Low-Cost Electrode Modification to Upgrade the Bioelectrocatalytic Oxidation of Tannery Wastewater Using Acclimated Activated Sludge
Low-Cost Electrode Modification to Upgrade the Bioelectrocatalytic Oxidation of Tannery...
Elabed, Alae;El khalfaouy, Redouan;Ibnsouda, Saad;Basseguy, Régine;Elabed, Soumya;Erable, Benjamin
2019-05-31 00:00:00
applied sciences Article Low-Cost Electrode Modification to Upgrade the Bioelectrocatalytic Oxidation of Tannery Wastewater Using Acclimated Activated Sludge 1 , 2 3 2 , 4 1 Alae Elabed , Redouan El khalfaouy , Saad Ibnsouda , Régine Basseguy , 2 , 4 1 , Soumya Elabed and Benjamin Erable * Laboratoire de GénieChimique, Université de Toulouse, CNRS, INPT, UPS, 31432 Toulouse, France; alae.elabed@gmail.com (A.E.); regine.basseguy@ensiacet.fr (R.B.) Laboratoire de Biotechnologie Microbienne, Faculté des Sciences et Techniques, Fès 30000, Maroc; saad.ibnsouda@usmba.ac.ma (S.I.); soumya.elabed@usmba.ac.ma (S.E.) Laboratoire de Science et Technologie du Génie des Procédés, Université Sidi Mohamed Ben Abdellah, Fès 30000, Maroc; redouan.elkhalfaouy@usmba.ac.ma Centre Universitaire Régional d’Interface, Université Sidi Mohamed Ben Abdellah, Fès 30000, Maroc * Correspondence: benjamin.erable@ensiacet.fr Received: 3 May 2019; Accepted: 29 May 2019; Published: 31 May 2019 Abstract: Eective and eco-friendly technologies are required for the treatment of tannery wastewater as its biological toxicity and large volume leads toground water pollution. Hydrophobic (unmodified carbon felt) and hydrophilic modified carbon felt with Linde Type A zeolite (LTA zeolite) and bentonite were examined for their eects on bacterial attachment, current generation, and tannery wastewater treatment eciency. Chronoamperometry and cyclic voltammetry confirmed the higher electron transfer obtained with modified anodes. Maximum current densities of 24.5 and 27.9 A/m were provided with LTA zeolite and bentonite-modified anodes, respectively, while the unmodified carbon felt gave a maximum current density of 16.9 A/m . Compared with hydrophobic unmodified carbon felt, hydrophilic modified electrodes increased the exploitation of the internal surface area of the 3D structure of the carbon felt by the electroactive biofilm. The study revealed 93.8 1.7% and 96.3 2.1% of chemical oxygen demand (COD) reduction for LTA zeolite and bentonite, respectively. Simultaneous chromium removal was achieved with values of 94.6 3.6 and 97.5 2.2 for LTA zeolite and bentonite, respectively. This study shows the potential approach of carbon felt clay modification for the ecient tannery wastewater treatment using bioelectrochemicals systems (BESs) accompanied with high current recovery. Keywords: clay; acclimated sludge; LTA zeolite; bentonite; tannery wastewater; bioelectrochemical systems 1. Introduction Microbial fuel cells (MFCs) technologies have a potential application in simultaneous wastewater treatment and electricity generation [1,2]. In fact, this technology is able to convert the chemical energy contained in organic and inorganic chemical compounds directly into electricity via microbial bioanodes [3,4]. The performance of MFCs, in terms of current production and euent treatment, show considerable variation due to the MFC designs and the electrode materials used. Many electrode materials have been tested to treat domestic or industrial wastewater in MFCs [5]. However, weak anodic performance, primarily limited by the extracellular electron transfer between the exoelectrogenic bacteria and the anode, represents a major problem for the scaling-up and future practical application of MFCs. Thus, ecient modification of anode electrodes is predicted to improve power output in MFCs [6–9]. For instance, carbon felt coating with akaganeite (b-FeOOH) was found to improve the Appl. Sci. 2019, 9, 2259; doi:10.3390/app9112259 www.mdpi.com/journal/applsci Appl. Sci. 2019, 9, 2259 2 of 11 electrochemical performance of a MFC by increasing the peak current density of the oxidation reaction 2 2 from 0.7 to 6.1 A/m . A maximum power density of 504 mW/m was obtained with the anode modified MFCs, which was 2.3 times higher than that with the unmodified anode [8]. Paul et al. (2017) reported a 3.6-times higher power density with carbon felt anodes modified with graphene oxide (GO)-zeolite composite (GZMA), than that of the unmodified anodes. The highly porous structure and increased hydrophilicity of zeolite with a few layers of thin GO oered better adhesion and higher surface area for bacterial cells to attach to the electrode, which improved anodic kinetics resulting in a greater performance of the MFC. Although considerable progress has been made recently regarding anode modification for the improvement of MFC energy recovery eciency, most of this research was restricted to synthetic media only. In contrast, the bioanode designed to treat