1. Introduction
Integrating anaerobic digestion (AD) with microbial electrolysis is considered to be an effective way to increase biogas production from waste activated sludge (WAS) [1,2,3]. Microbial electrolysis is an emerging process that can utilize the principle of electron transfer to produce methane [4,5]. The advantages of introducing microbial electrolysis in AD include, but are not limited to, a faster fermentation process, better adaptability to adverse environmental conditions, and high-quality biogas [6,7]. WAS, as a waste biomass rich in organic matter, is difficult to convert into energy because most of the organic matter exists inside the cells and is difficult to release [8,9,10]. At present, various pretreatment (physical, chemical and biological) methods are used to accelerate sludge disruption and organic matter hydrolysis, but the rate of methane production is still limited, and some pretreatment methods may also inhibit the methanogenesis process [11,12]. Among various pretreatment methods, alkaline and thermal pretreatment have been studied the most, which can effectively increase the dissolution of sludge organic matter, inhibit pathogens, and increase the methane content by 14–80% [13,14]. Studies have shown that the combination of sludge pretreatment and bioelectrolysis can further promote the hydrolysis of WAS while promoting the generation of methane [1,15].
Combining microbial electrolysis with anaerobic digestion can be easily achieved by inserting two electrodes in an anaerobic system and applying a small voltage of 0.3–1.1 V [7]. Under the influence of voltage, the cathode and anode can directionally enrich some slow-growing bacteria with electrochemically active and unique methanogenesis pathways [16]. Fermentation/acid-producing bacteria on the anode can accelerate the degradation of organic matter and transfer the generated electrons through the circuit to the cathode. The electrons are finally reduced to hydrogen at the cathode and converted into methane by cathodic hydrogenotrophic methanogens (4H2 + CO2 → CH4 + 2H2O or 8e− + CO2 + 8H+ → CH4 + 2H2O) [17]. Additionally, the conductive characteristic of the anode (carbon brush) could provide an environment for direct interspecies electron transfer between methanogens and electrochemically active microorganisms [18]. The favorable methanogenesis environment created by the microbial electrolysis system is considered to be the key reason for the enhanced methanogenesis rate [19,20].
Recently, many studies have reported the effect of different parameters (pretreatment conditions, voltage, electrode material, and electrode size) on the methanogenesis process of this coupled system [7,21,22,23,24,25]. However, no in-depth study of sludge concentration has been conducted. The sludge concentration is related not only to the content of organic matter in the sludge, but also to the content of suspended microorganisms. As the electrode size is determined, the sludge concentration is also related to the ratio of suspended microorganisms and electrode microorganisms, which in turn affects the contribution rate of bioelectrolysis reactions in the system. This effect is usually multiple and is related to limited substance competition, biomass distribution, and conductivity (dissolved conductive species content), which affects the electrochemical behavior of microbial electrolysis. Sludge concentration, which also acts as the organic load in this system, has always been the focus of attention in AD technology [26,27]. A high organic load may lead to excessive acidification and inhibit the methanogenesis process, so it is worthwhile controlling the organic load reasonably to obtain the optimal treatment efficiency [28].
Previous studies have shown that alkaline treatment could effectively improve the efficiency of sludge hydrolysis and acidification and had a synergistic effect with microbial electrolysis [29,30]. If the two processes are combined, the highest benefit could be achieved. Therefore, in this experiment, the effect of different organic loads controlled by the sludge concentration on the electrochemical performance of the microbial electrolysis system, substrate metabolism, and methanogenic rate of the integrated system were investigated. The electrochemical contribution and energy efficiency affected by different organic matter concentrations were evaluated as well as the optimized organic loading for the highest specific methane production and organic matter removal. The methanogenesis process under a high organic load of the integrated system and its contribution to relieving excessive acidification inhibition were analyzed. Overall, the results provide fundamental insights into the maximized energy yield and treatment effect on this integrated system.
