Efficient and Rapid Removal of Nickel Ions from Electroplating Wastewater Using Micro-/Nanostructured Biogenic Manganese Oxide Composite

: Manganese oxides reportedly exhibit pronounced adsorption capacities for numerous heavy-metal ions owing to their unique structural properties. Herein, a biogenic manganese oxide (BMO) composite was developed and used to remove Ni ions from Ni 2+ -containing electroplating wastewater. The formation of BMO and the micro-/nanoscale fine microstructure were characterized via scanning/high-resolution transmission electron microscopies and X-ray diffraction assays. Under the optimized conditions, with an adsorption temperature of 50 ◦ C, pH 6, the BMO composite showed a 100% removal efficiency within a rapid equilibrium reaction time of 20 min towards an initial Ni 2+ concentration of 10 mg L − 1 and a remarkable removal capacity of 416.2 mg g − 1 towards an initial Ni 2+ concentration of 600 mg L − 1 in Ni-electroplating wastewater. The pseudo-second-order equation was applicable to sorption data at low initial Ni 2+ concentrations of 10–50 mg L − 1 over the time course. Moreover, Freundlich isotherm models fitted the biosorption equilibrium data well. Fourier-transform infrared spectroscopic analysis validated that the removal capacity of the BMO composite was closely associated with structural groups. In five continuous cycles of adsorption/desorption, the BMO composite exhibited high Ni 2+ removal and recovery capacities, thereby showing an efficient and continuous performance potential in treating Ni 2+ -containing industrial wastewater.


Introduction
With the rapid development of the electroplating industry, the discharge of heavy metals into the environment from wastewater is becoming a serious environmental and health concern in China and other countries [1].Electroplating heavy-metal wastewater has been mainly categorized as chromium-containing, silver-containing, copper-containing, zinc-containing, cadmium-containing, nickel-containing, etc., and, as it is commonly mixed with other metals, cyanide, and multiple acidic and alkali substances, the resulting wastewaters are the third most severe industrial pollutants worldwide [2].In China, electroplating wastewater has an average annual volume of 2.7 billion gallons [3], with nickel concentrations in the range of tens to thousands of milligrams per liter [4,5], and has become a significant and intractable environmental issue in terms of managing hazardous substances and resource recycling.Various physicochemical and biological methods, such as membrane filtration, chemical precipitation, ion exchange, chemical oxidation and reduction, electroplating, and removal by biomasses generated by naturally occurring or genetically modified microorganisms [6][7][8], have been developed to treat electroplating Mn 2+ -oxidizing activity (i.e., the Mn oxide concentration formed by bacterial cells) of cell cultures that were incubated in 100 mL Lept broth (containing 1 mmol L −1 Mn 2+ ) over a time course of 10 days was determined according to a previously described method.

Preparation of the BMO Composite
The overnight-cultured MB04B cells were inoculated into 200 mL Lept medium supplemented with 1 mmol L −1 Mn 2+ at 1% (v/v) inoculum size for culturing at 28 • C for 48 h.The formed BMO/bacteria aggregates were centrifuged at 10,000 rpm for 10 min, dried by freeze drying, and stored at 4 • C until use.

Characterization of the BMO
SEM (JSM-6390/LV, NTC, Tokyo, Japan) was used to observe the surface morphology of the as-prepared BMO.An HRTEM (JEM-2100F, JEOL, Tokyo, Japan), equipped with an energy-dispersive spectroscopy detector, was used to investigate the microstructure of the BMO sample and analyze its elements.The HRTEM was operated at an acceleration voltage of 200 kV, and sample preparation and HRTEM observation were performed following the manufacturer's manual.The crystal structure of the BMO was determined by an XRD spectrometer (Bruker D8 Advance X, Billerica, MA, USA) as previously described [21].The crystal size was calculated by the software Jade 5.0.X-ray photoelectron spectroscopy (XPS) analysis of the BMO was conducted using an XPS spectrometer (VG Multilab 2000, Thermo Scientific, Waltham, MA, USA) with an Al Kα X-ray source (1486 eV) and a base pressure of 3 × 10 −9 Torr in the analytical chamber, following a previous protocol [22].