real wastewater still faces practical barriers such as low current density leaving a large gap between real raw wastewater and synthetic media [10]. The present study developed practical, easily fabricated, and low-cost modified electrode materials by Linde Type A (LTA) zeolite and bentonite to assist the bioelectrocatalytic oxidation of tannery wastewater by using an acclimated sludge obtained from a wastewater treatment plant. To the best of our knowledge, this was the first approach to combine both acclimation of activated sludge and electrode modification for the treatment of full strength tannery wastewater without any supplements of salt or vitamins in the BESs. 2. Material and Methods 2.1. Activated Sludge Acclimation to Industrial Tannery Wastewater The tannery wastewater euent was collected from industrial tanneries of Fez (Morocco). Initial COD of 5680 mg/L, total chromium of 651 mg/L, and pH 4.8 were quantified in the raw wastewater collected. Activated sludge was collected from a domestic wastewater treatment plant (Castanet-Tolosan, France). The synthetic acclimation medium consisted of (gL ) KH PO : 4.4, 2 4 K HPO : 3.4, NH Cl: 1.3, NaCl: 0.5, acetate: 1.0, CaCl : 0.0146, NaHCO : 1.0, yeast extract: 0.375, 2 4 4 2 3 peptone: 0.375. Prior to use, the supernatant of the centrifuged activated sludge was replaced with synthetic medium, then incubated for 24 h at 30 C. After that, the pellet was decanted and fresh synthetic medium with 20% of tannery wastewater was added to recover the original volume. The procedure of settling, decanting, and addition of synthetic medium and tannery wastewater was repeated at 24 h intervals, increasing the proportion of tannery wastewater by 20% each day, until the entire synthetic medium was replaced by tannery wastewater. 2.2. Preparation of Clay-Modified Electrodes LTA zeolite and bentonite-modified electrodes were prepared as films coated on carbon felt electrodes. LTA zeolite was synthesized following the protocol of Belaabed et al. [11] and bentonite was purchased from Sigma–Aldrich (France). Before deposition, the carbon felt electrode surface was washed with acetone and rinsed with water and ethanol. LTA zeolite and bentonite-modified carbon was prepared by hand mixing 1 g of LTA zeolite or bentonite in 100 mL of ethanol solution. Then, the carbon felt (2 cm ) was placed in the solution and sonicated for 30 min. The modified carbon felt was finally dried at 100 C [12]. 2.3. Characterization of Unmodified and Modified Electrodes FTIR absorption spectra of the unmodified and modified carbon anodes were recorded by a VERTEX 70 Optic spectrophotometer (Bruker) in the wave numbers range from 400 to 1400 cm . The specific surface areas (SSAs) of the anode materials were determined from an N adsorption–desorption experiment with an ASAP 2020 surface area analyzer (BET method). The hydrophobicity of the anode surfaces was determined by contact angle measurement using a goniometer (GBX Instruments, France). Appl. Sci. 2019, 9, 2259 3 of 11 2.4. Electroanalytical Techniques All the experiments were run in three-electrode (single chamber) bioelectrochemical reactors (600 mL) and were conducted at 30 C. Each bioreactor was equipped with a 2 cm projected surface area, working electrodes connected electrically via a thin platinum wire, a saturated calomel electrode (SCE) (SCE, +0.24 V vs. standard hydrogen electrode), and a 6 cm platinum grid auxiliary electrode. All the working electrodes were polarized at 0.2 V/SCE using a multi-channel potentiostat (Biologic VSP2). The polarization was periodically suspended to perform cyclic voltammetries at 1 mV/s in the potential range from 0.5 to 0.2 V/SCE. After inoculation, each reactor was purged with N for 30 min in order to create anaerobic conditions. 2.5. Biofilm Visualization A series of Environmental Scanning Electron Microscopy (ESEM) and epifluorescence microscopy images were taken to provide a visual characterization of electrode modifications and the surface morphologies of the biofilm growing over the electrode. Prior to ESEM imaging, fixation was performed using phosphate buer (400 mM, pH = 7.4) with 4% glutaraldehyde. The samples were rinsed in phosphate buer containing saccharose (0.4 M) and then dehydrated by immersion in increasing concentrations of the following solutions: acetone (50%, 70%, 100%), acetone and hexamethyldisilazane (50:50), 100% hexamethyldisilazane (HMDS). The last batch of HMDS was dried until all the moisture was removed. Prior to epifluorescence microscopy and in order to eliminate all soluble and solid materials except the attached biofilms, microbial biofilms developed on electrodes were washed with sterile physiological water. Before being left to dry at room temperature, bioelectrodes were colored with 0.03% acridine orange (A6014, Sigma) for 10 min. The biofilms were imaged using a Carl Zeiss Axio Imager-M2 microscope equipped for epifluorescence with an HXP 200 C light source and the Zeiss 09 filter (excitor HP450e 490, reflector FT 10, barrier filter LP520). Images were obtained with a digital camera (Zeiss AxioCamMRm) every 0.5 m along the Z-axis and the set of images was processed with the Zen software. 