2. Materials and Methods
2.1. The Storage and Pretreatment of WAS
Raw WAS was collected from a municipal wastewater treatment plant in Harbin, China. After filtration and concentration, the volatile suspended solid (VSS) content of the sludge was controlled at 14 g/L. The basic properties of WAS were as follows: total suspended solids (TSS) of 23 g/L, total chemical oxygen demand (TCOD) of 10.8 g/L, and pH of 6.92. Before anaerobic digestion, the WAS was pretreated with solid NaOH at a dosage ratio of 0.16 g/g VSS and placed in a shaker for 24 h. Then, the pH of the mixture was adjusted to 7.0 with 6 mol/L HCl solution and continuously fermented for 48 h in a 35 °C water bath shaker before use to ensure that the WAS was fully hydrolyzed at this stage. The VSS concentration of WAS was finally adjusted to 14 g/L, 10 g/L, 8 g/L, and 6 g/L according to the experimental needs.
2.2. Reactor Setup and Operation
Ten fully mixed anaerobic reactors (effective volume of 700 mL) assisted by bioelectrolysis were started and operated in a sequencing batch model, as in a previous study (Figure 1) [31]. Reactors were set up under a voltage of 0.8 V (set two in parallel) with different WAS concentrations of 14 g/L, 10 g/L, 8 g/L, and 6 g/L, respectively, and the other two reactors with WAS concentrations of 14 g/L were set as the controls without a voltage supply. The anode and cathode mainly used a conventional carbon brush (diameter 5 cm, length 5 cm) and stacked nickel foam (volume 1.413 cm3), and the distance between them was 2 cm. All of the reactors were first started up with 1 g/L acetate as a carbon source and then continuously fed with pretreated WAS for one month before this experiment. The voltage acquisition system (Keithley DAQ6510A, version 1.7.12) automatically monitored the current generated by the bioelectrolytic system through a 10 Ω resistor, and the anode potential was synchronously tested with a saturated calomel electrode (SCE). Reactor operation and sample testing were carried out at room temperature. Sludge and gas samples were taken every day for substance analysis, and the gas was collected using a gas collection bag.
2.3. Analysis and Calculation Method
2.3.1. Chemical Analysis Method
The TSS, VSS, and soluble chemical oxygen demand (COD) of WAS were determined using the Chinese standard methods as described in previous studies [13,32]. The main soluble substances in WAS including carbohydrates, proteins, and volatile fatty acids (VFAs), were determined by the phenol sulfate method, Lowry–Folin method, and gas chromatography analysis (Agilent, 7890A, J&W Scientific, USA), respectively [33]. The VFAs included acetate, propionate, iso- and n-butyrate, and iso- and n-valerate. The components of H2, CO2, and CH4 in biogas were determined using gas chromatography equipped with a flame ionization detector (FID) and thermal conductivity detector (TCD) [34].
2.3.2. Calculation Method
The actual methanogenic rate of WAS was calculated by fitting the first-order kinetic model of the cumulative methane curve. The theoretical electrochemical methane contribution was calculated by the formula 8e− + CO2 + 8H+ → CH4 + 2H2O according to the following equations:
Theoretical electrochemical methane (mL/d) =
∑I × t × V × 6.25 × 1018/6.02 × 1023/8(1)
where I is the current of the bioelectrolysis system; t = 24 × 3600 s is the time; V = 22.4 × 1000 mL/mol is the ideal gas volume; and 6.25 × 1018/6.02 × 1023 is the unit coefficient of Coulomb to molar.Net energy income (kJ/gVSS) = (energy output − energy input)/VSS(2)
where energy output is the calorific value of the produced methane calculated through the calorific value of CH4 of 35.88 MJ/Nm3; energy input is the electricity consumption calculated with U × I × t; U is the applied voltage of 0.8 V, and VSS is the total volatile suspended solid concentration in the reactor under different sludge concentrations.The half cycle of gas production (Gp) referred to the time required to achieve 50% of cumulative gas production.
