Chemical and biological approach to remove Mn from aqueous solution

Environmental Technology & Innovation 15 (2019) 100398

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Environmental Technology & Innovation journal homepage: www.elsevier.com/locate/eti

Chemical and biological approach to remove Mn from aqueous solution ∗

Fernanda Cristina Fonseca Camargo a , , Gabriel de Lacerda Caldas Silva a , Henrique Lages Barsand de Leucas a , Marília Ribeiro de Vasconcelos a , Versiane Albis Leão b , Ana Cláudia Queiroz Ladeira a a

Center for the Development of Nuclear Technology (CDTN), Av. Antônio Carlos 6627, Campus da UFMG, Pampulha, Belo Horizonte 31270-901, Brazil b Department of Metallurgical and Materials Engineering, Federal University of Ouro Preto, Campus Morro do Cruzeiro, Ouro Preto, MG CEP 35400-000, Brazil

highlights • • • •

High levels of Mn 150 mg L−1 were removed by biological and chemical process. The manganese oxide was able to remove 96% of Mn using alkali to adjust the pH to 7.0. MnO2 + Bacillus cereus added directly in the solution avoided alkali addition. MnO2 + Bacillus cereus immobilized in Ca-alginate caused no changes in the Mn removal efficiency.

article

info

Article history: Received 7 March 2018 Received in revised form 1 May 2019 Accepted 18 May 2019 Available online 22 May 2019 Keywords: Chemical manganese removal Manganese dioxide Biological manganese removal Bacillus cereus Biomass immobilization Alginate

a b s t r a c t Many approaches have been proposed to remove manganese from public supply waters as well as from acid mine drainage. This study investigated the removal of high levels of soluble Mn (II), similar to forms found in acid mine drainage in Brazil, by using a manganese oxide (MnO2 ) residue from the electrowinning process and a Bacillus cereus strain isolated from mine water, immobilized or not in calcium alginate. Experimental data for manganese removal by MnO2 showed that a pseudo-second-order kinetic model conformed well to the equilibrium adsorption data and the Langmuir isotherm was suitable to describe this adsorption process. Thermodynamic analysis showed that the adsorption of Mn (II) using MnO2 was spontaneous and endothermic under the experimental conditions. The manganese removal by B. cereus was 75% and by the MnO2 residue was 96% at the end of nine days. The removal using MnO2 and B. cereus together reached 96%. Immobilization of MnO2 and B. cereus using alginate biopolymer was also investigated. After nine days, the removal by B. cereus reached 93% and B. cereus + MnO2 reached 92%, both immobilizing in alginate. The immobilization promoted fewer changes in pH, which ranged from 7.5 to 8.5 during the experiments. The use of MnO2 alone or the use of B. cereus immobilized in alginate are two interesting alternative to remove high levels of manganese, however, only the last alternative is capable of maintaining an alkaline pH necessary to the process. © 2019 Elsevier B.V. All rights reserved.

∗ Corresponding author. E-mail address: [email protected] (F.C.F. Camargo). https://doi.org/10.1016/j.eti.2019.100398 2352-1864/© 2019 Elsevier B.V. All rights reserved.

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F.C.F. Camargo, G.L.C. Silva, H.L.B. de Leucas et al. / Environmental Technology & Innovation 15 (2019) 100398

