterns of newly formed BMOs treated with Mn(NO3)2. Figure S3: Repeated treatment of newly formed BMOs Ba(NO3)2. Figure S4: Effect of Cu2+-extraction on XRD patterns of newly formed and heated BMOs. Figure S5: XRD patterns of newly formed BMOs treated with Ba(NO3)2. Figure S6: XRD patterns of newly formed BMOs treated with mixed solutions of Ba(NO3)2 and Sr(NO3)2. Table S1: Data summary of sequestration experiments for Ba2+. Table S2: Data summary of sequestration experiments for Sr2+, Ca2+, or Mg2+. Table S3: Data summary of competitive sequestration experiments.

Author Contributions

Conceptualization, Y.T. and N.M.; methodology, Y.T., K.T. and N.M.; validation, Y.T., S.K., J.C., K.T. and N.M.; formal analysis, S.K. and J.C.; investigation, Y.T., K.T. and N.M.; data curation, Y.T., S.K. and J.C.; writing—original draft preparation, Y.T.; writing—review and editing, Y.T., K.T. and N.M.; visualization, Y.T.; supervision, Y.T.; project administration, Y.T.; funding acquisition, Y.T. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Japan Society of the Promotion of Science, JSPS KAKENHI, no. 20K12222 (Y.T.).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available in the Supplementary Materials (Tables S1–S3).

Acknowledgments

We would like to thank Editage for the editing assistance. The EXAFS measurements were performed with the approval of the Photon Factory, KEK (proposal no. 2018G111) and SPring-8 (proposal no. 2018B1012).