Adsorption Experiments
The biosorption experiments were performed in a 100 mL Erlenmeyer flask with a load of 40 mg (dry weight) BMO composite unless otherwise specified.In the removal capacity and the removal equilibrium experiments, the raw Ni-electroplating wastewater was diluted to a series of dilutions of 10, 50, 100, 200, 400, and 600 mg L −1 .In the secondorder kinetic analysis and isotherm fitting experiments, the removal was conducted at 50 • C and 200 rpm shaking for 60 min.After removal, the mixtures were centrifugated at 10,000 rpm for 10 min and Ni 2+ contents of the liquid supernatants were determined.The mixture without adding the BMO composite was set as the negative control.
A quantity of 10 mg L −1 Ni-electroplating wastewater was used in the adsorption/desorption cycle experiments.After removal, the biosorbents were harvested via centrifugation (10,000 rpm for 10 min) and then added into 10 mL of 0.1 mol L −1 HCl and shaken at 60 rpm for 30 min for the desorption of Ni 2+ ions from the BMO composite in each cycle.The HCl-treated BMO composite was washed with deionized water to neutral pH for further use in each cycle.

Kinetics and Isotherm Analysis
In all adsorption experiments, the residual Ni 2+ ion content was determined using an atomic absorption spectrophotometer (HITACHI 180-80, Tokyo, Japan).The residual Ni 2+ content was used to calculate the absolute removal rate and removal capacity of Ni 2+ in various wastewater dilutions using the following equations: where C i denotes the initial Ni 2+ ion concentration (mg L −1 ), C e denotes the equilibrium Ni 2+ concentration (mg L −1 ), and M denotes the mass concentration (g L −1 ) of the BMO composite.

FTIR Spectroscopy
The FTIR spectra of the BMO composite before and after Ni 2+ ion adsorption were analyzed using an FTIR spectrometer (Spectrum One, Perkin-Elmer, Waltham, MA, USA).All FTIR spectra were recorded within the 400-4000 cm −1 range.Samples were prepared as previously described [22].

Data Analysis
Graphs were prepared using Origin 11 software (Origin Lab Corp., Northampton, MA, USA).Data are presented as the average ± standard deviation (±SD) of at least three repeated experiments.Statistical analyses were conducted based on an analysis of variance (ANOVA) with the SPSS statistical software package (Version 19.0; SPSS, Inc., Chicago, IL, USA).Means were separated and compared using Fisher's protected least significant difference test.

Characterization of the BMO Aggregate Composite Formed by Mn 2+ -Oxidizing Pseudomonas sp. MB04B
We previously isolated a wild-type bacterium from a Fe-Mn nodule surrounding soil [23], which was preliminarily identified as Pseudomonas sp.MB04B.MB04B cells were subjected to continuous 1 mmol L −1 Mn 2+ enrichment in a laboratory shake-flask trial for 10 days to investigate the Mn 2+ -activity profile of this strain.The MB04B cultures exhibited a sharp increase in Mn 2+ activity after 24 h incubation and steadily maintained high activity across days 1-10 (Figure 1A).Interestingly, after 48 h incubation of the MB04B cells, irregular microspherical aggregates with diameters of approximately 5-7 µm were observed via SEM, and the bacteria attached to and embedded in the aggregates could be easily distinguished (Figure 1B).The XRD profile of the formed BMO (Figure 1C) revealed two characteristic diffraction peaks at 2θ of 37 • (311) and 65 • (440), which are consistent with the standard diffraction peaks of natural ramsdellite MnO 2 (JCPDS card no.42-11698) [24].Therefore, these results confirmed the pronounced Mn 2+ -oxidizing activity of the BMOs mainly comprising ramsdellite (MnO 2 ).
where Ci denotes the initial Ni 2+ ion concentration (mg L −1 ), Ce denotes the equilibrium Ni 2+ concentration (mg L −1 ), and M denotes the mass concentration (g L −1 ) of the BMO composite.

