Hathaichanok
Seelajaroen
*a,
Sabine
Spiess
*bc,
Marianne
Haberbauer
bc,
Melissa Maki
Hassel
c,
Abdalaziz
Aljabour
a,
Sophie
Thallner
bc,
Georg M.
Guebitz
cd and
Niyazi Serdar
Sariciftci
a
aLinz Institute for Organic Solar Cells (LIOS), Institute of Physical Chemistry, Johannes Kepler University Linz, Altenberger Strasse 69, 4040 Linz, Austria. E-mail: hathaichanok.seelajaroen@jku.at
bK1-MET GmbH, Stahlstrasse 14, 4020 Linz, Austria. E-mail: sabine.spiess@k1-met.com
cacib GmbH (Austrian Centre of Industrial Biotechnology), Krenngasse 37/2, 8010 Graz, Austria
dDepartment of Agrobiotechnology, Institute of Environmental Biotechnology, University of Natural Resources and Life Sciences Vienna, Konrad-Lorenz-Strasse 20, 3430 Tulln an der Donau, Austria
First published on 28th May 2020
Microbial electrolysis cells (MECs) consisting of a bioanode and biocathode offer a promising solution for wastewater treatment. These systems can degrade organic substances at the bioanode while converting carbon dioxide (CO2), a major greenhouse gas, to a value-added fuel, methane (CH4) at the biocathode. The bioelectrodes were inoculated with a mixed culture under anaerobic conditions. By applying a constant potential of 0.40 V vs. Ag/AgCl (3 M NaCl), the long-term performance of MECs has been studied by monitoring the removal of chemical oxygen demand (COD) in the anolyte which contained synthetic wastewater and CH4 generation in the cathode chamber. To investigate the effect of electrode modification, poly(neutral red) and chitosan modified carbon felt electrodes were prepared, and applied in MECs. The results revealed that MECs with modified electrodes showed remarkably enhanced overall performance. The average COD removal efficiency, faradaic efficiency towards CO2 reduction to CH4 and CH4 production yield of modified MECs were up to 67%, 55% and 0.14 LCH4/gCOD, respectively.
Bioanodes have been investigated for their capabilities of oxidizing organic matter, like glucose,25 acetate26 and more complex substrates like landfill leachate27 and wastewater from various sources.6 Such oxidation generates electrons, which are transferred to the anode. For example, 24 electrons could be harvested from the oxidation of glucose, as shown in eqn (1) (E0′ = −0.41 V vs. standard hydrogen electrode (SHE)).28 A system, which contains a bioanode and an abiotic cathode, is called a microbial fuel cell (MFC).4 This technology is considered as a promising wastewater treatment system due to its capability of organic oxidation concomitant with energy harvesting directly in electricity form.6
C6H12O6 + 6H2O → 6CO2 + 24H+ + 24e− | (1) |
In conventional MFCs, protons are generated from the oxidation of organic matters and coupled with oxygen, an electron acceptor, generating water at the cathode. To improve the efficiency of the system, introduction of prompted catalysts (like platinum) for useful chemical generation in the cathode chamber has been investigated.29 Instead of using expensive materials, microbial biocathodes are an alternative potential option.17,30–33 The direct electron uptake from the cathode through microbes has been adopted for several applications, for example, treatment of heavy-metals (bioremediation),34 reduction of nitrate (denitrification)35 and reduction of CO2 to value-added fuels such as formate11 and CH4 (eqn (2), E0′ = −0.24 V vs. SHE).2 Such BESs, where energy is invested to enhance reaction kinetics or overcome thermodynamic energy barriers, are called microbial electrolysis cells (MECs).5 The electrochemical CO2 reduction to CH4 usually suffers from large overpotential (for example, an overpotential of 1.22 V from using Cu electrodes36). Our group has shown the utilization of such microbial cathodes in a MEC for CO2 reduction to CH4 with a relatively low overpotential of 0.25 V37 and it has been reported that CH4 production was observed in a broad range of production rates.38 The combination of a bioanode and a biocathode now shall accomplish two tasks simultaneously and utilize the advantages of introducing microorganisms to both electrodes.39–42 The coupling of CO2 reduction with the aforementioned microbial oxidation of organic substances is, in principle, feasible by using electrons, protons and CO2 which are generated during oxidation on the bioanode.42 The required voltage of such systems could theoretically be eliminated due to a positive electrochemical cell voltage for CH4 production with glucose oxidation (Ecell = 0.17 V).
