Investigation of the Effect of Manganese Oxides on the Reduction of Hexavalent Chromium by Sodium Alginate-Dispersed Nano-Zero-Valent Iron and the Mechanism

Chromium (Cr) is a prevalent soil contaminant, and sodium alginate-modified nano-zero-valent iron (SA-NZVI) has been studied for the remediation of Cr(VI)-contaminated soils. However, the addition of manganese oxides during remediation may result in the re-release of Cr(VI), and the mechanism behind this process remains unclear. Therefore, this paper investigates the effect of different manganese oxides on the oxidation of Cr(III), the impact of manganese oxide on the reduction products of Cr(VI) and SA-NZVI, and the effect of manganese oxide addition on the remediation of Cr(VI)-contaminated soil by SA-NZVI. Solution incubation experiments, XRD characterization, and soil incubation experiments were conducted to analyze the results. Our findings show that acid birnessite (A-Bir) has the lease of Cr(VI) most influence on Cr(III) oxidation and affects the stability of the SA-NZVI and Cr(VI) reduction products. In the remediation of Cr(VI)-contaminated soils, the presence of A-Bir increases the soil pH and available Mn content and reduces the available Fe content, resulting in the re-release of Cr(VI), but the Cr converted to residue form by SA-NZVI is difficult to oxidize by A-Bir. This study suggests that A-Bir plays a crucial role in the re-release during the remediation of Cr(VI)-contaminated soils by SA-NZVI.


Introduction
Chromium (Cr) is one of the most prevalent contaminants in soil typically found in the valence states of trivalent chromium [Cr(III)] and hexavalent chromium [Cr(VI)] (Coyte et al., 2020). There are differences in the toxicities, mobility, and bioavailability of the two stable oxidation states. Cr(III) has relatively low toxicity and mobility because it often forms hydroxide solids or is adsorbed as complex ion onto mineral surfaces found in soil and water in natural systems. In contrast, Cr(VI) is primarily found as relatively soluble anion (Cr 2 O 7 2− , HCrO 4 − , and CrO 4 2− ). Due to its negative charge and strong oxidation, it is very reactive and mobile . Given that Cr(VI) is known to be mutagenic, teratogenic, and carcinogenic even at very low concentrations (1 mg/kg) in soils, it is highly desired from the perspective of environmental risk that Cr(VI) be converted to Cr(III) (Di Palma et al., 2015;Su et al., 2020), which is non-mobile and less toxic. As a result, substantial research has been conducted on Cr(VI) reduction to mitigate its effects on humans and animals (Ao et al., 2022;Qin et al., 2022).
Among the methods of Cr(VI) remediation that are frequently employed, the application of nanozero-valent iron (NZVI) has been extensively investigated and proven to be feasible and cost-effective (Li et al., 2008). NZVI frequently forms aggregates, significantly decreasing their dissemination in contaminated groundwater and soil. In contrast, sodium alginate-dispersed nano-zero-valent iron (SA-NZVI) has strong dispersion to alleviate the agglomeration problem (Liu et al., 2015;Zhao et al., 2020b). SA-NZVI is a powerful adsorption and reduction material, with numerous studies demonstrating its effectiveness as a reduction fixing material due to its large surface area. It can adsorb significant amount of Cr(VI) while also supplying a lot of electrons to reduce Cr(VI) to Cr(III) quickly and with good reduction effect (Qin et al., 2022). Despite its effectiveness, it has been found that re-release of Cr(VI) can occur after a period of remediation of Cr(VI)-contaminated soil by iron-based materials, possibly due to oxidants in the soil (Li et al., 2019;Wang et al., 2017;Xu et al., 2018). The fact that this condition will cause "secondary contamination" of the environment calls for widespread attention.
Manganese oxides occur naturally as oxidants and are typically found in manganese minerals such as Mn(II), Mn(III), and Mn(IV) (Ao et al., 2022). These minerals are ubiquitous and present in various environmental settings such as soils, sediments, the sea floor, and desert environments, as well as freshwater and marine systems, and trigger redox reactions in these environments. Furthermore, the conversion of Cr(III) to Cr(VI) by solid Mn oxides has been verified by numerous laboratory studies (Landrot et al., 2012;Reijonen & Hartikainen, 2016;Weaver & Hochella, 2003). Among the Mn minerals that can be identified as predominantly Mn(IV), the common ones are birnessite, colemanite, and todorokite (Zhao et al., 2020a). Of these, birnessite is the most prevalent type of layered structural manganese mineral found in soils and sediments, and is made up of co-lateral MnO 6 octahedral structural units with primarily Mn(IV)O 6 valence but also includes some Mn(III) O 6 and Mn(II)O 6 in small numbers. Studies have revealed that birnessite is one of the most potent sorbents in the surface environment and is crucial for oxidation-reduction and sorption-desorption processes in soil, groundwater, marine, and freshwater bodies while facilitating the rapid conversion of Cr(III) to Cr(VI) (Kong et al., 2019;Lu et al., 2019).
SA-NZVI can improve the removal of Cr(VI) from aqueous solutions, but limited research has been conducted on the remediation of Cr(VI)-contaminated soils. Studies have shown that Cr(VI) re-release may occur during remediation of Cr(VI)-contaminated soils, and those manganese oxides are an important substance influencing this phenomenon. However, there is a lack of studies investigating the specific role of manganese oxides in the process of Cr(VI) rerelease. Therefore, we investigated the effect of different manganese oxides on the oxidation of Cr(III), and explored the effect of manganese oxide on the reduction products of Cr(VI) and SA-NZVI and manganese oxide addition on the remediation of Cr(VI)-contaminated soil by SA-NZVI. Through the experimental results, we have obtained a preliminary mechanism by which manganese oxides affect the remediation of Cr(VI)-contaminated soil by SA-NZVI. The findings of this study are important in enhancing our comprehension of the remediation process of Cr(VI)-contaminated soils.