2.6. Wastewater Analysis Techniques COD and total chromium were analyzed according to standard methods [13]. COD was measured using a photometric cuvette test (LCK514 kit, DCO measurement 100–2000 mgO2/L). The % COD removal is defined as: COD COD initial final % COD removal = 100 COD initial The Coulombic eciency (CE) is defined as the ratio of total Coulombs actually transferred to the anode from the substrate and is calculated by: M I dt % CE = 100 FbVDCOD where M stands for the molecular weight of the substrate, F is Faraday’s constant (96,485 C/mol), b is the number of moles of electrons produced per mol of the substrate, V is the volume of liquid in the anode compartment, and DCOD is the change in COD over time t. Total chromium was determined by Inductively Coupled Plasma Atomic Emission Spectroscopy (ICP-AES). Each test was performed in triplicate and the mean values were recorded with standard deviations. Cr Cr initial final % Cr removal = 100 Cr initial Student t-test for COD removal, chromium removal, and CEs were conducted between modified and unmodified carbon felt. The significance level of statistical analyses was set at = 0.05. Appl. Sci. 2018, 8, x FOR PEER REVIEW 4 of 11 Student t-test for COD removal, chromium removal, and CEs were conducted between modified Appl. Sci. 2019, 9, 2259 4 of 11 and unmodified carbon felt. The significance level of statistical analyses was set at α = 0.05. 3. Results and Discussion 3. Results and Discussion 3.1. Effect of Activated Sludge Acclimation on Electroactive Biofilm Formation 3.1. Eect of Activated Sludge Acclimation on Electroactive Biofilm Formation Raw industrial tannery wastewater inoculated with 5% (v/v) of acclimated or unacclimated Raw industrial tannery wastewater inoculated with 5% (v/v) of acclimated or unacclimated activated sludge was first tested in three-electrode bioelectrochemical reactors. Unmodified carbon activated sludge was first tested in three-electrode bioelectrochemical reactors. Unmodified carbon felt material polarized at −0.2 V/SCE was used for the working electrodes, and two successive felt material polarized at 0.2 V/SCE was used for the working electrodes, and two successive additions of 20 mM acetate were made at t0 and t17days to accelerate the growth kinetics of the biofilm. additions of 20 mM acetate were made at t and t to accelerate the growth kinetics of the biofilm. 0 17days The bioelectrochemical reactor inoculated with the unacclimated activated sludge did not produce The bioelectrochemical reactor inoculated with the unacclimated activated sludge did not produce any any current during the 40 days of testing (Figure S1). current during the 40 days of testing (Figure S1). In contrast, with the progressively acclimated sludge, after a 5day lag phase, a rapid increase in In contrast, with the progressively acclimated sludge, after a 5 day lag phase, a rapid increase in current density was detected from day 5 to day 9. The current density reached a maximum exceeding current density was detected from day 5 to day 9. The current density reached a maximum exceeding 16 A/m² and gradually decreased after day 19 as the acetate availability was limited. The week of 16 A/m and gradually decreased after day 19 as the acetate availability was limited. The week of progressive acclimation of activated sludge helped the bacterial population growth to resist the usual progressive acclimation of activated sludge helped the bacterial population growth to resist the usual negative effects of toxic substances present in tannery wastewater. negative eects of toxic substances present in tannery wastewater. 3.2. Eect of Carbon Felt Modification 3.2. Effect of Carbon Felt Modification 3.2.1. Physicochemical Characterization of the Unmodified and Modified Carbon Felt Surfaces 3.2.1. Physicochemical Characterization of the Unmodified and Modified Carbon Felt Surfaces The FTIR spectra of the unmodified carbon felt before and after modification are shown in Figure 1 The FTIR spectra of the unmodified carbon felt before and after modification are shown in Figure and confirmed the successful electrode modification. The IR spectrum of LTA zeolite-modified carbon 1 and confirmed the successful electrode modification. The IR spectrum of LTA zeolite-modified 1 1 1 shows new peaks at 460 cm , 575 cm , and 1090 cm corresponding to vibrational modes bending −1 −1 −1 carbon shows new peaks at ≈ 460 cm ,575 cm , and 1090 cm corresponding to vibrational modes T–O, double six-rings, and asymmetric stretching vibration of internal tetrahedral T–O–T (with T = Al bending T–O, double six-rings, and asymmetric stretching vibration of internal tetrahedral T–O–T or Si), respectively, which are the dominating building units in the zeolite structure. Similarly, new (with T = Al or Si), respectively, which are the dominating building units in the zeolite structure. 