FTIR Spectroscopy
The FTIR spectra of the BMO composite before and after Ni 2+ ion adsorption were analyzed using an FTIR spectrometer (Spectrum One, Perkin-Elmer, Waltham, MA, USA).All FTIR spectra were recorded within the 400-4000 cm −1 range.Samples were prepared as previously described [22].

Data Analysis
Graphs were prepared using Origin 11 software (Origin Lab Corp., Northampton, MA, USA).Data are presented as the average ± standard deviation (±SD) of at least three repeated experiments.Statistical analyses were conducted based on an analysis of variance (ANOVA) with the SPSS statistical software package (Version 19.0; SPSS, Inc., Chicago, IL, USA).Means were separated and compared using Fisher's protected least significant difference test.

Characterization of the BMO Aggregate Composite Formed by Mn 2+ -Oxidizing Pseudomonas sp. MB04B
We previously isolated a wild-type bacterium from a Fe-Mn nodule surrounding soil [23], which was preliminarily identified as Pseudomonas sp.MB04B.MB04B cells were subjected to continuous 1 mmol L −1 Mn 2+ enrichment in a laboratory shake-flask trial for 10 days to investigate the Mn 2+ -activity profile of this strain.The MB04B cultures exhibited a sharp increase in Mn 2+ activity after 24 h incubation and steadily maintained high activity across days 1-10 (Figure 1A).Interestingly, after 48 h incubation of the MB04B cells, irregular microspherical aggregates with diameters of approximately 5-7 µm were observed via SEM, and the bacteria attached to and embedded in the aggregates could be easily distinguished (Figure 1B).The XRD profile of the formed BMO (Figure 1C) revealed two characteristic diffraction peaks at 2θ of 37° (311) and 65° (440), which are consistent with the standard diffraction peaks of natural ramsdellite MnO2 (JCPDS card no.42-11698) [24].Therefore, these results confirmed the pronounced Mn 2+ -oxidizing activity of the BMOs mainly comprising ramsdellite (MnO2).HRTEM was performed to investigate the fine microstructure of the formed BMO aggregates.Figure 2A shows the irregular microspherical structure of a randomly observed single aggregate particle.Quantities of nanocrystalline particles with diameters of HRTEM was performed to investigate the fine microstructure of the formed BMO aggregates.Figure 2A shows the irregular microspherical structure of a randomly observed single aggregate particle.Quantities of nanocrystalline particles with diameters of 5 ± 1 nm were dispersed and embedded in the organic matter (Figure 2A, indicated by red arrows).The lattice fringe of 0.206 nm corresponded to the d value of the (401) planespacing in the ramsdellite-type MnO 2 , suggesting that the BMO aggregates formed by bacterial mineralization were micro-/nanostructure-type composites (Figure 2B).Given the presence of porous surface and lattice vacancies that are apparently conducive to metal-ion removal [25][26][27], we further investigated the potential of this composite with respect to Ni 2+ removal performance.
J. Compos.Sci.2024, 8, x FOR PEER REVIEW 5 of 13 5 ± 1 nm were dispersed and embedded in the organic matter (Figure 2A, indicated by red arrows).The lattice fringe of 0.206 nm corresponded to the d value of the (401) planespacing in the ramsdellite-type MnO2, suggesting that the BMO aggregates formed by bacterial mineralization were micro-/nanostructure-type composites (Figure 2B).Given the presence of porous surface and lattice vacancies that are apparently conducive to metal-ion removal [25][26][27], we further investigated the potential of this composite with respect to Ni 2+ removal performance.

Ni 2+ Removal Capacity of the Composite
The industrial-grade raw Ni-electroplating wastewater used in this study contains complex and multicomponent toxic substances.In addition to a high content of Ni 2+ , it includes a high content of total-P, multiple cyanides, and acidic and alkaline substances and a high load of COD (Supplementary Figure S1), making it extremely hazardous wastewater that cannot be discharged directly.To evaluate the Ni 2+ biosorption capacity of the BMO composite with respect to the Ni-electroplating wastewater, an orthogonal test at four factors/three levels (Supplementary Table S1), based on temperature (30 °C, 40 °C, and 50 °C), pH (4, 5, and 6), removal time (10, 30, and 50 min), and initial Ni 2+ concentration (10, 50, and 100 mg L −1 ) in shake-flask incubation, was performed to optimize the adsorptive reaction conditions.As shown in Table 1, these four factors exhibited pronounced effects on the Ni 2+ removal capacity of the BMO composite, with an effective degree order of "initial Ni 2+ concentration > temperature > pH > removal time".The ANOVA analysis (Supplementary Table S2) also validated the significant effects of these factors.The optimized Ni 2+ -biosorption conditions can be defined as follows: temperature of 50 °C, pH value of 6, removal time of 50 min, and initial nickel ion concentration of 10 mg L −1 .