1. Introduction Manganese is a transition metal, found in all oxidation states between Mn (II) and Mn (VII) in different pHs and temperatures, with an electronic configuration of 1s2 2s2 p6 3s2 p6 d5 4s2 . The most common manganese ores are hydrated or anhydrous oxides, followed by silicates and carbonates (Habashi, 1997). Environmental conditions, such as pH, Eh, temperature and presence of microorganisms and organic compounds, influence manganese speciation. In aquatic environments Mn (II) is thermodynamically stable at a lower pH and in anoxic environments. On the other hand, at pHs above 8 and in the presence of microorganisms, it is commonly found in more oxidized states that are generally poorly crystalline or amorphous compounds. Mn(III) and Mn(IV) are favored in the presence of oxygen and at high pH. Mn(III), which is thermodynamically unstable and disproportionates in aqueous media to yield Mn(II) + Mn(IV), persists only in certain soluble organic complexes (Patil et al., 2016; Toyoda and Tebo, 2013). Mn (II) is stable in natural waters and it requires an increase the pH or Mn (II) chelators, such as manganese oxides (MnOx(s) ), added in order to provoke its precipitation (Nealson, 2006). The MnOx(s) are very important solids because the manganese oxidation reaction is autocatalytic. Murray (1975) demonstrated that the sorptive capacity of newly precipitated Mn oxides is extremely high for a variety of metal cations. In addition, the metal adsorption occurs with the release of protons, suggesting that the cations are bound to the atomic structure of the metal oxides (Murray, 1975). According to Morgan and Stumm (1964) the amount of manganese removed from a solution cannot be explained only by considering the stoichiometry of the oxidation reaction. The manganese oxides sorption capacity increases as the pH rises. The sorption capacity of 0.5 mole of Mn (II) per mole of MnO2 from dilute Mn (II) solutions was reported at slightly alkaline pH ranges, for example at pH 7.5. Capacities of 2 moles of Mn (II) per mole of MnO2 were obtained at pH values near 9.0. Many approaches have been proposed aiming the manganese removal from public water supplies and acid mine drainage. These approaches employed different techniques such as coagulation, flocculation, flotation (Charemtanyarak, 1999; Polat and Erdogan, 2007; Stoica et al., 1998) and precipitation using hydroxides, carbonate, air and sulfur dioxide (Silva et al., 2010; Aziz and Smith, 1992, 1996; Thornton, 1995; Zhang and Cheng, 2007). Mn (II) oxidation was also applied to form insoluble products by using oxidizing agents, e.g., chloride potassium permanganate, chloride dioxide and ozone (Patil et al., 2016; Tobiason et al., 2008; Cerrato et al., 2011; Knocke et al., 1991; Liu et al., 2010). The most water treatment systems employ oxidants to oxidize the metals, then precipitation and filtration of solids The resulting sorption/oxidation from the oxides is a physical/chemical process employed by the industry This process presents an effective technology to remove manganese and other metals from effluents and water supply (Patil et al., 2016). Among other techniques, adsorption using natural zeolite (Dimirkou and Doula, 2008; Rajic et al., 2009), carbon adsorbents obtained from mixtures of biomass treatment products (Savova et al., 2003), polymers (Al-Wakeel et al., 2015), ionic exchange (Zainol and Nicol, 2009; Choo et al., 2007) and oxidation/sorption in manganese oxides (Taffarel and Rubio, 2010; Morgan and Stumm, 1964) are employed. In biosorption, an array of biomaterials, including microorganisms such as Bacillus cereus, Saccharomyces carlsbergensis, Aspergillus niger, Leptothrix discophora and Pseudomonas aeruginosa both immobilized or not in supporting matrixes are used (Tsekova et al., 2010; Hallberg and Johnson, 2005; Barboza et al., 2015; Fadel et al., 2015; Chatterjee and Ray, 2008). Acid mine drainage (AMD) is one of the major environmental issues caused by the mining industry. In Brazil, AMD has been reported to occur in the gold, copper, zinc, uranium and coal mines, when sulfide minerals are exposed to oxidizing conditions to produce sulfuric acid. This acid can leach minerals present in the mining residues, generating a percolate rich in dissolved metals which may contaminate the surface or ground waters, resulting in serious environmental problems (Trindade and Soares, 2004). Currently, AMD treatment is carried out by adding hydrated lime to precipitate the metals. In the case of manganese, this process is efficient only for pH values above 10 (Patil et al., 2016). The stability of Mn (II) in aqueous solution makes the use of lime unviable due to the increased costs of the process. Moreover, the treated effluent pH would not comply with most environmental limits, which demands a pH range of 5.0–9.0 for effluent discharge (Nóbrega et al., 2008). The AMD in Brazil contains one of the highest dissolved Mn (II) levels in the world (up to 150 mg L−1 , a value far above the legal discharge limit of <1 mg L−1 ) because of its manganese enriched soils (Brazil, 2005, 2011). The complexity of manganese chemistry, along with the necessity to reduce its content to levels below 1 mg L−1 , makes the development of new removal techniques a challenge. The objective of the current study was to evaluate the manganese removal from aqueous solution by combining chemical and biological techniques. For this purpose, manganese oxide residue from electrowinning processes and bacteria isolated from mine water were employed. 2. Materials and methods 2.1. Liquid samples Laboratory solutions were prepared by diluting 0.461 g of MnSO4 .H2 O (Vetec-Brazil) in 1.0 L of deionized water (obtained from a Milli-Q system (Millipore)) to produce a solution with 150 mg L−1 of manganese (Mn concentrations similar to the Brazilian acid mine waters). The pH was adjusted with sodium hydroxide or lime using a pH meter (DIGIMED, model DM-22). The manganese was determined by atomic absorption spectrophotometry (VARIAN, model AA240FS). All solutions containing manganese were acidified with H2 SO4 before analysis.

F.C.F. Camargo, G.L.C. Silva, H.L.B. de Leucas et al. / Environmental Technology & Innovation 15 (2019) 100398