1 1 1 peaks appeared at 460 cm , 525 cm , and 1090 cm in modified bentonite carbon felt spectra, which −1 −1 −1 Similarly, new peaks appeared at 460 cm ,525 cm , and 1090 cm in modified bentonite carbon felt were attributed to the bending vibration of Si–O–Si, bending vibration of Al–O–Si, and stretching spectra, which were attributed to the bending vibration of Si–O–Si, bending vibration of Al–O–Si, vibration of Si–O, respectively. Additionally, the IR bands between 640 and 950 cm were due to the −1 and stretching vibration of Si–O, respectively. Additionally, the IR bands between 640 and 950 cm bending vibration of T–OH–T (with T = Al or Fe or Mg). were due to the bending vibration of T–OH–T (with T = Al or Fe or Mg). LTA zeolite modified carbon felt Bentonite modified carbon felt Carbon felt O-T-O T-O-T T-O T-OH-T Al-O-Si Si-O Si-O-Si 400 600 800 1000 1200 1400 -1 Wavenumber (cm ) Figure 1. FTIR analysis of modified and unmodified carbon felt. Figure 1. FTIR analysis of modified and unmodified carbon felt. The modified electrode mass increased by 0.1 and 0.14 g due to the deposition on carbon felt of LTA zeolite and bentonite, respectively. Transmittance (%) Appl. Sci. 2018, 8, x FOR PEER REVIEW 5 of 11 Appl. Sci. 2019, 9, 2259 5 of 11 The modified electrode mass increased by 0.1 and 0.14 g due to the deposition on carbon felt of LTA zeolite and bentonite, respectively. As observed by ESEM in Figure 2, the unmodified carbon felt was composed of intermingled As observed by ESEM in Figure 2, the unmodified carbon felt was composed of intermingled tubular fibers with an average diameter of 15–20 m. The surface of fibers was soft and clean. As a tubular fibers with an average diameter of 15–20 µm. The surface of fibers was soft and clean. As a consequence of the carbon felt modification by LTA zeolite and bentonite, the presence of crystalline consequence of the carbon felt modification by LTA zeolite and bentonite, the presence of crystalline solid particles was observed, randomly dispersed on the surface of the carbon fibers. More precisely, solid particles was observed, randomly dispersed on the surface of the carbon fibers. More precisely, the ESEM images of LTA zeolite and bentonite-modified carbon felt revealed a particle size ranging the ESEM images of LTA zeolite and bentonite-modified carbon felt revealed a particle size ranging from 2 to 4 m for elementary crystals forming individual deposits or aggregates non-uniformly from 2 to 4 µm for elementary crystals forming individual deposits or aggregates non-uniformly distributed around carbon fibers. distributed around carbon fibers. Figure 2. ESEM images of unmodified and modified carbon felt. (A) Commercial carbon felt, (B) Linde Figure 2. ESEM images of unmodified and modified carbon felt. (A)Commercial carbon felt, (B) Linde Type A (LTA) zeolite-modified carbon felt, (C) Bentonite-modified carbon felt. Type A (LTA) zeolite-modified carbon felt, (C) Bentonite-modified carbon felt. The SSA of the modified carbon felt increased from 6.2 to 13.3 and 16.7 m /g for LTA zeolite The SSA of the modified carbon felt increased from 6.2 to 13.3 and 16.7m²/g for LTA zeolite and and bentonite, respectively (Table S1). This augmentation of the SSA of the electrode material, by a bentonite, respectively (Table S1). This augmentation of the SSA of the electrode material, by a factor factor greater than 2, was mainly due to the mesoporous and microporous structures of the clay greater than 2, was mainly due to the mesoporous and microporous structures of the clay minerals, minerals, which can provide more sites for electroactive biofilm and consequently increases current which can provide more sites for electroactive biofilm and consequently increases current generation generation [14]. [14]. TheThe carbon carbon felt modification felt modification by clay minera by clay mineral coating l coati also had ng al anso had a eect on n the ef surface fect on the surf hydrophobicity ace . After hydrophobi coating,city. Af the surface ter coa of the ting, the carbon felt surfa changed ce of tcompletely: he carbon felt chan from superged hydr completely: from ophobic it became superhydrophobic it became superhydrophilic. The carbon hydrophobicity makes the diffusion of superhydrophilic. The carbon hydrophobicity makes the diusion of the electrolyte toward the felt the electrolyte toward the felt more difficult than in a hydrophilic architecture and consequently more dicult than in a hydrophilic architecture and consequently facilitates the biofilm colonization facilitates the biofilm colonization inside the 3D carbon felt [15]. inside the 3D carbon felt [15]. 