Ni 2+ Removal Capacity of the Composite
The industrial-grade raw Ni-electroplating wastewater used in this study contains complex and multicomponent toxic substances.In addition to a high content of Ni 2+ , it includes a high content of total-P, multiple cyanides, and acidic and alkaline substances and a high load of COD (Supplementary Figure S1), making it extremely hazardous wastewater that cannot be discharged directly.To evaluate the Ni 2+ biosorption capacity of the BMO composite with respect to the Ni-electroplating wastewater, an orthogonal test at four factors/three levels (Supplementary Table S1), based on temperature (30 • C, 40 • C, and 50 • C), pH (4, 5, and 6), removal time (10, 30, and 50 min), and initial Ni 2+ concentration (10, 50, and 100 mg L −1 ) in shake-flask incubation, was performed to optimize the adsorptive reaction conditions.As shown in Table 1, these four factors exhibited pronounced effects on the Ni 2+ removal capacity of the BMO composite, with an effective degree order of "initial Ni 2+ concentration > temperature > pH > removal time".The ANOVA analysis (Supplementary Table S2) also validated the significant effects of these factors.The optimized Ni 2+ -biosorption conditions can be defined as follows: temperature of 50 • C, pH value of 6, removal time of 50 min, and initial nickel ion concentration of 10 mg L −1 .

Adsorption Kinetics
The optimum biosorption conditions (50 • C, pH 6, and 50 min for saturated adsorption) were applied to identify the biosorption kinetics of the BMO composite in Ni 2+ biosorption at the varying initial Ni 2+ concentrations of 10, 50, 100, 200, 400, and 600 mg L −1 .Figure 3 shows that the adsorption equilibrium reaction was rapidly conducted for 40 min for all treatments, even for only 20 min for several biosorption reactions (i.e., 10-200 mg L −1 Ni 2+ ).In addition, with the increase in the initial Ni 2+ concentration, the removal capacity of Ni 2+ also significantly increased in parallel, i.e., a maximum Ni 2+ biosorption capacity of 416.2 mg g −1 was obtained under the optimized conditions for 600 mg L −1 of initial Ni 2+ concentration.
a Range of the corresponding values for each factor.

Adsorption Kinetics
The optimum biosorption conditions (50 °C, pH 6, and 50 min for saturated adsorption) were applied to identify the biosorption kinetics of the BMO composite in Ni 2+ biosorption at the varying initial Ni 2+ concentrations of 10, 50, 100, 200, 400, and 600 mg L −1 .Figure 3 shows that the adsorption equilibrium reaction was rapidly conducted for 40 min for all treatments, even for only 20 min for several biosorption reactions (i.e., 10-200 mg L −1 Ni 2+ ).In addition, with the increase in the initial Ni 2+ concentration, the removal capacity of Ni 2+ also significantly increased in parallel, i.e., a maximum Ni 2+ biosorption capacity of 416.2 mg g −1 was obtained under the optimized conditions for 600 mg L −1 of initial Ni 2+ concentration.The pseudo-second-order removal kinetic equation was used to test the fitting of the removal data over the time course.Lagergren's pseudo-second-order equation based on removal equilibrium capacity is generally defined as follows [28]: and a linearized equation can be expressed by integrating Equation (3): q q k q (4) in Equations ( 3) and (4), k2 is the secondary removal rate constant (g mg −1 min −1 ) and qe and qt denote the removal capacity at the sorption equilibrium and time t, respectively.
Table 2 shows the profiles of the time-course sorption data fitted using Equation (3) or (4).It shows that the corresponding k2 constant and the equilibrium removal capacity, qe, increase following the increase in initial Ni 2+ concentration, and the removal kinetics can be described using the pseudo-second-order model at a 10-50 mg L −1 initial Ni 2+ concentration (R 2 > 0.9).The pseudo-second-order removal kinetic equation was used to test the fitting of the removal data over the time course.Lagergren's pseudo-second-order equation based on removal equilibrium capacity is generally defined as follows [28]: and a linearized equation can be expressed by integrating Equation (3): in Equations ( 3) and (4), k 2 is the secondary removal rate constant (g mg −1 min −1 ) and q e and q t denote the removal capacity at the sorption equilibrium and time t, respectively.Table 2 shows the profiles of the time-course sorption data fitted using Equation (3) or (4).It shows that the corresponding k 2 constant and the equilibrium removal capacity, q e , increase following the increase in initial Ni 2+ concentration, and the removal kinetics can be described using the pseudo-second-order model at a 10-50 mg L −1 initial Ni 2+ concentration (R 2 > 0.9).