Soil Samples
The experiment soil was collected from topsoil (0-20 cm) of agricultural fields, which were free of pollution, at Guangxi University in Guangxi Province, China. After being allowed to dry naturally, the soil was homogenized in a mortar and put through a 20-mesh sieve. The soil was supplemented with a certain volume of 1000 mg/L aqueous potassium dichromate (K 2 Cr 2 O 7 ) solution, followed by distilled water to reach 60% of the maximum water holding capacity, and then held for another 3 months to ensure full blending. Table 1 displays the physicochemical characteristics of the prepared soil.

Material Preparation
Since birnessite serves as a model compound for manganese oxides and is the main mineral that contains manganese in several soils, acid birnessite (A-Bir) is the most oxidizing, and large specific surface area-birnessite can be synthesized in the laboratory at this time (Dai et al., 2009;Feng et al., 2006). Thus, A-Bir was used as the research subject in the experiment. For synthesis of A-Bir, refer to Xionghan Feng (Feng et al, 2006). After weighing 63.64 g of KMnO 4 dissolved in 600 mL of distilled water, the product was heated and boiled at a constant temperature oil bath of 110 °C with constant stirring, followed by the addition of 100 mL of 6 M HCl solution drop by drop, and the reaction was left to stand for 30 min. Deionized water was used to wash the synthesized material multiple times until the conductivity was less than 20 s/cm. The product was ground and bottled after drying in an oven at 40 °C. The supplementary information provides specifics regarding the basic properties of acid birnessite (Text SI).
This research used a liquid phase reduction process to synthesize SA-NZVI, which has been improved (Liu et al., 2005). The supplementary information provides specifics regarding the SA-NZVI synthesis modifications (Text SI).
Preparation of the Cr(VI) reduction product from SA-NZVI: the product of the reduction of Cr(VI) by SA-NZVI was obtained by weighing 0.015 g SA-NZVI in 50 mL of Cr(VI) solution (30 mg/L), shaking at 120 r/min for 720 min, and then pouring out the supernatant and drying the solid for 24 h in a vacuum freeze drier (Cr-SNZVI).
All of the chemicals employed in this investigation were pure analytical reagents, and the solutions were made with Milli-Q Water Systems' deionized water (Merck Millipore). Chemical reagents include sodium hydroxide, sodium alginate (SA), ferrous sulfate, absolute ethanol, 1,5-diphenylcarbazide, acetone, sodium borohydride, hydrochloric acid, sulfuric acid, and nitric acid, etc.

