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Article

Electrochemically Coupled Anaerobic Membrane Bioreactor Facilitates Remediation of Microplastic-Containing Wastewater

by
Kunpeng Zhou
1,†,
Huilin Yin
2,†,
Zhenyu Ding
2,
Nuchao Xu
2,* and
Yun Fan
2,*
1
Technical Centre for Soil, Agriculture and Rural Ecology and Environment, Ministry of Ecology and Environment, Beijing 100012, China
2
Chinese Academy of Environmental Planning, Beijing 100041, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Water 2024, 16(22), 3236; https://doi.org/10.3390/w16223236
Submission received: 21 October 2024 / Revised: 4 November 2024 / Accepted: 7 November 2024 / Published: 11 November 2024
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Abstract

:
Ubiquitous microplastics (MPs) severely affect the efficiency of anaerobic membrane bioreactors (AMBR) for wastewater treatment and energy recovery by inhibiting the metabolic activity of anaerobic microorganisms. The electrochemical system can not only accelerate waste metabolism but also improve microbial resistance by promoting interspecies electron transfer within the system, which has broad application potential in the remediation of MPs wastewater. This paper attempts to evaluate the effect of electrical stimulation on the efficiency of biological wastewater treatment processes containing MPs employing an electrochemical system coupled to an anaerobic membrane bioreactor (ECAMBR). The results showed that although MP exposure inhibited methanogenic performance, electrical stimulation effectively alleviated this inhibitory effect. Further analysis showed that microplastics increased cell damage and affected enzyme activity, but electrical stimulation could affect the stress response of microorganisms, leading to changes in their cell viability and enzyme activities. The 16S-rRNA sequencing indicated that the highest abundance of hydrolytic–acidogenic bacteria Firmicutes and Bacteroidota was found at the phylum level, whereas at the genus level, it was Christensenellaceae_R-7_group, and methanogens were dominated by Methylomonas, Methyloversatilis, and Methylobacter. Functional prediction analysis indicated that carbohydrate metabolism, amino acid metabolism, and energy metabolism were the dominant metabolic pathways and that electrical stimulation could enhance their activities. This study demonstrated the important role of electrochemical stimulation in the remediation of wastewater containing high concentrations of MPs.