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Illustration of the repeated treatment of the (A) newly formed and (B) heated biogenic manganese oxides (1 mM Mn) with mixtures of 1 mM Ba(NO3)2 and 1 mM Mn(NO3)2 in 20 mM 4-(2-hydroxyethyl)–1–piperazineethanesulphonic acid (HEPES) (pH of 7.0). (C) Cumulative concentration of the sequestered Ba2+ and (D) exchangeable and reducible Ba and Mn in the solid phases, assessed via the two-step extraction. Bathing solutions were renewed every 24 h (indicated by arrows).
Figure 1. Illustration of the repeated treatment of the (A) newly formed and (B) heated biogenic manganese oxides (1 mM Mn) with mixtures of 1 mM Ba(NO3)2 and 1 mM Mn(NO3)2 in 20 mM 4-(2-hydroxyethyl)–1–piperazineethanesulphonic acid (HEPES) (pH of 7.0). (C) Cumulative concentration of the sequestered Ba2+ and (D) exchangeable and reducible Ba and Mn in the solid phases, assessed via the two-step extraction. Bathing solutions were renewed every 24 h (indicated by arrows).
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Figure 2. Diagram showing the two-step extraction of Ba2+ and Mn from the newly formed and heated biogenic manganese oxides through repeated treatment with mixtures of (A) 0.15 mM, (B) 3 mM, and (C) 10 mM Ba(NO3)2 with 1 mM Mn(NO3)2 in 20 mM HEPES (pH of 7.0). (D) Plot displaying linear relationships between the extracted Ba and Mn in reducible phases, with the inset showing the Ba/Mn molar ratios as a function of the initial Ba2+ concentration.
Figure 2. Diagram showing the two-step extraction of Ba2+ and Mn from the newly formed and heated biogenic manganese oxides through repeated treatment with mixtures of (A) 0.15 mM, (B) 3 mM, and (C) 10 mM Ba(NO3)2 with 1 mM Mn(NO3)2 in 20 mM HEPES (pH of 7.0). (D) Plot displaying linear relationships between the extracted Ba and Mn in reducible phases, with the inset showing the Ba/Mn molar ratios as a function of the initial Ba2+ concentration.
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Figure 3. Mn K-edge extended X-ray absorption fine structure spectra for the newly formed biogenic Mn oxides (BMOs) treated with and without 10 mM Ba(NO3)2 and 1 mM Mn(NO3)2. δ-MnO2 was plotted as a reference phyllomanganate for comparison.
Figure 3. Mn K-edge extended X-ray absorption fine structure spectra for the newly formed biogenic Mn oxides (BMOs) treated with and without 10 mM Ba(NO3)2 and 1 mM Mn(NO3)2. δ-MnO2 was plotted as a reference phyllomanganate for comparison.
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Figure 4. X-ray diffractograms from analysis of the newly formed and heated biogenic manganese oxides (1 mM as Mn) treated thrice with mixtures of Ba(NO3)2 (0–10 mM) and 1 mM Mn(NO3)2 in 20 mM HEPES (pH 7.0). The bathing solutions were renewed every 24 h.
Figure 4. X-ray diffractograms from analysis of the newly formed and heated biogenic manganese oxides (1 mM as Mn) treated thrice with mixtures of Ba(NO3)2 (0–10 mM) and 1 mM Mn(NO3)2 in 20 mM HEPES (pH 7.0). The bathing solutions were renewed every 24 h.
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Figure 5. Ba K-edge EXAFS spectra of the newly formed BMOs treated in 10 mM Ba(NO3)2 with and without 1 mM Mn(NO3)2, highlighting the (A) EXAFS oscillations and (B) corresponding radial structural functions (RSFs). The irreversible fraction indicates the Ba2+ left on the BMO after extracting the reversible Ba2+ fraction using 10 mM Cu(NO3)2.
Figure 5. Ba K-edge EXAFS spectra of the newly formed BMOs treated in 10 mM Ba(NO3)2 with and without 1 mM Mn(NO3)2, highlighting the (A) EXAFS oscillations and (B) corresponding radial structural functions (RSFs). The irreversible fraction indicates the Ba2+ left on the BMO after extracting the reversible Ba2+ fraction using 10 mM Cu(NO3)2.
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Figure 6. Illustration of the two-step extraction of Ba2+ and Mn from the newly formed biogenic manganese oxides during repeated treatment with mixtures of 10 mM Ba(NO3)2, Sr(NO3)2, Ca(NO3)2, or Mg(NO3)2 with 1 mM Mn(NO3)2 in 20 mM HEPES (pH of 7.0). The bathing solutions were renewed thrice every 24 h. The conversion (%) from Mn2+ to solid Mn is displayed in the top panel.
Figure 6. Illustration of the two-step extraction of Ba2+ and Mn from the newly formed biogenic manganese oxides during repeated treatment with mixtures of 10 mM Ba(NO3)2, Sr(NO3)2, Ca(NO3)2, or Mg(NO3)2 with 1 mM Mn(NO3)2 in 20 mM HEPES (pH of 7.0). The bathing solutions were renewed thrice every 24 h. The conversion (%) from Mn2+ to solid Mn is displayed in the top panel.
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Figure 7. X-ray diffraction analysis of newly formed biogenic manganese oxides (1 mM as Mn) with mixed solutions of 10 mM Ba(NO3)2, Sr(NO3)2, C(NO3)2, or Mg(NO3)2 with 1 mM Mn(NO3)2 in 20 mM HEPES (pH 7.0). Bathing solutions were renewed thrice every 24 h.
Figure 7. X-ray diffraction analysis of newly formed biogenic manganese oxides (1 mM as Mn) with mixed solutions of 10 mM Ba(NO3)2, Sr(NO3)2, C(NO3)2, or Mg(NO3)2 with 1 mM Mn(NO3)2 in 20 mM HEPES (pH 7.0). Bathing solutions were renewed thrice every 24 h.
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Figure 8. Diagram showing the two-step extraction of (A) Mn; (B) Ba; and (C) Sr, Ca, or Mg from the newly formed biogenic manganese oxides during repeated treatments with mixed solutions of 1 mM Ba(NO3)2 and 1 mM Mn(NO3)2 in 20 mM HEPES (pH of 7.0) with 1 mM Sr(NO3)2, Ca(NO3)2, or Mg(NO3)2. The bathing solutions were renewed thrice every 24 h. (D) Plot of the Ba/Sr, Ba/Ca, and Ba/Sr molar ratios in the solid phases demonstrating sequestration selectivity.
Figure 8. Diagram showing the two-step extraction of (A) Mn; (B) Ba; and (C) Sr, Ca, or Mg from the newly formed biogenic manganese oxides during repeated treatments with mixed solutions of 1 mM Ba(NO3)2 and 1 mM Mn(NO3)2 in 20 mM HEPES (pH of 7.0) with 1 mM Sr(NO3)2, Ca(NO3)2, or Mg(NO3)2. The bathing solutions were renewed thrice every 24 h. (D) Plot of the Ba/Sr, Ba/Ca, and Ba/Sr molar ratios in the solid phases demonstrating sequestration selectivity.
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Figure 9. Diagram showing the two-step extraction of (A) Mn; (B) Ba; and (C) Sr, Ca, or Mg from the newly formed biogenic manganese oxides during repeated treatment with mixtures of 1 mM Ba(NO3)2 and 1 mM Sr(NO3)2, Ca(NO3)2, or Mg(NO3)2 in 20 mM HEPES (pH of 7.0) without exogenous Mn2+. The bathing solutions were renewed thrice every 24 h. (D) Plot of the Ba/Sr, Ba/Ca, and Ba/Sr molar ratios in the exchangeable and solid (exchangeable + reducible) phases showing sequestration selectivity.
Figure 9. Diagram showing the two-step extraction of (A) Mn; (B) Ba; and (C) Sr, Ca, or Mg from the newly formed biogenic manganese oxides during repeated treatment with mixtures of 1 mM Ba(NO3)2 and 1 mM Sr(NO3)2, Ca(NO3)2, or Mg(NO3)2 in 20 mM HEPES (pH of 7.0) without exogenous Mn2+. The bathing solutions were renewed thrice every 24 h. (D) Plot of the Ba/Sr, Ba/Ca, and Ba/Sr molar ratios in the exchangeable and solid (exchangeable + reducible) phases showing sequestration selectivity.
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Tani, Y.; Kakinuma, S.; Chang, J.; Tanaka, K.; Miyata, N. Preferential Elimination of Ba2+ through Irreversible Biogenic Manganese Oxide Sequestration. Minerals 2021, 11, 53. https://doi.org/10.3390/min11010053

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Tani Y, Kakinuma S, Chang J, Tanaka K, Miyata N. Preferential Elimination of Ba2+ through Irreversible Biogenic Manganese Oxide Sequestration. Minerals. 2021; 11(1):53. https://doi.org/10.3390/min11010053

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Tani, Yukinori, Satomi Kakinuma, Jianing Chang, Kazuya Tanaka, and Naoyuki Miyata. 2021. "Preferential Elimination of Ba2+ through Irreversible Biogenic Manganese Oxide Sequestration" Minerals 11, no. 1: 53. https://doi.org/10.3390/min11010053

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