Oxidation of Cr(III) by Manganese Oxides
Manganese oxide [Mn(II)], manganese tetroxide [Mn(III)], manganese dioxide [Mn(IV)], and A-Bir (δ-MnO 2 ) at 0.4, 0.5, and 0.6 g/L, respectively, were added to 30 mg/L of Cr(III) solution (prepared with 0.01 M NaNO 3 solution to control ionic strength) and shaken horizontally at 120 r/min for 24 h to determine the concentration of Cr (VI) in aqueous solution.

Stability Studies of Manganese Oxides on Reduction Products
At a certain temperature and pH, 0.15 g/L of A-Bir was suspended in 300 mL of NaNO 3 solution at a concentration of 0.01 M for 8-12 h to allow for sufficient hydration of its surface. The pH of the solution was adjusted to 4.4 with HNO 3 and NaOH solution, and the pH variation was maintained within ± 0.01. Cr-SNZVI solid (0.1500 g) was added to 10 mL of A-Bir solution and shaken at 25 °C at 200 r/min for 24 h. The precipitate was washed thoroughly with deionized water and dried in a freeze-drying oven for XRD.

Soil Incubation Experiments
Cr-contaminated soil 50.00 g was weighed into a series of 250 mL plastic bottles. Depending on the kind of reaction, there are four different systems: 1) the control system (blank soil system), 2) the SA-NZVI system (50.00 g of prepared soils were thoroughly mixed with the dry 1% SA-NZVI (w/w) particles), 3) the A-Bir system (50.00 g of prepared soils were thoroughly mixed with the dry 0.5% A-Bir (w/w) particles), and 4) the SA-NZVI + A-Bir system (50.00 g of prepared soils were thoroughly mixed with the dry 1% SA-NZVI and 0.5% A-Bir (w/w) particles).
To prevent excessive evaporation, all of the pots were covered with vented film. Treatments were created in triplicate and incubated for 28 days in the dark at a constant relative humidity of 60-70% and temperature of 25 °C. During this time, the soil moisture was monitored every 2 days using gravimetric measurements. Soil samples were collected at the 7, 14, 21, and 28 days, and all samples were air-dried, crushed, and sieved for measurements of the Cr(VI) leaching concentration. At the end of the incubation, soil pH, available Fe concentration, available Mn concentration, and Cr speciation analyses were determined.

Analytical Methods
After the soil was suspended in distilled water (1:2.5, w/v), the pH of the suspension was measured (VSTAR80; Thermo Fisher). The total Cr in the soil was removed using acidic digesting techniques. The water-soluble Cr was determined according to the National Standard of China (GB/T 25,282-2010), and Cr(VI) in soil was extracted with deionized water using the ratio of soil to water 1:10. Available Fe concentration and available Mn concentration in soil were extracted with 5 mM DTPA (diethylene triamine pentaacetic acid), 0.01 M CaCl 2 , and 0.1 M TEA (triethanolamine) at pH 7.3. Cr(VI) concentration was analyzed by 1,5-diphenylcarbazide spectrophotometry (Rayleigh ultraviolet-1800) (Akter et al., 2016). A flame atomic absorption spectrophotometer was used to measure the available Fe, Mn, and total Cr concentrations in the experiment (AAS, AA-7000; Shimadzu, Japan) (Ao et al., 2022). Extraction of chromium fractions is according to Sut-Lohmann's method (Sut-Lohmann et al., 2022).
Structure identification of synthetic A-Bir was carried out by powder XRD. IBM SPSS Statistics SPSS 25.0 was used for statistical analysis, while Origin 2021 was used to create the figures.

Characteristics of A-Bir
XRD analysis of the synthesized A-Bir revealed diffraction peaks with d values of 0.722, 0.363, 0.245, and 0.141 nm, which matched the diffraction peaks that birnessite is known for, and no other diffraction peaks were present, in agreement with the results of card JCPDS 86-0666 (Fig. 1). The data provided in Table 2 are also used to estimate the parameters of Mn oxidation and the chemical makeup of the produced A-Bir. The manganese oxidation degree was 3.94, and the chemical composition was K 0.27 MnO 2 (H 2 O) 0.54 . These results were consistent with previously published findings (Justin Raj et al., 2022).