CO2 + 8H+ + 8e− → CH4 + 2H2O | (2) |
A schematic of an MEC system where a bioanode and a biocathode are combined, is demonstrated in Fig. 1a. Such systems have been investigated for various applications e.g. oxygen reduction to hydrogen peroxide,30 denitrification35 and CO2 reduction to CH4.42,43 The MEC approach for CH4 production offers several advantages, for example the tunability of the degradation/generation rate.41 Therefore, the MEC could be an effective addition to the existing anaerobic digestion systems by improving biogas quality.5,44,45 The performance of BESs largely depends on the quality of electroactive biofilms on electrodes and also on the electron transfer process.46,47 Therefore, several attempts have been made to investigate the effects of different electrode materials and modifications.48 Various electrodes including carbon-based materials (e.g. graphite, carbon felt, carbon cloth and carbon mesh) and other inert materials (e.g. stainless steel) are commonly used in BESs.14,29,46 Further, the surfaces of these materials were modified, aiming to improve microbial growth and electron transfer processes. One example is the modification of carbon-based electrodes with positively charged materials like ammonia,49 chitosan,50 or conductive polymers, for example, polyaniline51 and polypyrrole.52 Chitosan is a bio-polymer and a derivative of chitin, a component of arthropod exoskeletons. It has been applied in many applications due to its low cost, biocompatibility, non-toxicity and high chemical and thermal stability.53 These modifications resulted in improved bacterial colonization and enhanced electron transfer, which further improved the overall performance of BESs.54,55 Another interesting material is poly(neutral red). It is a conductive polymer which could be prepared electrochemically in a slightly acidic to neutral pH solution56 and its monomer, neutral red, is a staining dye which was used in various bio-electrochemical systems as a redox mediator to facilitate electron transfer between the microbe and electrode.57–59 Recently, we reported on the contribution of poly(neutral red) modified carbon felt cathodes, for the enhancement of microbial electrochemical reduction of CO2 to formate by Methylobacterium extorquens. The study showed an improvement in electron transfer processes leading to higher formate production rates, as compared to non-treated electrodes.60 However, to the best of our knowledge, each of the chitosan and poly(neutral red) electrode modifications has not been investigated for the anode and cathode at the same time in a MEC. Therefore, this idea has attracted our interest in order to investigate the effect of modified electrodes not only on one redox reaction but also on both redox processes simultaneously.
In this study, we report a full assembly of an MEC (Fig. 1b), equipped with bioelectrodes, for two applications: wastewater treatment at the bioanode and CO2 reduction to CH4 at the biocathode. The long-term performance of the methane-producing MEC for synthetic wastewater treatment was monitored. The system was evolved by using bioelectrodes (bioanode and biocathode) inoculated with the same mixed culture microorganisms. The experiments were performed at a controlled anode potential of 0.40 V vs. Ag/AgCl (3 M NaCl) and the oxidation of synthetic wastewater was observed by monitoring the change of the anolyte chemical oxygen demand (COD) value, which reflected directly the efficiency of wastewater treatment. Moreover, electromethanogenesis at the biocathode was tracked by CH4 generation in the headspace. Furthermore, carbon felt electrodes were modified with chitosan and poly(neutral red), serving as supports for microorganisms for both the cathode and anode. These two materials were chosen due to the previously reported results, low material costs, good biocompatibility and facile synthesis.52,55 The performance of all three MECs namely MEC 1 (equipped with non-modified carbon felt electrodes), MEC 2 (equipped with poly(neutral red) modified carbon felt electrodes) and MEC 3 (equipped with chitosan modified carbon felt electrodes) were compared, reflecting the effect of electrode modifications.
Scheme 1 Schematic preparation of chitosan modified carbon felt. EDC: N-hydroxy-3-(3-dimethylaminopropyl)-N′-ethylcarbodiimide; NHS: N-hydroxysuccinimide. |
To investigate the long-term performance of MECs, three MECs namely MEC 1, 2 and 3 were built. In MEC 1, non-modified carbon felts were used as the anode and cathode, while MEC 2 and 3 were equipped with poly(neutral red) and chitosan modified electrodes, respectively.