Isotherm Equation Fitting
The Langmuir and Freundlich models were applied to analyze the removal data with different initial Ni 2+ concentrations.The Langmuir model linearization equation [7] can be expressed as: 1 where Q e is the removal capacity at the equilibrium of the sorbent (mg g −1 ), Q max (mg g −1 ) is the maximum removal capacity of the sorbent (mg g −1 ), C e (mg L −1 ) is the equilibrium concentration of Ni ions in solution, and K s is the saturation constant (mg L −1 ).
The Freundlich model linearization equation can be expressed as: ln where Q e and C e are the same parameters indicated above, and K f and n are Freundlich constants denoting the removal capacity and removal intensity, respectively.Figure 4 shows that Ni 2+ biosorption by the BMO composite is better fitted by the Freundlich isotherm model (with the parameter of R 2 = 0.96) than the Langmuir model (R 2 = 0.84).These results suggest that the Ni 2+ removal of the BMO composite in Nielectroplating wastewater is a multiphase chemical removal process, which is consistent with the intrinsic structural features of the BMO composite possessing multiple surface charge groups and a layered and porous surface [29].This multiphased biosorption is conducive to a greater sorption capacity than single-layer removal under only one level.600 y = 0.00112x + 0.07375 0.6934 0.000017 892.8

Isotherm Equation Fitting
The Langmuir and Freundlich models were applied to analyze the removal da different initial Ni 2+ concentrations.The Langmuir model linearization equation [7] expressed as: where Qe is the removal capacity at the equilibrium of the sorbent (mg g −1 ), Qmax (m is the maximum removal capacity of the sorbent (mg g −1 ), Ce (mg L −1 ) is the equil concentration of Ni ions in solution, and Ks is the saturation constant (mg L −1 ).
The Freundlich model linearization equation can be expressed as: where Qe and Ce are the same parameters indicated above, and Kf and n are Freu constants denoting the removal capacity and removal intensity, respectively.
Figure 4 shows that Ni 2+ biosorption by the BMO composite is better fitted Freundlich isotherm model (with the parameter of R 2 = 0.96) than the Langmuir mo = 0.84).These results suggest that the Ni 2+ removal of the BMO composite in Ni-e plating wastewater is a multiphase chemical removal process, which is consistent w intrinsic structural features of the BMO composite possessing multiple surface groups and a layered and porous surface [29].This multiphased biosorption is con to a greater sorption capacity than single-layer removal under only one level.

Characterization of Removal Using FTIR and XRD Assays
FTIR spectroscopic analyses of the BMO composite before and after Ni 2+ re were performed to verify the chemical groups involved in the binding of Ni ions.5 shows similar spectra for both, in which the displayed peaks at 3400-3800 cm −1 rep the stretching vibration peak of free -OH [30] and the peak at 2900 cm −1 represents H (e.g., CH3) stretching vibration peak, while the peak at 1300-1600 cm −1 represe bending vibration of the -OH [31] and the varied -OH wavenumbers at 1384 cm −1 cm −1 before and after Ni 2+ removal are likely due to electrostatic interaction [32].Th at 1021.23 cm −1 represents the bending vibration of Mn-OH on the surface of the B addition to the characteristic vibration peaks of relatively weak Mn-O bonds in the of 500-700 cm −1 , thereby proving that Mn-O bonds exist in the BMO [33].It is notew