Oxidation of Cr(III) by Manganese Oxides
The study investigated the oxidation of Cr(III) by Mn(II), Mn(III), Mn(IV), and A-Bir at various dosing levels to assess the impact of various manganese oxides on the oxidation of Cr(III) (Fig. 2). Results indicated that the oxidation rate of Cr(III) by the same manganese oxide increased with dose, and the total oxidation rate of Cr(III) by various manganese oxides indicated that A-Bir > Mn(III) > Mn(IV) > M n(II). The poorest Cr(III) oxidation capability was demonstrated by Mn(II) manganese oxide, which had a dosage of 0.6 g/L and a 24-h Cr(III) oxidation rate of 15.59%. A-Bir showed the most influence on the oxidation of Cr(III), with an oxidation rate of 88.93% after 24 h, indicating that A-Bir had the biggest impact on the oxidation of Cr(III). Our findings are  consistent with those of Weaver (Weaver & Hochella, 2003) and Feng (Feng et al., 2007a). This is because A-Bir, in the form of a lamellar aggregate, a high-

Stability Studies of Manganese Oxides on Reduction Products
Cr-SNZVI exhibited an alkaline pH of 8.66 and had a total Cr concentration of 30.52 mg/kg. The absence of Cr(VI) indicated that all the Cr in Cr-SNZVI was Cr (III). The crystal structures of Cr-SNZVI consist of chromite (FeCr 2 O 4 ), hematite (Fe 2 O 3 ), and magnetite (Fe 3 O 4 ). The body-centered cubic structure's distinctive peak, α-Fe 0 (110), vanished near 24.6° (Fig. 3), indicating that most of the conversion to Fe(III) or a small amount of the distinctive Fe(II) peak combined to form Fe(III)-Cr(III) oxides. These results indicate that the SA-NZVI particles underwent reduction to convert Cr(VI) to Cr(III). The characteristic peaks of Cr-Mn oxides (Fig. 3c), Mn(CrMn)O 4 (card JCPDS 82-0663), appear at 2θ = 31, 36, 57, and 63° after the A-Bir treatment, and the analysis shows that the valence of this Cr is + 3, indicating that Cr(III) can be adsorbed by A-Bir. This is mainly due to it having low PZC (point of zero charge), large surface area and strong acid sites, strong adsorption capacity, and excellent oxidative and catalytic activity for the adsorption of heavy metals, organic pollutants, etc. . Banerjee and Nesbitt (Banerjee & Nesbitt, 1999) found that after Cr(III) adsorbed onto the surface of A-Bir, it exchanged electrons with the highervalent manganese in hydrous sodic manganese ore, which in turn was converted to Cr(VI) (Feng et al., 2007a). This is consistent with the findings of our study, so we can infer that hydrous sodic manganese ore can adsorb Cr(III). It was discovered that A-Bir is a potent oxidizer of Cr(III) (Fig. 3c) and could destabilize the reduction product by oxidizing the adsorbed Cr(III) to Cr(VI).