3. Results and Discussion
3.1. Effect of Organic Matter Concentration on the Electrochemical Behaviors of the Bioelectrolysis System
To evaluate the effect of organic matter concentration on the performance of the integrated system, multiple groups of anaerobic reactors were operated with sludge digested for 3 days after alkaline pretreatment. The initial sludge concentrations were 14 g/L, 10 g/L, 8 g/L, and 6 g/L. Considering that the high concentration of organic acids generated after the digestion of solid organic matter has an inhibitory effect on methane production, anaerobic fermentation with a high concentration (14 g/L) in an open circuit was set as the control group to study the role of the electrochemical system. The results showed that during the whole digestion process, the conductive substrates dissolved from the sludge itself and the alkali input could make the electrochemical system maintain a high circuit current and a stable anode potential (Figure 2). The initial peak current of the reactor was not much different under different sludge concentrations, reaching 10 mA at 0–6 d. However, as the substrates were depleted, the organic matter that could be anodized gradually decreased, resulting in a gradual decrease in the current value. The anodic current decreased most obviously at a concentration of 6 g/L. Among the main substrates (proteins, carbohydrates and VFAs) in sludge that can be oxidized by the anode, the composition of VFAs had a great influence on the current value, among which the highest response current could be obtained by the anodic metabolism of acetate, followed by butyrate [35]. Therefore, the peak current at 14 g/L slightly increased to 12 mA, perhaps because it provided a richer substrate for anodic current formation or substrates that were more easily converted to current. The generated current could help synthesize methane through the cathodic reaction, so a high current was more conducive to promoting methane recovery. Different sludge concentrations had little effect on the anode potential, which was maintained at −450 mV, indicating that the anodes maintained high activity throughout the digestion process. During the later stages of digestion, the anode potential gradually increased due to substrate starvation. Finally, the reactor with a sludge concentration of 14 g/L obtained the highest peak current, and the average current reached 12 mA. As the sludge concentration decreased, the current value decreased slightly. Compared with previous studies, bioelectrolysis generally required a buffer solution to maintain the solution conductivity and the pH balance of the cathode and anode [36]. In this experiment, it was found that the sludge after alkali treatment had a high conductivity, which could help the bioelectrolysis system maintain good electrochemical behavior without the need for a buffer solution.
3.2. Effect of Bioelectrolysis and Organic Matter Concentration on Biogas Production
The changes in biogas production dominated by hydrogen and methane in the fermentation process were further studied. In the first three days of fermentation, hydrogen was detected in the reactors with the bioelectrolysis system, but no hydrogen was detected in the control group without the bioelectrolysis system. There were two main sources of hydrogen in the anaerobic reactor with the bioelectrolysis system: hydrogen evolution at the cathode and generation under the action of hydrogen-producing acetogenic bacteria [37]. Under the premise that the initial current value was similar, the hydrogen produced by the cathode hydrogen evolution was similar, and the hydrogen concentration (15%) in the high-concentration sludge was significantly higher than that in the low-concentration sludge (4–11%). Therefore, the hydrogen detected in the system was more likely to come from the acidogenic fermentation process. However, no hydrogen was detected in the control group, indicating that bioelectrolysis probably had a certain promoting effect on acidogenic fermentation. Further comparing the cumulative methane production under different sludge concentrations (Figure 3), it was found that the total amount of accumulated methane increased with increasing sludge concentration. The methane yield reached the highest value of 96.2 mL/gVSS at a sludge concentration of 14 g/L. However, relatively sluggish methanogenesis occurred in the control group (14 g/L). Compared with the control group, the faster and higher methane production reflected that the bioelectrolysis-assisted AD system had greater advantages in dealing with high-concentration organic loads.
In the stable stage of methanogenesis, the average methanogenic rate was calculated according to the first-order kinetic equation. The cumulative methane yield, VSS removal rate, half cycle of gas production (Gp), and methanogenic rate are shown in Table 1. The results showed that with increasing sludge concentration, the methanogenic rate and cumulative methane per VSS gradually increased from 7.9 mL/d to 47.1 mL/d and 36.6 mL/gVSS to 96.2 mL/gVSS, respectively. There were two reasons for the promotion of methanogenesis: one was the increase in substrate concentration, and the other was the increase in system biomass. The cumulative methane of the control group was significantly lower than that of the group under the same conditions, which proved the promoting effect of bioelectrolysis on methanogenesis. Furthermore, Gp increased with increasing sludge concentration, and the VSS removal rate decreased gradually. Because the sludge would partially adhere to the electrode surface, the VSS removal rate was close to 100% when the sludge concentration was 6 g/L. The VSS removal rates of 10 g/L and 8 g/L were similar, reaching 79.2% and 82.1%, respectively, while the VSS removal rate of the control group was only 56%. Hence, considering the time and economic benefits, 14 g/L was the optimal sludge concentration for both the methanogenic rate and cumulative methane yield. The half-cycle of methane production at a 14 g/L concentration was already longer than 23 days, which indicated that the sludge concentration for alkaline waste sludge fermentation should not be higher than 14 g/L.