Characterization of Removal Using FTIR and XRD Assays
FTIR spectroscopic analyses of the BMO composite before and after Ni 2+ removal were performed to verify the chemical groups involved in the binding of Ni ions. Figure 5 shows similar spectra for both, in which the displayed peaks at 3400-3800 cm −1 represent the stretching vibration peak of free -OH [30] and the peak at 2900 cm −1 represents the C-H (e.g., CH 3 ) stretching vibration peak, while the peak at 1300-1600 cm −1 represents the bending vibration of the -OH [31] and the varied -OH wavenumbers at 1384 cm −1 to 1403 cm −1 before and after Ni 2+ removal are likely due to electrostatic interaction [32].The peak at 1021.23 cm −1 represents the bending vibration of Mn-OH on the surface of the BMO, in addition to the characteristic vibration peaks of relatively weak Mn-O bonds in the range of 500-700 cm −1 , thereby proving that Mn-O bonds exist in the BMO [33].It is noteworthy that the BMO composite also includes Mn(II)-oxidizing cells and extracellular polymeric substances and thus has abundant anionic carboxyl and hydroxyl functional groups that might participate in Ni ion removal [34].Moreover, the BMO composite is structurally layered and generally contains varying amounts of Mn(III) and vacant sites in the Mn layers [35], and the significant variation in the Mn-O bond wavenumbers before and after Ni 2+ removal indicates that the Mn-O bond also plays a specific role in the Ni 2+ removal process of the BMO composite.
contained different valence forms consisting of mainly Mn , Mn , and Mn portion of Mn oxides in all three valent states changed significantly before removal, especially the ratio of Mn 2+ in the Mn element, which increased by a 15% (Supplementary Table S3).Moreover, 4.39% of Ni 3+ in the Ni element ap BMO after Ni 2+ removal (Supplementary Table S4).It has been revealed that able to oxidize many organic compounds and metals as a pronounced oxid ural environment [35].The potential difference between the low potential o tain organic matters (such as malic acid, tartaric acid, and citric acid, which the COD content) in electroplating wastewater and the high potential in the site-derived electron transfer between Mn 3+ /Mn 4+ and Mn 2+ may increase t Mn 2+ via Mn reduction reaction [36].Therefore, we presume that the remo by the BMO composite occurred not only via adsorption but also via Ni 2+ o  XPS assays were performed to compare the varied valence states and the proportions of Mn and Ni in the BMO before and after Ni 2+ removal.Figure 6 shows that the BMO contained different valence forms consisting of mainly Mn 2+ , Mn 3+ , and Mn 4+ , and the proportion of Mn oxides in all three valent states changed significantly before and after Ni 2+ removal, especially the ratio of Mn 2+ in the Mn element, which increased by approximately 15% (Supplementary Table S3).Moreover, 4.39% of Ni 3+ in the Ni element appeared in the BMO after Ni 2+ removal (Supplementary Table S4).It has been revealed that the BMO was able to oxidize many organic compounds and metals as a pronounced oxidant in the natural environment [35].The potential difference between the low potential of Ni 2+ and certain organic matters (such as malic acid, tartaric acid, and citric acid, which contributed to the COD content) in electroplating wastewater and the high potential in the BMO compositederived electron transfer between Mn 3+ /Mn 4+ and Mn 2+ may increase the amount of Mn 2+ via Mn reduction reaction [36].Therefore, we presume that the removal of Ni ions by the BMO composite occurred not only via adsorption but also via Ni 2+ oxidation.Figure 6.XPS patterns of Mn (2p3/2) spectrograms of the BMO composite before (A) and Ni 2+ removal.In A/B, the upper circles represent observed data.The upper thick olive curves the best fit of the data.The black curves represent Mn 4+ multiplet peaks, the red curves r Mn 3+ , the blue curves represent Mn 2+ .