All bioelectrodes in each MEC were inoculated with a mixed culture taken from sewage sludge in a two-compartment electrochemical cell with a controlled potential of 0.40 V vs. Ag/AgCl (3 M NaCl). During the adaptation phase, the bioanode was fed once a week with synthetic wastewater consisting of organic substances like glucose and acetate, while the biocathode was fed with glucose and CO2 to ensure enough biomass formation. After a 4 week adaptation, the faradaic currents were observed at around 2 mA, indicating successfully developed bioelectrodes.61
After the adaptation period, the cathodic solution was replaced with a glucose-free medium. All three developed MECs showed capabilities of organic oxidation in the anodic compartment and simultaneous CH4 generation in the cathodic compartment. To investigate the systems' performance, long-term electrolyses of MEC 1, 2 and 3 were carried out, by applying a constant potential of 0.40 V vs. Ag/AgCl (3 M NaCl) at the anode in a batch operation mode. During the operation of around 90 days, half of the anodic solution was replaced twice a week with a freshly prepared medium, consisting of synthetic wastewater with an average COD concentration of 600 mg L−1, while cathodic chambers were purged with CO2 two times a week. The systems were monitored for 3 running cycles, through analysis of organic degradation by COD determination of anodic solutions and headspace analysis of CH4 production in cathodic chambers.
The accumulated COD removal in each running cycle (red circle data point) was plotted together with total electrical charge (Q) (blue triangle data point) over the entire running time, as shown in Fig. 2a–c for MEC 1, 2 and 3, respectively. The data were fitted linearly as presented in dashed lines, showing reaction rates in each cycle. The total COD removal, COD removal rate, average COD removal efficiency, total Q and Q rate are summarized in Table 1.
MEC 1 | MEC 2 | MEC 3 | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
1 | 2 | 3 | Average ± SD | 1 | 2 | 3 | Average ± SD | 1 | 2 | 3 | Average ± SD | |
CH4 production/mmol | 0.8 | 1.3 | 1.8 | 1.3 ± 0.5 | 2.6 | 2.7 | 2.2 | 2.5 ± 0.3 | 2.8 | 3.3 | 2.0 | 2.7 ± 0.7 |
Q/103 C | 2.0 | 3.4 | 3.7 | 3.0 ± 0.9 | 3.3 | 4.5 | 4.2 | 4.0 ± 0.6 | 3.8 | 3.5 | 4.2 | 3.8 ± 0.4 |
COD removal/g L−1 | 1.0 | 1.8 | 2.2 | 1.7 ± 0.6 | 1.6 | 2.6 | 2.5 | 2.2 ± 0.6 | 1.9 | 2.4 | 2.3 | 2.2 ± 0.3 |
CH4 production rate/μmol per day | 25 | 40 | 60 | 42 ± 18 | 90 | 80 | 70 | 80 ± 10 | 90 | 110 | 60 | 87 ± 25 |
Q rate/C per day | 60 | 110 | 130 | 100 ± 36 | 110 | 150 | 140 | 133 ± 21 | 130 | 110 | 140 | 127 ± 15 |
COD removal rate/mg per L per day | 40 | 60 | 70 | 57 ± 15 | 55 | 85 | 80 | 73 ± 16 | 65 | 80 | 70 | 72 ± 8 |
Average% FECH4 | 39 | 29 | 38 | 35 ± 6 | 66 | 47 | 44 | 52 ± 12 | 57 | 72 | 36 | 55 ± 18 |
Average% COD removal efficiency | 25 | 52 | 55 | 44 ± 17 | 52 | 67 | 72 | 64 ± 10 | 56 | 73 | 71 | 67 ± 9 |
CH4 yield/LCH4/gCOD | 0.09 | 0.08 | 0.09 | 0.09 ± 0.01 | 0.18 | 0.12 | 0.10 | 0.13 ± 0.04 | 0.16 | 0.15 | 0.10 | 0.14 ± 0.04 |
The results revealed that accumulated COD removal in MEC 1 increased from 1.0 g L−1 in the first cycle to 1.8 and 2.2 g L−1 in the second and third cycles, respectively, showing an enhancement of the oxidation process over the running cycles. Significantly higher COD removal values were observed at 1.6 and 1.9 g L−1 in the first cycle of MEC 2 and 3. In the second cycle, the accumulated COD values found in MEC 2 and 3 were enhanced by 1.0 and 0.5 g L−1 from the first cycle, respectively, while a slight drop was detected in the third cycle. The removal rates obtained from the slope of fitting lines, were found to be in the range of 40–85 mg per L per day. The results revealed that the removal rate increased largely from 40 mg per L per day in the first cycle to 70 mg per L per day in the third cycle of MEC 1, while the highest removal rates were observed in MEC 2 and 3 with 85 and 80 mg per L per day in cycle 2, respectively. The large increase in COD removal from the first to the second cycle in all MECs might be related to biofilm growth in the first cycle. Over the whole experiment, average COD removal rates were observed at 57, 73 and 72 mg per L per day in MEC 1, 2 and 3, respectively. Additionally, average COD removal efficiencies were calculated giving the overall efficiencies of 44%, 64% and 67% in MEC 1, 2 and 3, respectively. These results reflected that enhanced organic degradation strongly related to both modifications.