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2.2. Characterization of the manganese oxide The MnO2 solid, used herein as the sorbent for the soluble Mn, was a residue from the zinc electrowinning process. It was neutralized with NaOH 0.1 mol L−1 , filtered and dried at 60 ◦ C. The specific surface area was 38.35 m2 g−1 , determined by Braunauer, Emmet and Teller model (BET) method multiple point technique (Quantachrome Corp., NOVA-2200). MnO2 content in the residue was around 56%, determined by X-ray fluorescence analysis (SHIMADZU model EXD-720). The particle size distribution was determined by wet sieving. X-ray diffraction (XRD) spectra were obtained with an X-ray diffractometer Rigaku (D\MAX ULTIMA) equipped with a goniometer (4◦ 2θ/min), at 2θ/θ range, using CuKα radiation operated at 40 kV and 30 mA. For the thermogravimetric analysis (TGA) a 2960 SDT and 9 mg of samples were used. Experiments were conducted in air with a heating rate of 10 K min−1 . The valences of manganese were estimated based on X-ray photoelectron spectroscopy (XPS) Mn 2p3/2 spectra. XPS was collected using Specs Phoibos 150 MCD-9 detector employing a monochromatic Al Kα (E = 1486.6 eV) X-ray source. The binding energies were corrected using as reference C (1s) 284.6 eV. The pHPZC (Zero Point Charge) was determined by acid–base titration of three different masses of solid in a solution containing 0.001 mol L−1 NaNO3 , using an automatic titrator (Mettler Toledo model DL50 Grafin). 2.3. Adsorption studies with MnO2 Sorption isotherms were determined in a batch sorption equilibrium using solid MnO2 as the sorbent. A 200 mL volume of aqueous solutions containing 150 mg L−1 Mn (II) and different solid masses were agitated in Erlenmeyer flasks for 24 h in an orbital shaker at 150 rpm, at 25 ◦ C, 30 ◦ C and 40 ◦ C. The pH was maintained to 7.0 ±0.2 by using NaOH (0.1 mol L−1 ) according to Aguiar et al. (2013). After sorption, the supernatant was decanted, and 5 mL aliquots were filtered through a 0.45 µm cellulose acetate membrane filter and analyzed by an AA spectrometer. The kinetic experiments were carried out with 200 mL of solution containing 150 mg L−1 Mn (II) at pH 7.0 ±0.2, and 2.00 g of solid MnO2 for 6 h. Distinct 5 mL aliquots were collected, filtered through a 0.45 µm membrane and analyzed by an AA spectrometer. All the experiments were performed in duplicate. 2.4. Adsorption studies with bacteria The experiments were performed in batch with 150 mg L−1 Mn (II), solid MnO2 and Bacillus cereus strains supplied by DEMET-UFOP (Laboratório de Bio&Hidrometalurgia, Departamento de Engenharia Metalúrgica e de Materiais da Universidade Federal de Ouro Preto) (Reis et al., 2013). According to the procedure described by Reis et al. (2017), a ‘‘stock culture’’ was prepared using a growth medium that contained (per liter): 1 g glucose, 0.5 g yeast extract, 0.5 g casamino acid-peptone, 0.222 g of CaCl2 .2H2 O, 0.8 g of MgSO4 .7H2 O, 0.001 g of FeSO4 .7H2 O, 0.15 g of MnSO4 .H2 O, and 10 mL of a trace-element solution pH 7.0. The trace-element solution contained (per liter of deionized water): 10 mg of CuSO4 .5H2 O, 44 mg of ZnSO4 .7H2 O, 20 mg of CoCl2 .6H2 O, and 13 mg of Na2 MoO4 .2H2 O. Approximately 7.5 × 106 cells were transferred to 200 mL of growth medium and incubated for 28 days, at 30 ◦ C. The inoculum was prepared using 10 mL of stock culture and 90 mL of the growth medium. The inoculum was kept in an orbital shaker (RH Basic SI da IKA Labortechnik) at 150 rpm, 30 ◦ C for 5 days. Prior to the batch experiments, the culture was prepared using 20 mL of stock culture and 180 mL of the growth medium which was kept in an orbital shaker (RH Basic SI da IKA Labortechnik) at 150 min−1 , 30 ◦ C for 24 h. Thereafter, the culture was used to prepare solutions according to the experimental plan in Table S1. All batch experiments were performed at 30 ◦ C under stirring speed of 150 min−1 , in a 2-week-long period, maintaining the pH at 7.5 ±0.2 to avoid Mn removal by chemical precipitation. Experiment 1 corresponded to the condition of an aqueous solution of 150 mg L−1 Mn (II) with a culture containing B. cereus and the solid MnO2 . Experiment 2 corresponded to the condition of an aqueous solution of 150 mg L−1 Mn (II) with culture but without the solid MnO2 . Experiment 3 corresponded to the condition of with the culture and the solid MnO2 in order to verify if the bacteria would dissolve the solid MnO2 . Experiment 4 consisted of just an aqueous solution of 150 mg L−1 Mn (II) to evaluate the chemical precipitation of manganese in aqueous solution. Experiment 5 consisted of pure water with the solid MnO2 in the absence of the culture to evaluate the dissolution of MnO2 in aqueous solution. Conditions 2 and 5 were considered blank essays. R R In order to prevent bacterial growth, 4.0 mL of nipagin⃝ (0.14% w/v) and nipazol⃝ (0.1% w/v) was added in the essays 4 and 5. Aliquots of 5.0 mL were collected periodically, centrifuged at 3000 rpm and filtered through a 0.22 µm cellulose R nitrate membrane. The filtrate was acidified with sulfuric acid and analyzed by ICP-OES (Varian⃝ 725-ES) to evaluate the manganese concentration and pH. According to literature, biopolymers have been known to exhibit excellent adsorption ability for multivalent metal ions. Therefore, calcium alginate beads were used to fix and retain the B. cereus and solid MnO2 in order to test the manganese removal efficiency. Calcium alginate gel beads (Ca-alginate) were prepared at the concentration of 4%, according to the literature (Gok and Aytas, 2009; Cataldo et al., 2013). Firstly, 4% w/v of sodium alginate was prepared by adding 4.00 g of sodium alginate (Na-alginate) in 100 mL of water. The mixture was heated at approximately 155 ◦ C under magnetic agitation and cooled at room temperature. After cooling, 20 mL of 4% w/v Na-alginate was diluted in 40 mL of water and

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F.C.F. Camargo, G.L.C. Silva, H.L.B. de Leucas et al. / Environmental Technology & Innovation 15 (2019) 100398 Table 1 Mn 2p3/2 peak parameters: binding energy (eV) and percentage of Mn and O. Specie

B.E (eV)