Cr(VI) Removal in Soils
The results show that SA-NZVI can significantly reduce Cr(VI) in Cr(VI)-contaminated soil, and that the removal rate of Cr(VI) increases gradually with the increase of soil incubation days (Fig. 4). This is attributed to the superior dispersion and high oxidation resistance of SA-NZVI, which facilitates the availability of active sites for reaction. SA-NZVI interacts with Cr(VI) by reduction, complexation, precipitation, adsorption, and ion exchange, changing Cr(VI) into a more stable form of Cr (III) [(Cr(OH) 3 and Cr(III)/Fe(III) oxide/hydroxide] (Gil-Diaz et al., 2017; Soliemanzadeh & Fekri, 2017). The removal rate of Cr(VI) was highest during the initial 7 days of the reaction, possibly due to the gradual occupation of SA-NZVI's reaction sites by Cr(VI) pollutants as the reaction progressed, resulting in a gradual decrease in the removal rate after 7 days. The A-Bir treatment system exhibited significant potential for reducing Cr(VI) in Cr(VI)-contaminated soil during the first 14 days. This can be attributed to the ability of A-Bir, a manganese oxide mineral, to adsorb Cr(VI) from the soil, resulting in reduced mobility (Charbonnet et al., 2020;He & Xie, 2018;Villalobos et al., 2014). The Cr(VI) content of the soil gradually increased after 21 days. The reason for this may be that changes in the environment can lead to a decrease in the soil redox potential (Eh) of the reaction system, causing the dissolution of A-Bir, allowing the release of heavy metals that have been enriched in the short term (Schaffner et al., 2015).
The presence of A-Bir in the soil has a significant influence on the stability of SA-NZVI and Cr(VI) reduction. The removal of Cr(VI) by SA-NZVI was promoted in the first 7 days of incubation, resulting in a 7.93% increase in the removal of Cr(VI) by SA-NZVI. This increase could be due to the synergistic effect of Cr(VI) reduction by SA-NZVI and the adsorption of Cr(VI) by A-Bir, which resulted in a decrease in the amount of Cr(VI) and the toxicity of the heavy metal. After 7 days, the Cr(VI) content of the soil became higher, and the Cr(VI) content at the end of the incubation increased by 22.2% compared to 7 days. It is possible that A-Bir would have adsorbed Cr(III) already reduced by SA-NZVI in the early stage and oxidized the adsorbed Cr(III) to Cr(VI) after 7 days. It is suggested that the leaching concentration of Cr(VI) showed a rapid decrease followed by a slow increase with increasing incubation time. A-Bir significantly promoted the removal of Cr(VI) by SA-NZVI during the first 7 days of incubation, and A-Bir might re-oxidize the reduced Cr(VI) after 7 days.

Cr Fractions in Soil
The effect of the addition of NZVI on the morphological transformation of Cr in the soil after 28 days of treatment with different soil moisture treatments was investigated by using the sequential extraction method (SEP) (Fig. 5). The fractions of Cr are divided into exchangeable (EX), carbonate bound (CB), Fe/Mn oxidized (OX), organic bound (OM), and residue (RS) states, with the relative order of availability being EX > CB > OX > OM > RS.
After 28 days of remediation, the chromium species in the untreated soil were mainly divided into EX (4%), CB (4%), OM (49%), OX (32%), and RS (12%). The most significant changes in Cr fractions after SA-NZVI treatment were in the EX, OM, and RS fractions. The EX and OM fractions decreased by 4 and 6%, respectively and the RS fraction increased significantly by 10%, which is mainly due to the production of iron-chromium precipitates during the reaction. When A-Bir was added to the soil, the EX, OX, and RS fractions were increased by 4, 5, and 6%, respectively, and the OM and CB were reduced by 14 and 2%, respectively. This indicates that A-Bir can interact with OM (dissolved chromium) and CB [precipitated chromium in the form of Cr(OH) 3 ] but has difficulty in oxidizing Cr(III) in the residual state in the form of a lattice. With the SA-NZVI and A-Bir treatments, the percentage of EX and CB was lower and mainly present as OM and with OX, possibly due to the formation of Fe-Mn oxides through the combination of A-Bir and SA-NZVI, which increases soil OX. This demonstrates that SA-NZVI has a certain passivating effect on the soil heavy metal Cr, which can make the Cr in the exchangeable state shift toward the residual state of Cr in the soil and reduce the SPLP leaching (the synthetic precipitation leaching procedure) of soil Cr, and that the Cr(III) converted to RS under the action of SA-NZVI is difficult to be oxidized by A-Bir in the soil (Papassiopi et al., 2014).