Furthermore, the electrical charge plots revealed that during all three cycles, electrons were consumed continuously in all MECs. In MEC 1, accumulated charges increased from 2.0 × 103 C in the first cycle to 3.4 × 103 and 3.7 × 103 C in the second and third cycles, respectively. The accumulated charges collected in the first cycle of MEC 2 and 3 were found to be almost two times higher than that of MEC 1, suggesting an enhanced electron transfer process at the first cycle in the modified electrode containing systems. This observation might relate to better coverage of biofilms on modified carbon felts. The accumulated charges were further improved in the second cycle and dropped slightly in the third cycle of MEC 2. While those of MEC 3 were of 3.5 × 103 and 4.2 × 103 C in cycle 2 and 3, respectively. Average rates for electron flux were observed for MEC 1, 2 and 3 at 100, 133 and 127 C per day, respectively. The highest electron flux was observed in MEC 2 with 150 C per day in cycle 2, followed by MEC 3 with 140 C per day in cycle 3. Although MEC 1 showed a much lower Q rate in the first cycle relative to MEC 2 and 3, it reached the rate of around 100 C per day which is in the same range as MEC 3 in the second cycle. This observation suggested that biofilm formation on bare carbon felts took longer, as compared to treated carbon felts.
In the cathodic compartment, the CH4 production was quantified twice a week. Fig. 2d–f show the plots of accumulative CH4 concentration (black square data point) and accumulative Q (blue triangle data point) during each running cycle of MEC 1, 2 and 3. The CH4 production rate and the average faradaic efficiencies are summarized in Table 1. The produced CH4 observed in MEC 1 rose continuously from 0.8 mmol in the first cycle to 1.3 mmol in the second cycle to finally 1.8 mmol in the third cycle. In MEC 2, the amount of produced CH4 in cycles 1 and 2 was relatively stable at 2.6 and 2.7 mmol, respectively. However, the production declined to 2.2 mmol in the third cycle, while produced CH4 in MEC 3 increased from 2.8 mmol in cycle 1 to 3.3 mmol in cycle 2 and dropped significantly to 2.0 mmol in cycle 3. The decline observed in MEC 2 and 3 in the third cycle, might result from the instability of the modified electrodes and/or detachment of biofilms. The CH4 production rates in the three MECs were found to be in the range of 25–110 μmol per day and the average production rates over the entire experiments in MEC 1, 2 and 3 were 42, 80 and 87 μmol per day, respectively. Together with the obtained charges, faradaic efficiencies towards the CO2 reduction to CH4 were calculated according to the equation given in the experimental part. The corresponding faradaic efficiencies were averaged within each running cycle. MEC 1 showed efficiencies of 39% in cycle 1, 29% in cycle 2 and 38% in cycle 3, and an overall average efficiency of 35% while the highest faradaic efficiency in MEC 3 was reached at 72% in cycle 2 and then decreased to 36% in cycle 3. The overall average efficiencies of MEC 2 and 3 were reported to be 52 and 55%, respectively.
Considering CH4 production relative to the removed COD (CH4 yield), MEC 1 revealed a relatively stable CH4 yield at 0.09 LCH4/gCOD while the yield observed from MEC 2 and 3 decreased from the first cycle to the third cycle and the average yields were of 0.13 and 0.14 LCH4/gCOD, respectively.