%

Mn (IV) Mn (II) O2−

642.4 645.0 529.8

84.4 15.6 59.11

the solution was dropped with a 60.0 mL syringe into 100 mL of 2% w/v CaCl2 , under constant magnetic agitation. Beads were filtered and washed with water, then stored in water at 4 ◦ C for at least 24 h. A culture immobilized in gel beads of calcium alginate was also prepared by entrapping the culture in an alginate matrix produced by ionic polymerization in calcium chloride solution, according to the following steps: the 20 mL of culture were added to 20 mL Na-alginate (4% w/v) and 20 mL of water. The mixture was then dropped into 2% w/v CaCl2 solution under constant magnetic agitation. The resultant beads were filtrated, washed and stored in water at 4 ◦ C for at least 24 h. Ca-alginate beads containing manganese oxide (MnO2 ) and the culture were prepared by dropwise addition of homogeneous suspension containing 20 mL of culture, 20 mL of Na-alginate (4% w/v), 20 mL of water, 2 mL of MnO2 (17% w/w) and 100 mL of 2% w/v CaCl2 , under constant magnetic agitation. After that, the beads were washed with water and stored under the same conditions described above. 3. Results and discussion 3.1. Chemical and mineralogical characterization The solid MnO2 is a residue from the zinc electrowinning process, generated in the bottom of the electrowinning cell in the form of a sludge. The MnO2 content in this residue was around 56%, the specific surface area is 38.35 m2 g−1 and the grain size was 87% below 44 µm. X-ray diffraction showed that the main crystalline phases were gypsum (CaSO4 .2H2 O), a pyrolusite (β-MnO2 ) and cryptomelane K1−1,5 (Mn+4 ,Mn+3 )8 O16 . The full X-ray diffraction data is available in the supplementary material (Fig. S1). 3.2. X-ray photoelectron spectroscopy — XPS XPS is a useful technique for surface analysis due to its ability to determine elements on a solid surface and their oxidation states. Manganese oxides are generally expressed as MnOx because of the six stable Mn oxidation states, but only the states II, III and IV present significant multiplets that can be identified. Therefore, XPS analyses were carried out to identify the Mn species on the residue surface since the MnOx adsorption and catalytic properties depend on the Mn valence states. The Mn 2p3/2 peak is often used to provide oxidation state information because it yields the highest intensity signs of all other XPS Mn orbitals. The Mn2p region, characterized by a spin–orbit splitting (2p3/2 – 2p1/2 ) of 11.7 eV, is broadened by multiplet splitting and satellite structures (Moulder et al., 1992; Han et al., 2006; Katsoyiannis and Zouboulis, 2004; Nesbitt and Banerjee, 1998). The asymmetric signal at 642.2 eV is composed of two peaks; the most intense signal is 642.4 eV, which is attributed to the species Mn (IV) of MnO2 . These results comply with those found in the literature (Nesbitt and Banerjee, 1998; Wang et al., 2012) as well as those in the NIST Standard Reference Database, which described an Mn (IV) energy of 642.6 ± 0.5 eV. The second less intense energy signal 645 eV was assigned to free Mn (II). In the report by Moulder et al. (1992), the energy for this species ranged from 644.5 eV to 646.0 eV. The supplementary material shows further details about the XPS spectra of Mn 2p3/2 for the MnO2 residue (Fig. S2). The percentage of Mn (II) and Mn (IV) were 15.6% and 84.4%, respectively (Table 1). According to the literature, three oxygen species may be present in manganese oxide solids: the lattice oxygen (O2− ), hydrogen oxygen (OH− ) and oxygen in molecular water (H2 O), which can be chemisorbed or physisorbed as well as structural water and water in poor electrical contact with the mineral surface (Wang et al., 2012). It is possible to determine the oxygen species in the residue by evaluating the photopeak for each element. The binding energy of 529.8 suggested that the species of oxygen present in MnO2 is O2− . Similar values were found in the literature: 529.6 eV for synthetic birnessite (γ-MnO2 ) (Nesbitt and Banerjee, 1998), 529.4 eV for β-MnO2 nanopincers (Cheng et al., 2014), 529.4 for β-MnO2 (Santos et al., 2010) and 529.7 eV for manganese oxide recovering zeolite (Zou et al., 2006). Table 1 also shows the binding energy of the photoelectron peaks of O1s. 3.3. Thermogravimetric analysis — TGA Thermogravimetric analysis (TGA) was performed to assess the phase transformations of the residue submitted to intense heating. According to Berbenni and Marini (2003), Stobbe et al. (1999) and Sorensen et al. (2010), when heated in air at 500–1000 ◦ C, MnO2 decomposes into oxides with lower valence states. For example, pyrolusite (β-MnO2 ) transforms into bixbyite (Mn2 O3 ) between 625 ◦ C and 725 ◦ C and the Mn2 O3 changes into hausmannite (Mn3 O4 ) between 950 ◦ C and

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Fig. 1. Potentiometric mass titration curves for the PZC determination of MnO2 .