Ni 2+ Adsorption/Desorption Cycles
To investigate the reusability of the BMO composite with respect to its con performance in treating Ni-electroplating wastewater, its Ni 2+ adsorption and des efficiency was determined through five cycles of adsorption and desorption.F shows that relatively high Ni 2+ adsorption/desorption capacities were retained in of five cycles, with adsorption efficiencies of 98.1%, 94.6%, 84.5%, and 71.5% in cy (cycle 1 was set as 100%), respectively, and comparable recovery efficiencies (the desorption/adsorption in each cycle) of 86.7%, 85.7%, 84.0%, 71.2%, and 71.8% in c 5, respectively.The results indicate that the BMO composite can be reused in con adsorption/desorption operations to treat industrial wastewater containing Ni 2+ .

Ni 2+ Adsorption/Desorption Cycles
To investigate the reusability of the BMO composite with respect to its continuous performance in treating Ni-electroplating wastewater, its Ni 2+ adsorption and desorption efficiency was determined through five cycles of adsorption and desorption.Figure 7 shows that relatively high Ni 2+ adsorption/desorption capacities were retained in a total of five cycles, with adsorption efficiencies of 98.1%, 94.6%, 84.5%, and 71.5% in cycles 2-5 (cycle 1 was set as 100%), respectively, and comparable recovery efficiencies (the ratio of desorption/adsorption in each cycle) of 86.7%, 85.7%, 84.0%, 71.2%, and 71.8% in cycles 1-5, respectively.The results indicate that the BMO composite can be reused in continuous adsorption/desorption operations to treat industrial wastewater containing Ni 2+ .Numerous studies have reported the efficient removal of heavy metals from wastewater using abiotic or biotic masses consisting of naturally occurring or recombinant microorganisms [37,38].Several previously described systems exhibited higher levels of Ni 2+ removal, with a maximum removal capacity of 411.8 mg g −1 (Table 3).In comparison, the highest Ni 2+ removal capacity of the BMO composite prepared in this study was 416.2 mg g −1 at the initial Ni 2+ concentration of 600 mg L −1 , a slightly higher capacity than the available biosorbents with the highest levels, thereby suggesting a comparable high absolute Ni 2+ removal capacity for the BMO composite.The nickel electroplating wastewater used in this study contained Ni 2+ , P (mainly phosphite and hypophosphite), and COD (malic acid, tartaric acid, and citric acid) (pH 3.0).To achieve the standard of safe discharge, we designed the following processing steps that will be studied in the future: (1) recovery of nickel by multistage cycles of adsorption using the BMO composite at pH 6.0; (2) addition of CaO to remove P, a pH > 5.0 promoting this process; and (3) microbial treatment to remove COD, with neutral pH as the optimum.To the best of our knowledge, the present study is the first attempt to use a bacterial BMO composite to treat raw industrial Ni-electroplating wastewater.It is worth noting that the current BMO composite exhibited relative easiness and cost-effectiveness of preparation under mild bacterial culture conditions, effectively removing Ni ions in Ni- Numerous studies have reported the efficient removal of heavy metals from wastewater using abiotic or biotic masses consisting of naturally occurring or recombinant microorganisms [37,38].Several previously described systems exhibited higher levels of Ni 2+ removal, with a maximum removal capacity of 411.8 mg g −1 (Table 3).In comparison, the highest Ni 2+ removal capacity of the BMO composite prepared in this study was 416.2 mg g −1 at the initial Ni 2+ concentration of 600 mg L −1 , a slightly higher capacity than the available biosorbents with the highest levels, thereby suggesting a comparable high absolute Ni 2+ removal capacity for the BMO composite.The nickel electroplating wastewater used in this study contained Ni 2+ , P (mainly phosphite and hypophosphite), and COD (malic acid, tartaric acid, and citric acid) (pH 3.0).To achieve the standard of safe discharge, we designed the following processing steps that will be studied in the future: (1) recovery of nickel by multistage cycles of adsorption using the BMO composite at pH 6.0; (2) addition of CaO to remove P, a pH > 5.0 promoting this process; and (3) microbial treatment to remove COD, with neutral pH as the optimum.To the best of our knowledge, the present study is the first attempt to use a bacterial BMO composite to treat raw industrial Ni-electroplating wastewater.It is worth noting that the current BMO composite exhibited relative easiness and cost-effectiveness of preparation under mild bacterial culture conditions, effectively removing Ni ions in Ni-electroplating wastewater, especially at low concentrations, and repeatable performance in treating elec-troplating wastewater.However, modifying the surface ion charges and pore sizes is thought to be definitely conducive to a more efficient and coordinated adsorptive capacity of this system.Thus, the development of capacity-promoted BMO-biosorption systems is now one of our primary research goals.