Concerning the performance in both cathodic and anodic chambers, MEC 2 and MEC 3 showed significantly higher organic degradation efficiencies, faradaic efficiencies toward the conversion of CO2 to CH4 and CH4 yield, as compared to those of MEC 1. Moreover, higher numbers of electrons were delivered in the modified electrode containing systems. This might be due to biofilm coverage and/or facilitated electron transfer by the coating. As suggested in the previous report, a positively charged electrode modification with chitosan coating, could enhance the interaction between the electrode and Gram-negative microorganisms like Sporomusa ovata, resulting in improved microbial electrolysis rates.54 However, the instability of the modified systems for CO2 reduction to CH4 was observed during the long-term running.
Compared to the reported studies on methane-producing MECs using non-treated carbon felt electrodes (Table 2), our results (MEC 1) showed lower COD removal efficiency but significantly higher CH4 yield. While, with the electrode modifications (MEC 2 and 3), the higher efficiencies were now comparable to those of the continuous-operating MECs equipped with graphite granules and nickel mesh. Furthermore, using carbon felt offers several advantages as it is highly flexible, has high active surface area, high conductivity and is less corrosive.62 However, it is important to be noted that apart from electrode material, other parameters like cell configuration, inoculation, substrate and operation parameters are of importance.63 Therefore, this comparison was aimed to show the general view of this field and parameters which could be further optimized.
Anode material | Cathode material | Operation | Cell geometry | E app or Vapp | Substrate | %COD removal | %FECH4 | CH4 yield/LCH4/gCOD | Ref. |
---|---|---|---|---|---|---|---|---|---|
a Calculated from the given data; Eapp: applied potential; Vapp: applied voltage; NG: not given, max: maximum value. | |||||||||
Graphite granules | Graphite granules | Continuous | Two chamber | +0.2 V vs. SHE | Synthetic organic mixture | 75 ± 10% | 61 ± 5% | 0.25a | 65 |
Graphite granules | Graphite granules | Continuous | Two chamber | +0.2 V vs. SHE | Synthetic organic mixture | 70 ± 2% | 47 ± 2% | 0.17a | 43 |
Graphite granules | Nickel mesh | Continuous | Upflow | 0.8 V | Beer wastewater | 90% (max) | NG | 0.14 | 66 |
Graphite granules | Graphite granules | Continuous | Two chamber | +0.2 V vs. SHE | Acetate | 94% | 79 ± 2% | ∼0.25a | 67 |
Carbon felt | Carbon felt | Continuous | Two chamber | 0.8 V | Synthetic wastewater | ∼80% | NG | 0.04a | 68 |
Carbon felt | Carbon felt | Batch | Two chamber | +0.4 V vs. Ag/AgCl | Synthetic wastewater | 44 ± 17% | 35 ± 5.5% | 0.09 | This work |
Poly(neutral red) modified carbon felt | Poly(neutral red) modified carbon felt | Batch | Two chamber | +0.4 V vs. Ag/AgCl | Synthetic wastewater | 64 ± 10% | 52 ± 11.9% | 0.13 | This work |
Chitosan modified carbon felt | Chitosan modified carbon felt | Batch | Two chamber | +0.4 V vs. Ag/AgCl | Synthetic wastewater | 67 ± 9% | 55 ± 18.1% | 0.14 | This work |
After the long-term operation of around 90 days, samples of bioanodes and biocathodes of all MECs were dried under ambient conditions overnight for SEM measurements. Fig. 3 presents SEM images of bioanodes and biocathodes of MEC 1, 2 and 3. The bioanodes obtained from modified carbon felt electrodes showed better coverage and thicker biofilms (Fig. 3b and c). High magnification images (Fig. 3d–f), from both modified and non-modified carbon felt electrodes are colonized from different cell shape bacteria, revealing mixed microbial strains. In the SEM images of all biocathodes, rod-shaped cells of bacteria were found to be located on carbon fibers (Fig. 3j–l). This characteristic shape refers to some species from phylum Firmicutes like S. ovata64 and the Euryarchaeota Methanobacterium palustre,2 which are capable of growing autotrophically by using a cathode as the sole electron donor and CO2 as the carbon source.