1050 ◦ C. Cryptomelane exhibits an analogous change of those occurring with the pyrolusite: a transformation to bixbyite (Mn2 O3 ) at about 600 ◦ C and to hausmannite (Mn3 O4 ) at about 900 ◦ C (Bish and Post, 1989). Mass weight loss observed between 0 ◦ C and 150 ◦ C was attributed to moisture. A progressive weight loss was observed at temperatures between 150 ◦ C and 500 ◦ C. According to Reis et al. (2010) and Figueira et al. (2008), this loss might be associated with the decomposition of hydrated minerals, such as gypsum (CaSO4 .2H2 O), present in the residue according to the X-ray analysis. At temperatures around 600 ◦ C, the weight loss occurred due to the transformation of MnO2 into Mn2 O3 . The weight loss at 950 ◦ C may be explained by the transformation of Mn2 O3 into Mn3 O4 . Fig. S3 shows the TGA data for MnO2 . 3.4. Zeta potential — PZC Solids in a liquid medium may gain electric charge, affecting the ion distribution in its vicinity. Thus, the concentration of counter-ions near the surface may increase, which creates an electric layer at the interface of the particle and liquid. Due to this double layer, the hydrated oxide surface exhibits ion exchange properties, which are correlated to the net charge on the oxide surface. Moreover, the net charge on the oxide surface depends on the solution pH because the solid surface may behave as an acid or a Brönsted–Lowry base. An important parameter to define whether the oxide surface will be negatively or positively charged is the pH measured when the net charge on the surface is equal to zero. This pH value is called point of zero charge (PZC) (Kosmulski, 2009). The results of the potentiometric mass titration are shown in Fig. 1. The intersection points of the four curves determined the PZC of the oxide as 7.36. In the literature, PZCs equal to 7.3 and 7.5 were found for natural pyrolusite (β-MnO2 ) when different methods were employed (Healy et al., 1966; Young et al., 2015; Mustafa et al., 2008). The PZC value of 7.36 may indicate that, under this pH, the surface of the manganese oxide is positively charged. This may hamper the Mn (II) adsorption for pHs higher than the PZC. 3.5. Adsorption isotherm The adsorption isotherm is always employed to explain the interaction between adsorbate and adsorbent because it establishes the nature of the interactions which govern the removal process. In this study, the Langmuir isothermal model was applied to fit the experimental data obtained at different temperatures (Eq. (1)): Q=

Qmáx* KL ∗ Ceq 1 + KL ∗ Ceq

(1)

In which Q is the amount of Mn (II) sorbed (mg g−1 ), Qmax is the maximum amount of Mn (II) sorbed on MnO2 (mg g−1 ), Ceq is the equilibrium concentration of Mn (II) (mg L−1 ) and KL is the Langmuir constant (L mg−1 ) that it is related to the sorption energy as a function of sorption enthalpy and temperature. The Langmuir model presents three assumptions: the surface of the adsorbent is uniform (all the adsorption sites are equivalent), adsorbed molecules do not interact, and all adsorptions occur through the same mechanism. Finally, Langmuir isotherm represents only monolayer

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Fig. 2. Adsorption isotherms for Mn (II) in MnO2 at different temperatures, pH = 7.0 ± 0.1 maintained with NaOH, time 24 h. Table 2 Langmuir parameters for Mn (II) adsorption on solid MnO2 and equilibrium parameter at different temperatures. Temperature ◦ C

Qmax (mg g−1 )

KL (L mg−1 )

R2

RL

25 30 40

25.80796 ± 0,94877 33.5592 ± 2,5115 53.87398 ± 2,43895

0.0527 ± 0,00651 0.0600 ± 0,0133 2.2358 ± 0,47297

0.98708 0.97083 0.96820

0.1213 0.0989 0.0032

adsorption processes, wherein the adsorption process ceases after the saturation of available sites. However, this model was also successfully used to describe the sorption phenomena in heterogeneous surfaces (Dabrowski, 2001; Scheufele et al., 2016). Fig. 2 shows the experimental data for different temperatures and the Langmuir model fitting. Fig. 2 shows that the Mn (II) sorption increases as the temperature rises. The maximum adsorption capacity improved from 25.81 mg g−1 (25 ◦ C) to 53.87 mg g−1 (40 ◦ C), demonstrating the endothermic character of the adsorption process (Table 2). At 40 ◦ C, the solid MnO2 presented a greater affinity to Mn (II), as evidenced by the sharp inclination of the isotherm curve, clearly showing that sorption still occurred even at low concentrations of manganese ions. Similarly to the adsorption capacity, the Langmuir constant (KL ) increased with the temperature rise, indicating that the binding energy between the sorbent and manganese ions is higher at elevated temperatures (Xu et al., 2012). According to Aguiar et al. (2013), at 25 ◦ C, the maximum amount of adsorbed Mn (II) on MnO2 is 32 mg g−1 , for a manganese initial concentration of 100 mg L−1 and pH at 7.0 ± 0.2. In general, isotherms can be considered as favorable or non-favorable by calculating the separation factor or equilibrium factor (RL ) (Eq. (2)), in which Co is the initial Mn(II) concentration. RL =

1

(2)

1 + KL ∗ C0

The RL value for each temperature indicates if the isotherms are irreversible (RL = 0), favorable (0 < RL < 1), linear (RL = 1) or unfavorable (RL > 1) (McCabe et al., 1993; Figueira et al., 2008; Xu et al., 2012). Table 2 shows that the values of RL suggested a favorable isotherm. In addition, the Langmuir model exhibited a good fit to the experimental data, once the correlation coefficients (R2 ) are close to 1. According to the Van’t Hoff equation (Eq. (3)), the values of enthalpy (1H◦ ) and entropy (1S◦ ) can be obtained from the slope and intercept of ln KL against 1/T: ln KL =

1S0 R

−

1H0 RT

(3)

In which KL is the Langmuir constant, which indicates the affinity of the composite to be adsorbed by the solid, calculated according to linear Langmuir isotherms (Fig. 2), R is the gas constant (8. 314 J mol−1 K−1 ) and T is the absolute temperature (K). In the present work, 1H◦ and 1S◦ were calculated by a curve-fitting program OriginPro as shown in Fig. 3.

F.C.F. Camargo, G.L.C. Silva, H.L.B. de Leucas et al. / Environmental Technology & Innovation 15 (2019) 100398

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Fig. 3. Influence of the temperature on the behavior of Mn(II) adsorption on solid MnO2 .

The Gibbs free energy (1G◦ ) was calculated according to Eq. (4) (Gok and Aytas, 2009; Donat and Aytas, 2005; Dal Bosco et al., 2005).