Conclusions
The current study demonstrated, for the first time, that the BMO composite formed using an Mn 2+ -oxidizing bacterium efficiently and rapidly removed Ni 2+ ions from industrial Ni-electroplating wastewater.The adsorption equilibrium was conducted for 20 min towards an initial concentration of 10 mg L −1 Ni 2+ ions, and the highest removal capacity of 416.2 mg g −1 was conducted under optimized conditions towards an initial concentration of 600 mg L −1 Ni 2+ ions.FTIR and XPS showed that the Ni removal by the BMO composite was not only contributed by adsorption via hydroxyl and carboxyl groups and Mn-O bands, but was also contributed by Mn(III)/Mn(IV) oxidation.In addition, the engineered BMO composite exhibited efficient and feasible Ni 2+ -removal/-recycling performance in five continuous adsorption/desorption cycle operations.Therefore, further development of this BMO material could be especially valuable for large-scale or continuous biosorption processes in treating industrial electroplating wastewater.

Figure 1 .
Figure 1.(A) Mn 2+ -oxidizing activity curve of the BMO cultures of Pseudomonas sp.MB04B; (B) SEM micrograph of the formed aggregates at 48 h; (C) XRD pattern of Mn oxides of the BMO aggregates.In (B), red arrows indicate the attached or embedded MB04 cells.

Figure 1 .
Figure 1.(A) Mn 2+ -oxidizing activity curve of the BMO cultures of Pseudomonas sp.MB04B; (B) SEM micrograph of the formed aggregates at 48 h; (C) XRD pattern of Mn oxides of the BMO aggregates.In (B), red arrows indicate the attached or embedded MB04 cells.

Figure 2 .
Figure 2. (A) HRTEM micrograph of a representative BMO aggregate particle; (B) measured lattice spacings of the micro-/nanostructured BMO aggregate matter.

Figure 2 .
Figure 2. (A) HRTEM micrograph of a representative BMO aggregate particle; (B) measured lattice spacings of the micro-/nanostructured BMO aggregate matter.

Figure 5 .
Figure 5. FTIR spectra of the BMO composite before and after Ni 2+ removal.

Figure 5 .
Figure 5. FTIR spectra of the BMO composite before and after Ni 2+ removal.

Figure 6 .
Figure 6.XPS patterns of Mn (2p 3/2 ) spectrograms of the BMO composite before (A) and after (B) Ni 2+ removal.In A/B, the upper circles represent observed data.The upper thick olive curves indicate the best fit of the data.The black curves represent Mn 4+ multiplet peaks, the red curves represent Mn 3+ , the blue curves represent Mn 2+ .

Figure 7 .
Figure 7. Ni 2+ adsorption/desorption capacity of the BMO composite under continuously repeated operations.

Figure 7 .
Figure 7. Ni 2+ adsorption/desorption capacity of the BMO composite under continuously repeated operations.

Table 1 .
Significance analysis of the factors in the L9-orthogonal test of Ni removal efficiency.

Table 1 .
Significance analysis of the factors in the L9-orthogonal test of Ni removal efficiency.
a Range of the corresponding values for each factor.

Table 2 .
Fitting parameters of pseudo-second-order kinetics.

Table 2 .
Fitting parameters of pseudo-second-order kinetics.

Table 3 .
Comparison of the maximum Ni 2+ -removal capacities of different materials in this work and previous reports.

Table 3 .
Comparison of the maximum Ni 2+ -removal capacities of different materials in this work and previous reports.
a Wet weight.b The maximum removal capacity.EPS, exopolysaccharides.