3.2.2. Electrochemical Performances of Tannery Wastewater Oxidizing Bioanodes 3.2.2. Electrochemical Performances of Tannery Wastewater Oxidizing Bioanodes 3.2.2.1. Chronoamperometry Analysis Chronoamperometry Analysis The ability to generate a current of oxidation on unmodified electrodes and electrodes modified The ability to generate a current of oxidation on unmodified electrodes and electrodes modified by clay minerals was evaluated directly in real tannery wastewater completed with acetate (20mM). by clay minerals was evaluated directly in real tannery wastewater completed with acetate (20 mM). The experiments were conducted in parallel and were inoculated at the same time with the same The experiments were conducted in parallel and were inoculated at the same time with the same acclimated activated sludge (5% v/v). All the working electrodes were maintained at −0.2 V vs. SCE. acclimated activated sludge (5% v/v). All the working electrodes were maintained at 0.2 V vs. SCE. The current density on LTA zeolite and bentonite-modified electrodes increased rapidly after the The current density on LTA zeolite and bentonite-modified electrodes increased rapidly after the inoculation, reaching 1.5 A/m² and 0.5 A/m², respectively, after only 2 days (Figure 3). Then, the 2 2 inoculation, reaching 1.5 A/m and 0.5 A/m , respectively, after only 2 days (Figure 3). Then, the current decreased because of acetate depletion. Successive additions of 20 mM acetate restarted the current decreased because of acetate depletion. Successive additions of 20 mM acetate restarted the current generation. After the third addition of acetate, the electroactive biofilm colonizing the current generation. After the third addition of acetate, the electroactive biofilm colonizing the modified modified anodes reached maximum current densities of 24.5 A/m² and 27.9 A/m² for zeolite and 2 2 anodes reached maximum current densities of 24.5 A/m and 27.9 A/m for zeolite and bentonite, bentonite, respectively. In contrast, for unmodified carbon felt, the initial lag time before any current respectively. In contrast, for unmodified carbon felt, the initial lag time before any current increase increase was detected was very long. The oxidation current began to increase after 5 days. The highest was detected was very long. The oxidation current began to increase after 5 days. The highest current current density, of 16.9 A/m², was also reached after the third addition of acetate. In sum, coating the density, of 16.9 A/m , was also reached after the third addition of acetate. In sum, coating the carbon carbon felt with clay minerals changed its bioelectrochemical behavior. The start-up time of the felt with clay minerals changed its bioelectrochemical behavior. The start-up time of the current current generation using a hydrophilic surface (LTA zeolite and bentonite) was shorter than that generation using a hydrophilic surface (LTA zeolite and bentonite) was shorter than that required by a required by a hydrophobic surface (unmodified carbon felt). Several groups have reported that hydrophobic surface (unmodified carbon felt). Several groups have reported that microorganisms adhere dierently to materials with dierent hydrophobicity, and it is easier for bacteria to adhere to Appl. Sci. 2018, 8, x FOR PEER REVIEW 6 of 11 Appl. Sci. 2019, 9, 2259 6 of 11 microorganisms adhere differently to materials with different hydrophobicity, and it is easier for hydrophilic materials than hydrophobic ones, therefore, hydrophilic materials should be applied as bacteria to adhere to hydrophilic materials than hydrophobic ones, therefore, hydrophilic materials anodes in MFC systems to shorten the start-up time [16,17]. should be applied as anodes in MFC systems to shorten the start-up time [16,17]. Figure 3. Evolution of the current density on raw carbon felt and modified carbon felt electrodes Figure 3. Evolution of the current density on raw carbon felt and modified carbon felt electrodes polarized at −0.2 V vs. SCE in tannery wastewater and 20mM of acetate inoculated with acclimated polarized at 0.2 V vs. SCE in tannery wastewater and 20 mM of acetate inoculated with acclimated activated sludge. The inset gives a closer look at the first six days of the experiments. activated sludge. The inset gives a closer look at the first six days of the experiments. Cyclic Voltammetry 3.2.2.2. Cyclic Voltammetry Applying cyclic voltammetry at dierent phases of the formation of a bioanode and the metabolic Applying cyclic voltammetry at different phases of the formation of a bioanode and the activity of electroactive biofilm can provide important information on the mechanism of anodic electron metabolic activity of electroactive biofilm can provide important information on