Changes in the Chemical Characteristics of Soil
Soil pH increased after 28 days of SA-NZVI treatment (Fig. 6a) from 7.51 to 7.67, probably due to the reduction of SA-NZVI with Cr(VI) resulting in the utilization and depletion of H + in the soil (Eq. B1), which in turn led to an increase in soil pH. When the soil was treated with A-Bir, the soil pH decreased  (Fig. 6a) from 7.51 to 7.42, probably because A-Bir has a pH of 4.4, which is acidic and has a moderating effect on soil pH. In the presence of A-Bir and SA-NZVI, the soil pH increased (Fig. 6a) from 7.51 to 7.73, probably because the reaction between A-Bir and Cr(III) reduced by SA-NZVI consumes some H + (Eq. B2). While the reaction between SA-NZVI and A-Bir to form ferromanganese oxides also consumes some H + , the formed Fe-Mn oxides contain -OH and -COOH on their surface, which can protonate with H + and consume a certain amount of H + . Together, the fact that Fe-Mn oxides undergo hydrolysis in the environment to release OH − , which will bind to H + in the soil and thus regulate the pH of the soil . The available Fe and Mn contents in the SA-NZVI-treated soil increased significantly ( Fig. 6b and 6c), probably due to the soil moisture environment reducing Fe and Mn to the lower soluble form, thus increasing the available state of soil Fe and Mn (Wang et al., 2016).
The addition of A-Bir significantly reduces the available Fe content of the soil (Fig. 6b), probably because the addition of iron and manganese-based materials causes an increase in soil pH through redox reactions and the increase in soil pH leads to an increase in OH − in the soil. In the soil environment, iron ions are highly susceptible to the formation of intolerant iron hydroxide precipitates with OH − , resulting in a lower available Fe content in the soil.
SA-NZVI is a Fe-based material and can be used as an external source to increase the effective Fe content of the soil. However, this treatment may disrupt the balance of the Fe-Mn system in the soil and result in an increase in the effective Mn content (Jiang et al., 2021). Therefore, the addition of SA-NZVI to the treated soil significantly increased the content of soil Mn in the effective state (Fig. 6b). The significant increase in the effective state of Mn after the simultaneous application of SA-NZVI and A-Bir to the soil may be since Mn in the soil is prone to rapid transformation in response to environmental changes and the addition of exogenous Mn can significantly change the effective state of Mn (Xu et al., 2019).
(1)  (Hausladen & Fendorf, 2017). Therefore, it is hypothesized that in the oxidation of Cr(III) in the reduction products by A-Bir, two categories can be distinguished (Fig. 7) (Liang et al., 2021). The first type involves a reaction between the solid A-Bir surface and the dissolved Cr(III) in the reduction product. The entire procedure includes the following steps: 1) dissolving Cr(III) from the reduction products, 2) adsorbing dissolved Cr(III) onto or inside the A-Bir surface, 3) oxidizing adsorbed Cr(III) into Cr(VI), and 4) dissolving Cr(VI) and releasing it into the aqueous phase. The second kind involves the oxidative adsorption of Mn(II) from A-Bir onto the surface of Cr(III) and the reaction between the products of the reduction of Cr(VI) by SA-NZVI [Cr(OH) 3 and Cr x Fe 1−x (OH) 3 ]. The whole process may include 1) dissolved Mn(II) is adsorbed onto the surface of Cr(OH) 3 and Cr x Fe 1−x (OH) 3 , 2) adsorbed Mn(II) is then oxidized by dissolved oxygen to create Mn(III/IV), 3) Mn(III/IV) oxidizing Cr(OH) 3 and Cr x Fe 1−x (OH) 3 , and 4) electron transfer from the surfaces of Cr(OH) 3 and Cr x Fe 1−x (OH) 3 can catalyze the oxidation of Mn(II).

Conclusion
It was found that A-Bir had the most influence on the oxidation of Cr(III) with an oxidation rate of 88.92%, and that the characteristic peak of chromium-manganese oxide [Mn(CrMn)O 4 ] appears after the reaction with SA-NZVI and Cr(VI) reduction products. Results from soil incubation experiments showed that SA-NZVI effectively reduced over 90% of Cr(VI) in the soil and had a notable passivation effect on Cr(VI)-contaminated soil. However, the addition of A-Bir will result in the re-release of Cr(VI). We speculated that the effect of A-Bir on soil Cr is mainly caused by adsorption in the early stage, and then Cr(III) is oxidized to Cr(VI) and released under the action of electron transport. Therefore, manganese minerals pose a significant threat to the stabilization of Cr(III) in soils, after which the effect of acidic aqueous sodium manganese ore on SA-NZVI in Cr(VI)contaminated soils at different dosing amounts and dosing times can also be investigated to provide a theoretical basis for future nano-zero-valent iron in practical soil remediation.
Funding The study was supported by the National Natural Science Foundation of China (No. 4226701) and the Natural Science Foundation of Guangxi, China (No. 2020GXNSFAA297035).
Data Availability All data generated or analyzed during this study are included in this published article. The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Declarations
Competing Interests The authors declare no competing interests. Mn(II/III/IV)Ox