Fig. 3 SEM images of bioanodes of MEC 1 (a and d), MEC 2 (b and e) and MEC 3 (c and f) and biocathodes of MEC 1 (g and j), MEC 2 (h and k) and MEC 3 (i and l). |
The utilization of electrochemical impedance spectroscopy (EIS) in BESs is highly significant since extensive information of the systems can be extracted, such as the charge transfer resistances and the mechanism of the electron transfer, among many others. In this present study, the electrical loss in the system was evaluated.
All impedance spectra were recorded in the frequency range of 10−1 to 105 Hz with a perturbation amplitude of 50 mV. Firstly, the resistance of the medium as an electrolyte solution (Rsol) was determined in a one-compartment cell, having platinum electrodes as the working (WE) and counter (CE) electrodes, showing 8.9 Ω. The platinum electrodes were then transferred to a two-compartment electrochemical cell containing a medium to determine the resistance of a Nafion membrane (RNF). The electrical circuit used for data fitting is shown in Fig. 4. In this configuration, RNF was found to be 530 Ω and connected in series with Rsol, the resistance of carbon felt (RCF) and the resistance of biofilm (Rbiofilm). RCF is in parallel with the constant phase element of carbon felt (CPECF) and Rbiofilm is in parallel with the capacitance of the biofilm (Cbiofilm), representing the bioanode.
Then, the platinum electrodes were replaced with bare carbon felt electrodes and the impedance spectrum was measured in a similar manner. After that, these carbon felt electrodes were used as electrodes for biofilm formation in MEC 1. With these two bioelectrodes, impedance spectra were recorded to investigate changes of the system in the presence of biofilms. Fig. 5 presents Bode plots for the two-electrode setup of platinum, bare carbon felt and carbon felt with the biofilm, and the data evaluated from the measurements are summarized in Table 3.
WE | CE | R sol/Ω | R CF/Pt/kΩ | R NF/Ω | R biofilm/kΩ | C biofilm/F | CPE-T (10−4) | CPE-E |
---|---|---|---|---|---|---|---|---|
Platinum | Platinum | 8.9 | 8.7 | 530 | — | — | 6.6 | 1.1 |
Carbon felt | Carbon felt | 70 | 1.1 | 530 | — | — | 2.5 | 1.1 |
Carbon felt with biofilm | Carbon felt with biofilm | 8 | 0.4 | 530 | 0.4 | 0.1 | 1.6 | 0.7 |
The constant phase element was used for the description of the non-ideal capacity of spongy-like carbon felt electrodes. Thus, the resistances of electrodes (RCF) as bare carbon felt and carbon felt with a biofilm were found to be 1.1 and 0.4 kΩ, respectively. The calculated resistance and capacitance of the biofilm (Rbiofilm, Cbiofilm) were 0.4 kΩ and 0.1 F. Further, the results reveal that, with the biofilm on electrodes, a decrease in capacitive current was observed in a low frequency regime due to enhanced electron transport, indicating the establishment of a conductive biofilm and a larger surface area due to biofilm formation.61 Moreover, EIS results indicated negligible losses of this MEC.
Apart from the observed enhanced performance of the modified electrodes containing MECs, the economic aspects should be addressed as they impact significantly on up-scaling. However, only a few studies have been reported on the cost of electrode modification for this type of MEC. We performed cost studies for such modifications from the price of chemicals which were used in each modification process (see details in the ESI†). The calculation showed that poly(neutral red) modification (∼100 € per m2) was much cheaper, as compared to chitosan modification (∼5400 € per m2) due to the costly coupling reagents (NHS and EDC). Compared to the reported metal based electrodes like Ni mesh66 (∼8600 € per m2), carbon felt (∼170 € per m2) modified with poly(neutral red) (in total ∼270 € per m2) are much cheaper and showed similar results with respect to the CH4 yield (Table 2). Moreover, this poly(neutral red) modified carbon felt is more cost effective than the conventional platinum based electrodes (e.g. Pt (60%) carbon cloth is ∼4100 € per m2,62) which are normally used and, being the main cost of MFC technology made it less feasible for up-scaling reactors.
Footnote |
† Electronic supplementary information (ESI) available. See DOI: 10.1039/d0se00770f |
This journal is © The Royal Society of Chemistry 2020 |