the mechanism of transfer. Figure 4 shows the low scan rate cyclic voltammograms (CVs) recorded at the beginning of the anodic electron transfer. Figure 4 shows the low scan rate cyclic voltammograms (CVs) recorded at experiment (Figure 4A) and when the current density was at its maximum (Figure 4B) for unmodified the beginning of the experiment (Figure 4A) and when the current density was at its maximum and modified electrodes. When the maximum current density was reached, the rate of electron transfer (Figure 4B) for unmodified and modified electrodes. When the maximum current density was rose rapidly at a potential higher than 0.450 V/SCE. reached, the rate of electron transfer rose rapidly at a potential higher than −0.450 V/SCE. The kinetic behavior of the bioelectrochemical oxidation reaction is clearly dierent between The kinetic behavior of the bioelectrochemical oxidation reaction is clearly different between 0.450 and 0.200 V vs. SCE, on the one hand, and 0.200 and +0.200 V vs. SCE, on the other hand. −0.450 and −0.200 V vs.SCE, on the one hand, and −0.200 and +0.200 V vs.SCE, on the other hand. Between 0.200 and +0.200 V vs. SCE, the kinetics of oxidation slowed down (weaker slope J/E) for Between −0.200 and +0.200 V vs.SCE, the kinetics of oxidation slowed down (weaker slope J/E) for bioanodes formed on unmodified and zeolite-modified carbon felt. This slowing down was not as bioanodes formed on unmodified and zeolite-modified carbon felt. This slowing down was not as remarkable in the case of the bioanode formed from the bentonite-modified carbon felt, probably remarkable in the case of the bioanode formed from the bentonite-modified carbon felt, probably because the quantity of bacterial cells ensuring the oxidation activity was greater on this electrode because the quantity of bacterial cells ensuring the oxidation activity was greater on this electrode (more biofilm on the electrode where the mineral clay deposit is the highest).Above all, the CV curves (more biofilm on the electrode where the mineral clay deposit is the highest).Above all, the CV curves 2 2 showed that LTA zeolite and bentonite-modified carbon felt could provide at least 50 A/m and 35 A/m , showed that LTA zeolite and bentonite-modified carbon felt could provide at least 50 A/m² and respectively, at a potential of +0.200 V vs. SCE (Figure 4). 35 A/m², respectively, at a potential of +0.200 V vs. SCE (Figure 4). Appl. Sci. 2019, 9, 2259 7 of 11 Appl. Sci. 2018, 8, x FOR PEER REVIEW 7 of 11 Figure 4. Cyclic voltammetries recorded on untreated carbon felt and modified carbon felt electrodes Figure 4. Cyclic voltammetries recorded on untreated carbon felt and modified carbon felt electrodes in in tannery wastewater and 20mM of acetate inoculated with acclimated activated sludge. (A) At the tannery wastewater and 20 mM of acetate inoculated with acclimated activated sludge. (A) At the beginning beginning of the experiment and (B) at the maximum current density measured during the of the experiment and (B) at the maximum current density measured during the chronoamperometry. chronoamperometry. 3.3. Biofilm Colonization 3.3. Biofilm Colonization In order to correlate the maximum current generation obtained with biofilm formation inside the por In order to osity of carbon correlate the felt-based maximum electrodes, current gener epifluorescence ation obt micr ained oscopy with biof was ilm used format in conjunction ion inside with ESEM imaging to explore the microbial development on and inside the porous carbon felt. the porosity of carbon felt-based electrodes, epifluorescence microscopy was used in conjunction Each with ESE of the M i bianodes maging to formed explore t byhchr e mic onoamper robial deve ometry lopment on modified on and ins and ide t unmodified he porous ccarbon arbon felt felt . Eac was h cross-sectioned so that the external and the internal distribution of the microbial colonization could be of the bianodes formed by chronoamperometry on modified and unmodified carbon felt was cross- imaged. sectioned The so images that the externa of the LTA l azeolite nd the interna and bentonite-modified l distribution of the microbial co anodes showed an lonization co extensive biofilm uld be covering the complete electrode surface, which was much thicker than the one obtained on unmodified imaged. The images of the LTA zeolite and bentonite-modified anodes showed an extensive biofilm carbon covering felt the complete e (Figure 5). lectrode surface, which was much thicker than the one obtained on ESEM imaging of the unmodified electrode presented an open structure with space between colonized unmodified carbon felt (Figure 5). fibersESEM , whileimaging of the un the modified onesmodified e had a verylec tig trode pres ht networented an open structure with k of interwoven threads. An a space betwe lmost unifore m n biofilm was