3.3. Substrate Metabolism and Conversion
Further investigation of the changes in organic compounds under different sludge concentrations showed that with increasing sludge concentration, the major macromolecular organic compounds (carbohydrates and proteins) in the sludge increased and were gradually decomposed and transformed as the digestion process proceeded (Figure 4). The residual protein concentration was higher in the reactor with a high initial sludge concentration. The final protein removal rate of sludge with different concentrations was only approximately 50%, which proved that the residual protein might be difficult to decompose and transform. Compared with protein, the residual concentration of total dissolved carbohydrate was relatively low (<250 mg/L), indicating that most carbohydrate could be further decomposed and converted after increasing the sludge concentration, while the soluble protein was difficult to metabolize and remained at the end of digestion. The protein and carbohydrate metabolism of the control group and the experimental group with the same sludge concentration were consistent overall, which proved that although the methanogenesis process of the control group was inhibited due to the high organic matter, the protein and carbohydrate metabolism was not affected.
Analysis of the changes in soluble VFA components produced by carbohydrate and protein metabolism showed that the concentrations of all VFA components except acetic acid continued to increase during the early operation stage (0–15 d), and propionate, butyrate, and valerate continued to accumulate (Figure 5). Generally, the decrease in acetic acid concentration marked entry into the methanogenesis stage. Except for the sludge concentration of 14 g/L, the acetic acid concentration with a low sludge concentration (6–10 g/L) continued to decline and was accompanied by an increase in methane, proving the smooth progress of the methanogenesis stage. The acetic acid concentration in the experimental group with a sludge concentration of 14 g/L dropped to below 2000 mg/L, accompanied by methane production after day 8, while the acetic acid in the control continued to rise to 2900 mg/L without methane production, which proved that the methanogenesis process was completely inhibited at this sludge concentration. The results of substrate metabolism and methanogenesis showed that the resistance of this bioelectrolysis-assisted reactor to high organic matter concentrations was significantly stronger than that of traditional anaerobic reactors.
3.4. The Contribution and Energy Benefit of Bioelectrolysis to Methanogenesis
The contributions of bioelectrolysis to VFA metabolism and methane production were further investigated to evaluate their role in anaerobic digestion. The anode biofilm was mainly dominated by Geobacter, which is an electrochemically active microorganism using acetate as the electron donor [2]. According to the estimation that the anode only oxidizes acetate (CH3COO− + 2H2O → 2CO2 +8e− +7H+), the anode needs to oxidize 78.9 mg of acetate per day to maintain a current of 11 mA, which is equivalent to 112.8 mg/L acetate consumed per day (700 mL reaction system). Therefore, it was speculated that the oxidation process of acetate by the anode played a key role in alleviating the inhibition of high concentrations of organic matter in the early stage of anaerobic digestion. It was also found that the consumption of acetate could promote the decomposition and conversion of n-butyrate and n-valerate to acetate. On day 22, isobutyrate and isovalerate were almost completely consumed, and methane was produced in large quantities. Propionate accumulation is a common phenomenon in anaerobic digestion. The propionate concentration of different concentrations of sludge continued to rise throughout the digestion process and only began to decline in the late stage of digestion. A slight increase in the reactor current was observed during the degradation of propionate, possibly due to its degradation to acetic acid by β-oxidation; at this time, the concentration of acetate increased slightly.