1G0 = 1H0 − T1S0

(4)

The high and positive value obtained for 1H0 (205.84 kJ mol−1 ) indicated an endothermic process, suggesting that a high amount of heat must be transferred to dehydrate the Mn (II) ions in the solution in order to render them available for adsorption. Another phenomenon that may account for this high value is the adsorption of water molecules on the solid surface (Birkner, 2015). The positive entropy of 0.66 kJ K−1 mol−1 indicated an increase of the system disorder, which may be attributed to two factors: (i) the Mn (II) on interactions with the active sites of the adsorbent, which goes through structural changes (Xu et al., 2012); (ii) the reduction of adsorbed metallic ions dehydration (Eren et al., 2011). The values of 1G◦ suggested that the Mn (II) adsorptions were non-spontaneous under temperatures of 25 ◦ C and 30 ◦ C (1G◦ = 8.51 kJ mol−1 and 5.20 kJ mol−1 , respectively) and spontaneous at 40 ◦ C (1G◦ = −1.42 kJ mol−1 ). It was also noticeable that the spontaneity degree rose as the temperature of the system increased. 3.6. Sorption kinetics The study of sorption kinetics is important to understand the reaction pathway and the sorption mechanisms as well as to describe the solute uptake rate. Therefore, the kinetics may provide information about the rate at which the manganese is removed. The formation rate of manganese oxides from Mn (II) ions in aqueous systems have been investigated by various researchers because these solids not only act as self-catalysts, but also can promote the removal of other metals in the medium. In the present work, the kinetics of Mn (II) adsorption by MnO2 was assessed by adjusting two different models: Lagergren’s first-order equation and Ho’s second-order expression (Ho and McKay, 1998a,b, 1999; Ho, 2006). Lagergren’s first-order equation or pseudo-first-order equation (Eq. (5)) was presented by Ho and McKay (1998a): dqe dt

= kp1 (qe − qt )

(5)

In which qe and qt (mg g−1 ) are the adsorption capacities at equilibrium and a determined time (min), respectively, and velocity constant kp1 (min−1 ) is the pseudo-first rate constant for the kinetic model. The integration of Eq. (5), assuming the boundary conditions of qt = 0 to t = 0 and qt = qt to t = t, generates Eq. (6): ln(qe − qt ) = ln qe − kp1 t

(6)

The pseudo-first-order equation is a model which describes the adsorption rate based on the adsorption capacity of solids in liquid–solid systems. According to Ho and McKay (1998b), for most of the adsorbent/adsorbate systems, the Lagergren’s first order equation does not adjust well to the full range of contact time and it is generally applicable only in the first 30 min of the adsorption process. Therefore, Ho and McKay (1999) proposed the pseudo-second-order to describe adsorption processes which were not well fit into the pseudo-first-order equation.

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Fig. 4. Kinetic experiments under different temperatures, pH = 7.0 ± 0.1 adjusted with NaOH, [Mn] = 150 mg L−1 and MnO2 mass of 2.00 g.

The pseudo-second-order equation is described by Eq. (7), in which qe and qt (mg g−1 ) are the adsorption capacity at equilibrium and a determined time (min), respectively; kp2 (g mg−1 min−1 ) is the pseudo-second order kinetic constant and the component (qe − qt ) is proportional to the available fraction of the active sites (Qiu et al., 2009). dqt dt

= kp2 (qe − qt )2

(7)

By integrating Eq. (8) for the boundary conditions qt = 0 to t = 0 and qt = qt to t = t, Eq. (8) is obtained: 1 (qe − qt )

=

1 qe

+ kp2 t

(8)

Pseudo-second-order assumes that the rate-limiting step is the surface adsorption involving chemisorption, in which the removal is due to physicochemical interactions between the two phases and the sorption capacity is proportional to the number of active sites occupied on the sorbent. A number of authors have applied this model to describe the removal of metal and organic substances from effluents and soils using solid substrates (Robati, 2013; Ho and McKay, 1999; Qiu et al., 2009; Zou et al., 2006; Ho, 2006; Puppa et al., 2013). As the first model adjusted to experimental data only at the beginning of the experiment, the adsorption was believed to happen in two phases and only the first one would fit into the Lagergren’s first-order equation. In the case of the pseudo-second-order equation, the chemical sorption was contemplated it represents the slowest phase of the process since covalent bonds between the sorbent and sorbate are formed. Therefore, the pseudo-second order model adjusted to the experimental data throughout the entire process (Ho and McKay, 1999). Taking into consideration the fact that the rate-limiting step of Mn (II) removal by the solid MnO2 may happen through a chemical sorption, the two models mentioned above were applied for the kinetic analysis. Fig. 4 shows that the adsorption kinetics was fast at the beginning, and the mean lifetime for Mn (II) sorption was below 8 min of reaction, slowing down over time. Fig. 5a was obtained by plotting ln (qe − qt ) as a function of time (t) and the pseudo-first order kinetic model was adjusted to the data. The values of the velocity constant kp1 (min−1 ) and the adsorption capacity of the substrate at equilibrium qe (mg g−1 ) corresponds to the slope and intercept of the curve. The adjustment to the pseudo-second order (Fig. 5b) was made by plotting the t/qt values as a function of time (t). The velocity constant kp2 (g mg−1 min−1 ) and qe (mg g−1 ) were determined in a way similar to the pseudo-first model. Table 3 depicts the values of adsorption capacities at equilibrium in different temperatures by using from pseudo-firstorder and pseudo-second order models as well as the correlation coefficients (R2 ). The correlation coefficients (R2 ) showed that the pseudo-second order model, which is used to describe chemiosorption processes (Zou et al., 2006), is the one that best fits into the experimental data. The adsorption capacity of the solid increased as the temperature rose, indicating an endothermic process, in accordance with the adsorption isotherms analysis. Dal Bosco et al. (2005) studied the sorption of some metals, including Mn (II), by natural zeolites (scolecite), and they demonstrated that the kinetic model that best fits the process was the pseudo second order model. Puppa et al. (2013) also proposed this model in the study of copper, cadmium, lead and zinc removal by the birnessite.