observable on bentonite-modified carbon felt (Figure 5C), while the LTA zeolite-modified colonized fibers, while the modified ones had a very tight network of interwoven threads. An almost uniform biofilm was observable on bentonite-modified carbon felt (Figure 5C), while the LTA zeolite- modified carbon felt surface was only partly clogged (Figure 5B). The images acquired in Appl. Sci. 2019, 9, 2259 8 of 11 Appl. Sci. 2018, 8, x FOR PEER REVIEW 8 of 11 Appl. Sci. 2018, 8, x FOR PEER REVIEW 8 of 11 carbon felt surface was only partly clogged (Figure 5B). The images acquired in epifluorescence microscopy epifluorescence microscopy confirmed that the colonization was denser on the modified electrodes confirmed that the colonization was denser on the modified electrodes (Figure 5). (Figure 5). epifluorescence microscopy confirmed that the colonization was denser on the modified electrodes (Figure 5). Figure 5. ESEM and epifluorescence microscopy images of bioanodes formed on unmodified carbon Figure 5. ESEM and epifluorescence microscopy images of bioanodes formed on unmodified carbon felt electrodes (A and D), LTA zeolite-modified electrode (B and E) and bentonite-modified electrode Figure 5. ESEM and epifluorescence microscopy images of bioanodes formed on unmodified carbon felt electrodes (A,D), LTA zeolite-modified electrode (B,E) and bentonite-modified electrode (C,F) (C and F) polarized at −0.2V/ECS for 45 days in tannery wastewater supplemented with 20 mM of felt electrodes (A and D), LTA zeolite-modified electrode (B and E) and bentonite-modified electrode polarized at 0.2 V/ECS for 45 days in tannery wastewater supplemented with 20 mM of acetate and acetate and inoculated with acclimated activated sludge. (C and F) polarized at −0.2V/ECS for 45 days in tannery wastewater supplemented with 20 mM of inoculated with acclimated activated sludge. acetate and inoculated with acclimated activated sludge. It should be noted that the electrode cross section (Figure 6) shows that the modification of It should be noted that the electrode cross section (Figure 6) shows that the modification of carbon carbon felt allowed a large cross-sectional area for the electroactive biofilm to penetrate into the 3D It should be noted that the electrode cross section (Figure 6) shows that the modification of felt allowed a large cross-sectional area for the electroactive biofilm to penetrate into the 3D structure structure and exploit the internal surface area of the electrode, while unmodified ones are not carbon felt allowed a large cross-sectional area for the electroactive biofilm to penetrate into the 3D and exploit the internal surface area of the electrode, while unmodified ones are not colonized at all. colonized at all. In contrast, Blanchet et al. attributed the weak biofilm penetration into the 3D porous structure and exploit the internal surface area of the electrode, while unmodified ones are not In contrast, Blanchet et al. attributed the weak biofilm penetration into the 3D porous electrode to the electrode to the formation of a surface biofilm that clogged the porosity of the felt [18]. These findings colonized at all. In contrast, Blanchet et al. attributed the weak biofilm penetration into the 3D porous formation of a surface biofilm that clogged the porosity of the felt [18]. These findings contradict our contradict our results because, even when the surface was not totally colonized, biofilm was unable electrode to the formation of a surface biofilm that clogged the porosity of the felt [18]. These findings results because, even when the surface was not totally colonized, biofilm was unable to penetrate into to penetrate into the electrode, which could be explained by the superhydrophobic nature of the contradict our results because, even when the surface was not totally colonized, biofilm was unable the electrode, which could be explained by the superhydrophobic nature of the carbon felt. However, carbon felt. However, the superhydrophilic nature of the modified electrode allowed the medium to to penetrate into the electrode, which could be explained by the superhydrophobic nature of the the superhydrophilic nature of the modified electrode allowed the medium to penetrate into the penetrate into the electrodes, thus making it possible for biofilm colonize the 3D carbon felt. carbon felt. However, the superhydrophilic nature of the modified electrode allowed the medium to electrodes, thus making it possible for biofilm colonize the 3D carbon felt. penetrate into the electrodes, thus making it possible for biofilm colonize the 3D carbon felt. Figure 6. Epifluorescence microscopy images of cross sectioned anodes formed on carbon felt (A), LTA zeolite-modified anodes (B), and bentonite-modified anodes (C). Figure Figure 6. 