Comparing the net energy income under different sludge concentrations, it was found that with the increase in sludge concentration, the net energy income gradually increased (Figure 6). The maximum net energy income was obtained at a sludge concentration of 14 g/L, reaching 1.27 kJ/gVSS. Further evaluation of the electrochemical contribution for methanogenesis showed that according to the theoretical methane contribution with the formula 8e− + CO2 + 8H+ → CH4 + 2H2O and assuming that the electrons/H2 generated by the circuit are all converted into methane, the electrochemical reaction contributed 15.9–25.7 mL/d methane (calculated based on the average current of 6.34–10.25 mA). In comparison, it was found that the actual methanogenic rate (15.9–18.0 mL/d) of the low sludge concentration (6–8 g/L) was significantly lower than the theoretical methane contribution rate, indicating that the hydrogen produced by the cathode had not been completely converted to methane. Moreover, because the content of suspended sludge in the 6 g/L sludge concentration reactor was low, methane mainly came from the electrode reaction, so it can be concluded that the effective conversion rate of methane at the cathode was less than 50%. The methane production rate of the suspended sludge in the 14 g/L sludge concentration reactor was 37.0 mL/d, as shown in Table 1, and the actual methane production rate was 47.1 mL/d. According to the theoretical electrochemical methane contribution (25.73 mL/d), it can be concluded that only 39.3% of the theoretical electrochemical methane was converted to an actual methane increment (25.73% × 39.3% + 37.0 = 47.1). Therefore, how to further improve the methane conversion rate of the cathode will be the focus of future research.
4. Conclusions
The results showed that the organic loads of sludge had a significant effect on the performance of the bioelectrolysis-assisted AD system, which is directly related to the current and the contribution rate of methanogenesis by bioelectrolysis. With the increase in solid organic load, the production of VFAs increased, but the methanogenesis process showed a gradual lag phenomenon. The methane production rate increased most obviously when the sludge concentration increased from 8 g/L to 10 g/L. Further increasing the sludge concentration slowed the increase in the methane rate and prolonged the methane production cycle, which was not conducive to the maximum recovery and treatment of sludge. Hence, the maximum net energy income of 1.27 kJ/gVSS and methanogenic rate of 47.1 mL/d were obtained at a sludge concentration of 14 g/L with 71.6% VSS removal and 96.2 mL/gVSS total methane yield. Compared with the control at the same concentration, the bioelectrolysis-assisted reactor had significant advantages in reducing the reaction time and increasing the methane yield while also demonstrating its shock resistance under high organic loading.
Writing—original draft, X.K.; Writing—review & editing, W.L. and C.L.; Supervision, L.W.; Project administration, Y.L. All authors have read and agreed to the published version of the manuscript.
Informed consent was obtained from all subjects involved in the study.
The data presented in this study are available in insert article here.
The authors declare no conflict of interest.
Footnotes
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.
Enlarge this image.Figure 1. Schematic diagram of the mixed anaerobic reactors assisted by bioelectrolysis.
Enlarge this image.Figure 2. The anode current (A) and potential vs. SCE (B) with different sludge concentrations.
Enlarge this image.Figure 4. Changes in (A) proteins and (B) carbohydrates during the sludge acidification process.
Enlarge this image.Figure 5. Changes of (A) acetate, (B) propionate, (C) isobutyrate, (D) n-butyrate, (E) isovalerate, (F) n-valerate during the acidification process under different sludge concentrations.
Enlarge this image.Figure 6. The actual methanogenic rate, theoretical electrochemical methane contribution, and net energy income of the bioelectrolysis-assisted AD system with different sludge concentrations.
Methane production rate and VSS removal rate at different sludge concentrations.
| Sludge Concentrations | 14 g/L | 10 g/L | 8 g/L | 6 g/L | 14 g/L (Control) |
|---|---|---|---|---|---|
| VSS removal/% | 71.6 | 79.2 | 82.1 | 100 | 56 |
| Methanogenic rate /mL·d−1 | 47.1 | 34.6 | 11.7 | 7.9 | 37.0 |
| Cumulative methane/mL·gVSS− | 96.2 | 88.8 | 58.3 | 36.6 | 46.3 |
| Gp/d | 23 | 17 | 17 | 15 | 31 |
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; Wang, Ling 4
; Li, Chaolin 2 1 School of Civil and Environmental Engineering, Harbin Institute of Technology, Shenzhen 518055, China; Shenzhen Shenshui Water Resources Consulting Co., Ltd., Shenzhen 518004, China
2 School of Civil and Environmental Engineering, Harbin Institute of Technology, Shenzhen 518055, China
3 School of Civil and Environmental Engineering, Harbin Institute of Technology, Shenzhen 518055, China; State Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of Technology, Harbin 150090, China
4 School of Environmental and Municipal Engineering, Qingdao University of Technology, Qingdao 266000, China