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Fig. 5. Curves obtained by the adjustment of the pseudo-first order and pseudo-second order kinetic model to the adsorption experimental data. Table 3 Kinetic parameters obtained for the Mn (II) sorption by MnO2 at different temperatures with the respective correlation coefficient (R2 ). Temperature (◦ C)

Pseudo first order k1 (min−1 )

qe (mg g−1 )

R2

k2 (g mg−1 min−1 )

Pseudo second order qe (mg g−1 )

R2

qe mg g−1

Experimental

25 30 35 40

0.01122 0.00845 0.00855 0.01148

5.6587 4.7737 5.5695 6.7729

0.9263 0.8755 0.9056 0.9588

0.0062 0.0036 0.0042 0.0038

11.5447 12.6390 13.0412 13.5685

0.9986 0.9986 0.9972 0.9985

11.345 12.625 12.975 13.333

The amount of adsorbed metal ions per mass unit of adsorbent was determined from the measured bulk concentrations, using the following equation (Eq. (9)): qe =

V (C0 − Ce ) m

(9)

In which q (mg g−1 ) is the adsorbent sorption, C0 and Ce (mg L−1 ) are the initial and equilibrium concentrations of Mn, V (L) is the volume of the solution added to the sorbent and m (g) is the weight of the employed sorbent. The experimental adsorption capacities at equilibrium calculated by Eq. (9) were close to the values found for the pseudo-second order kinetic, model indicating that this model is suitable to explain the manganese removal by MnO2 (Table 3). 3.7. Chemical/biological removal 3.7.1. Batch culture experiments and MnO2 Fig. 6a shows the Mn (II) percentage as a function of time. The association B. cereus + MnO2 promoted a higher removal only on the first three days when compared to the chemical (MnO2 ) and biological (B. cereus) methods separately. After the ninth day, the removal with the association was approximately 96%, similar to the amount reached with the use of oxide alone. At the end of the fifteenth day, 99% of Mn (II) was removed, whereas for solutions containing only the B. cereus, the removal was less efficient and reached only 75%. The removal kinetics of manganese was enhanced in the presence of B. cereus + MnO2 , reaching 80% in three days. In the absence of B. cereus, the removal in 3 days was close to 60%. Manganese removal by B. cereus cultivated in the same grown medium employed in the present study was investigated for Reis et al. (2017) and the metal removal was 95% of Mn (II) present in the initial solution (50 mg L−1 ) on the fourteenth day. In the chemical control (experiment without MnO2 and culture), approximately 18% of the Mn present in a solution containing 150 mg L−1 of Mn (II) was precipitated at the end of the fifteenth day (Fig. 6a). It was investigated the influence

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Fig. 6. Manganese removal by Bacillus cereus and MnO2 , with pH monitoring, [Mn]initial = 150 mg L−1 , under agitation at 150 min−1 , pH = 7.5 and T = 30 ◦ C.

of MnO2 on increasing Mn concentrations in solution, it was observed that there was no MnO2 degradation incurred by the B. cereus, nor MnO2 solubilization in deionized water (data no shown). Fig. 6b shows that for the essays with the MnO2 solid, the pH reduced for values up to 5.7 in the first 24 h, and daily addition of NaOH was necessary to maintain the pH at 7.5. For the system of Mn (II) solutions with B. cereus, the pH remained between 7.5 and 8.5, and for the experiment with B. cereus + MnO2 , the pH stabilized between 6.8 and 7.7. As the removal of Mn proved more effective in higher pH, usually above 7.5, this was the main advantage of using bacteria since there is no need to add NaOH, as required in the experiment carried out with only MnO2 . Barboza et al. (2015) carried out removal experiments with solutions of Mn (II) 50 mg L−1 using a culture isolated from water samples collected from a manganese mine in the Iron Quadrangle region (Minas Gerais, Brazil). The results showed that Mn (II) decreased continuously throughout 15 days, presenting a removal efficiency of 99.7% and a pH variation between 7.36 (initial) and 7.86 (final). The authors associated the rise in pH with bacterial growth, given the fact that the pH in the control solution remained stable at 7.4 and no significant removal occurred. Also, as part of the study, Barboza et al. (2015) isolated the bacteria present in the culture and identified three types (Bacillus, Stenotrophomonas and Lysinibacillus) resistant to Mn concentrations of 1200 mg L−1 . Throughout all removal experiments, the authors observed an improvement in the Mn removal and a rise in pH values (up to 8.5). The authors suggested that the rise in pH occurred due to microbial metabolism, which promotes the chemical oxidation of Mn, and in turn, the formation of MnO2 . Reis et al. (2017) investigated manganese removal in a batch test containing 50 mg L−1 of Mn (II) and stock culture containing B. Cereus, at pH 7.0. According to the authors, on the fourteenth day, the maximum removal of manganese (46.8 ±0.21 mg L−1 ) was attained and no significant changes were observed until the twentieth day. The maximum microbial growth and pH values up 8.0 were also observed on the fourteenth day. By associating the results found by Barboza et al. (2015), Reis et al. (2017) and the ones found in the present study, the hypothesis of the occurrence of chemical removal of Mn (II) though the rise in pH caused by microbial metabolism can be supported. 3.7.2. Experiments with culture of B. cereus and MnO2 immobilized in alginate biopolymer (ALG) As an attempt to improve the manganese removal, chemical/biological batch essays were carried out by using a culture of B. cereus along with the solid MnO2 both immobilized in alginate biopolymer (Fig. S4). Alginate biopolymer is largely