6. Epifluor Epifluorescence m escence micr icroscopy oscopy im images ages of cro of cross ss sectioned sectioned anode anodess f formed ormed on carbon felt ( on carbon felt (A A ), ),L TA LTA zeolite-modified anodes (B), and bentonite-modified anodes (C). zeolite-modified anodes (B), and bentonite-modified anodes (C). 3.4. COD, Chromium Removal, and Coulombic Efficiency 3.4. COD, Chromium Removal, and Coulombic Efficiency Appl. Sci. 2019, 9, 2259 9 of 11 3.4. COD, Chromium Removal, and Coulombic Eciency 3.4.1. COD Removal and Coulombic Eciency It was observed that the LTA zeolite and bentonite-catalyzed electrode performances were better in terms of COD removal and CE as compared to the unmodified carbon felt. Table 1 shows the COD reduction and CE for batch runs for unmodified carbon felt, LTA zeolite, and bentonite-modified anodes. The COD removal for bentonite and LTA zeolite-modified carbon felt (96.3 2.1 % and 93.8 1.7%, respectively) was significantly higher (p < 0.001) than that obtained with the unmodified carbon felt (78.7 1.3). CEs increased significantly (p < 0.001) when the modified anodes were employed. The CE was 29.4 1.5%with the bentonite-modified anode, 21.2 2.1% with the LTA zeolite-modified anode, and 14.4 1.9% with the unmodified carbon felt, even though the same tannery wastewater was used. The relatively higher CE obtained with the modified anodes might be explained by a greater amount of electro-oxidative bacteria with the ability to oxidize more organic substrates (COD) and transfer more electrons. Table 1. COD removal rate and COD removal rate constant, chromium removal rate, and coulombic eciency (CE) obtained with unmodified and modified carbon felt bioanodes. COD Removal (%) Cr Removal (%) CE (%) Carbon felt 78.7 1.3 72.4 3.1 14.4 1.9 LTA zolite-modified anode 93.8 1.7 94.6 3.6 21.2 2.1 Bentonite-modified anode 96.3 2.1 97.5 2.2 29.4 1.5 3.4.2. Chromium Removal Student t-tests underlined that for each anode the dierences in the chromium removal rate were significant (p < 0.001). High chromium removal values (94.6 3.6% and 97.5 2.2%) were found using LTA zeolite and bentonite, respectively (Table 1). Meanwhile, a lower chromium removal value was found using the unmodified carbon felt (72.4 3.1%). These findings could be explained by the adsorption properties of zeolite and bentonite [19,20]. Also, the microorganisms adhering to LTA zeolite and bentonite were proven to be highly ecient in biological heavy metal removal from wastewater, especially of chromium [21,22]. There are several mechanisms that might contribute to chromium removal in the BESs. The chromium removal in the unmodified carbon felt with acclimated activated sludge suggests that biosorption is an important mechanism for the heavy metals. The components participating in biosorption are principally the functional groups (carboxylate, hydroxyl, phosphate, amine, and sulfate) of polysaccharides, proteins, and lipids on the microbial cell walls [23]. Metal precipitation due to the presence of bicarbonate anions in the solution may also contribute to the metal removal in this study, since bicarbonate is created as a byproduct of acetate oxidation at the bioanode. The non-inoculated reactors with activated sludge showed electrodeposition of low concentrations of chromium on the surface of the carbon felt anode, which means that chromium reduction was implicated in the chromium removal process. Besides the mechanisms described above, the LTA zeolite and bentonite particles adsorbed chromium in modified anodes. 4. Conclusions Bioelectrochemical systems electrodes were eectively modified by LTA zeolite and bentonite. The resulting electrodes were successfully explored for tannery wastewater treatment and proved that the clay modification approach anticipated in this study is reliable and BESs can be fabricated using low-cost electrodes to maximize COD/chromium removal from real wastewater with improved electricity generation. Appl. Sci. 2019, 9, 2259 10 of 11 Supplementary Materials: The following are available online at http://www.mdpi.com/2076-3417/9/11/2259/s1, Table S1: Characteristics of unmodified and modified carbon felts; Figure S1: Variation of the current density on carbon felt electrodes polarized at 0.2 V vs. SCE in tannery wastewater and 20 mM of acetate inoculated with acclimated activated sludge (dotted line) or non-acclimated activated sludge (solid gray line). Author Contributions: All authors contributed conception of the manuscript. A.E. and R.E.k. wrote the first draft of the manuscript. All authors contributed to manuscript revision, read and approved the submitted version. A.E., B.E., S.E. and R.E.k. contributed to conception and editing of the manuscript, and final approval of the version to be published. Funding: This work was done as part of the Volubilis project. We are grateful to the organizations responsible for managing this project. 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