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Fig. 7. (a) Removal of manganese by Bacillus cereus and MnO2 immobilized in Ca-alginate (b) Variation of pH in the removal of Mn with culture and MnO2 immobilized in Ca-alginate spheres. [Mn]initial = 150 mg L−1 , agitation at 150 min−1 , T = 30 ◦ C.

used in cell immobilization studies and biosorption of metals. The advantages of this technique include biomass retention within the working environment, biocompatibility, easy separation of products from cells, high affinity for metals and ability to form gel (Al-Rub et al., 2004; Cataldo et al., 2013; Xu et al., 2012; Garnham et al., 1992; Gok and Aytas, 2009; Gotoh et al., 2004). The removal of manganese using Ca-alginate spheres is depicted in Fig. 7a. After 9 days, the removal reached 93% when microorganisms only immobilized in Ca-alginate were used, and 92% when bacteria immobilized in spheres and MnO2 were applied. The results obtained with the Ca-alginate + MnO2 (59%) and only Ca-alginate (51%) showed similar removal. This low value of manganese removal using immobilized MnO2 was due to the low amount of oxide in the spheres, which is well below the 2.00 g used in the batch experiments without immobilization. Attempts to immobilize larger amounts of MnO2 in alginate were not successful. The significant removal of 51% of Mn (II) by alginate spheres can be explained by the fact that these polymers hold carboxylic groups capable of sorbing ions from solution. Some authors, such as Plazinski (2011), Cataldo et al. (2014), Gok and Aytas (2009), Al-Rub et al. (2004) and Paul et al. (2006) investigated adsorption of metals such as Cu (II), Cd (II), U (IV), Ni (II) an Pb (II) using Ca-alginate spheres and attested the sorption of these elements. Fig. 7b shows the pH profile during the removal of Mn with alginate spheres. The pH rose gradually keeping values between 7.0 and 8.5 in all conditions. The pH variation throughout the experiment using Ca-alginate is lower if compared to the experiments without immobilization in Ca-alginate (Fig. 6b). According to Morgan and Stumm (1964) and Hem (1981) when adsorbed on the surface of a solid, Mn (II) is oxidized to MnO2 and as a result of this reaction H+ is produced resulting in a pH drop. Therefore, the supposition that the amount of solid MnO2 in the spheres is low was confirmed because no significant pH changes were observed (Fig. 7b). As far as the immobilization of the culture is concerned, at the end of a nine day period, the removal was more effective and reached 92% in relation to 66% attained for bacteria free in the solution, either due to the maintenance of an alkaline pH or to the contribution of the Ca-alginate in the adsorption. Experiments are under development to define a methodology which is able to immobilize a greater MnO2 amount, improving the removal efficiency. In the batch experiments without immobilization in alginate (Fig. 6a), Mn (II) removal reached 99% at the end of a 15 day period, when MnO2 was used alone. However, when the B. cereus and MnO2 were immobilized in alginate, the same removal was reached with the solution pH kept between 7.5 and 8.5, preventing the consumption of base and making the use of B. cereus suitable. Barboza et al. (2016) studied manganese removal by manganese-oxidizing bacteria including B. cereus and proposed that bacterial growth promotes an increase in pH values, therefore, the biological manganese oxidation by the isolates

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and the consortium followed a nonenzymatic pathway because the final pH attained values in which chemical manganese oxidation predominated. According to Reis et al. (2017), increases in pH and manganese removal were only observed in those tests performed with B. cereus, implying that the pH profile is defined by the bacterial metabolism. Further studies are required to elucidate the description of manganese removal mechanism by B. cereus. 4. Conclusions The results showed that the Mn uptake is described by Langmuir adsorption isotherm, which provided the maximum uptake around 54 mg g−1 at 40 ◦ C. The pseudo-second-order kinetic model was the one that best fitted the kinetic data. Thermodynamic parameters showed the spontaneous and endothermic nature of the process of Mn (II) uptake by MnO2 . Solid MnO2 , when added directly to a solution, was able to remove high levels (up to 96%) of manganese (150 mg L−1 ). When the solid MnO2 was trapped in Ca-alginate, 59% of manganese was removed probably due to the small amount of residue that was immobilized. The Mn (II) removal using only B. cereus (75%) was lower than the one using B. cereus immobilized in Ca-alginate (93%). It is possible that Ca-alginate also contributed to the uptake of the Mn (II) ion. B. cereus and MnO2 together removed 96% of Mn in solution; however, the addition of small amounts of alkali was necessary. B. cereus and MnO2 immobilized in alginate were able to remove 96% of Mn in solution as well; however, the addition of alkali was not necessary. In conclusion, B. cereus in combination with Ca-alginate was able to maintain the pH between 7.5 and 8.5 avoiding the addition of alkalis. In addition, the use of Ca-alginate as an immobilizer agent is necessary for industrial purposes. 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