1. Introduction

Plastic products are extensively utilized for their portability, durability, and malleability, and it is estimated that more than 7 billion tons of plastic waste have been generated globally and is growing at 400 million tons per year [1]. More than 80% of these plastic products are discarded without treatment, making plastic pollution an increasingly serious environmental problem. These waste plastics entering the environment will crack into microplastics (MPs, 1 µm~5 mm) or nanoplastics (NPs, <1 µm) under the action of hydrolysis, ultraviolet irradiation, mechanical abrasion, and biodegradation, further aggravating plastic pollution of the environment [2,3]. Sewage treatment plants serve as important points of MPs entry into the aquatic environment, releasing up to 80% of the total amount of MPs in natural waters [4]. There are many kinds of MPs in the wastewater, mainly polyethylene (PE), polypropylene (PP), polyvinyl chloride (PVC), and polyethylene terephthalate (PET), of which PE and PP account for 60% of the total [5,6]. In addition, examination of the MPs concentration in the wastewater revealed that the MPs in the raw wastewater ranged from 0.06 to 1.2 mg/L, with the highest being up to 29.6 mg/L [7]. In the biological treatment of wastewater, the presence of these MPs can not only direct contact with microorganisms and induce oxidative damage to microorganisms, leading to the rupture of cell membranes, but even enter the microbial cells, leading to alterations in functional enzyme activity and gene expression [8]. Moreover, MPs can also act as carriers for more complex combined pollution by attaching other exogenous pollutants (heavy metals, antibiotics, viruses, etc.) in the wastewater [9].
Anaerobic membrane bioreactors (AMBRs), which combine anaerobic digestion (AD) with membrane filtration technology, have a broad potential for application in high-strength wastewater treatment and biomass energy recovery [10,11]. Compared with conventional biological wastewater treatment methods, AMBR has the advantages of higher energy recovery efficiency, better degradation of high-strength organic wastes, longer sludge retention time, and better effluent quality. These advantages of AMBR make it widely applicable in many polluted wastewater remediation applications. For example, AMBR is frequently used for anaerobic bioremediation of pharmaceutical and swine wastewater, often with higher removal efficiencies than traditional anaerobic fermentation [12]. In addition, the microbial membrane in AMBR can also effectively intercept pesticides, polycyclic aromatic hydrocarbons, and antibiotics in wastewater and promote the degradation of these emerging pollutants [13]. However, the remediation of microplastic-containing wastewater by AMBR is currently unknown. The current study suggests that the effect of MPs on the activity of anaerobic microorganisms is two-fold, with typically low exposures stimulating enhanced microbial activity and high exposures inhibiting microbial metabolism [14]. The hazards of MPs mainly include three aspects: (1) the damage caused by particles of MPs in direct contact with cells or into the intracellular; (2) MPs as carrier adsorption of other pollutants, resulting in a compound pollution effect; and (3) MPs release of chemical substances or additives caused by the toxic effects [8,15]. Therefore, during wastewater treatment, the presence of high concentrations of microplastics can not only affect the cell viability of biofilms (BF) in the membrane module but also the metabolism of fluid anaerobic sludge (AS) in the non-module, which can greatly inhibit the overall fermentation performance.
To mitigate microplastic pollution in wastewater treatment and to improve the remediation of the system, the introduction of electrochemically coupled AMBR (ECAMBR) was considered an effective wastewater disposal approach [16]. Electrochemical coupling focuses on promoting the direct interspecies electron transfer (DIET) efficiency of microorganisms by applying a suitable voltage (0.2~1.0 V) to the system through an external power source, thereby enhancing the metabolic activity of microorganisms [17,18]. Electrochemical action for remediation of microplastic pollution consists of two main aspects: one is to promote the metabolism and mineralization of MPs, and the other is to enhance the resistance of microorganisms. Currently, researchers have found many anaerobic bacteria identified as having microplastic degradation capabilities, such as Holomonas, Cloacamonales, Thermotogales, and the number of sludge microbial communities [19]. Electrochemistry can act directly or indirectly on these microorganisms to enhance their metabolic activity or stimulate the expression of their functional genes by facilitating the electron transfer rate. In addition, electrochemical action can also promote the secretion of extracellular polymeric substances (EPS) of microorganisms, and it can directly adsorb MPs, thereby improving the resistance of microorganisms to adverse environments [20]. Wang et al. summarized the effects of electrochemistry as a potentially effective technology for mitigating microplastic contamination in wastewater in a review as follows: (1) accelerated the aging and decomposition process of MPs in wastewater; (2) enhanced the metabolic activity of microplastic-degrading microorganisms; (3) increased microbial resistance to MPs and the pollutants they release or adsorb; and (4) attenuated the compounding effect of MPs with other pollutants [21]. In another study by Wang et al., it was also demonstrated that bioelectrochemistry was effective in mitigating MP contamination during wastewater treatment and methane recovery [22]. In addition, another review by Wang et al. also demonstrated the possibility and prospect of bioelectrochemical systems for MPs removal in wastewater [23]. Conclusively, electrochemically coupled anaerobic microbial fermentation has great potential for the remediation of microplastic-containing wastewater, but its combined effect with AMBR has not been studied.
To fill the knowledge gap in this field, two systems, AMBR and ECAMBR, were used in this study to explore the microbial response to electrochemical action under different microplastic exposures (PE-MP and PVC-MP). For this objective, the fermentation performance of the reactor during operation was monitored, including the gas production performance and the fermentation broth physicochemical parameters. After the operation, biofilms (AS) attached to the membrane module and unattached anaerobic sludge (BF) were collected to analyze the effects of microplastic exposure on both microbial communities. On the one hand, the cell damage and functional enzyme activity of these samples were measured, and on the other hand, the microbial community structure and relative abundance were analyzed. Finally, the measured gene abundance was used to predict the change in its metabolic level. In summary, these findings demonstrate the important effect of electrochemistry in the remediation of microplastic-containing wastewater.

2. Materials and Methods

2.1. Reactor Construction

This experimental device was divided into two sizes: a normal anaerobic membrane bioreactor (AMBR) and an electrochemically coupled anaerobic membrane bioreactor (ECAMBR) (Figure 1). To avoid interference from external plastics, the AMBR utilized a 250 mL (working volume of 200 mL) glass bottle as a reactor with one membrane module. The ECAMBR employed two 250 mL glass bottles (total working volume of 400 mL) connected to form a single-chamber reaction device, with two membrane modules to facilitate the coupling of electrochemistry to form a bioanode and a biocathode. Carbon cloth (3 k, HesenElectric Co., Ltd., Shanghai, China) (thickness = 0.40 mm, pore size = 50 μm, porosity = 78.8%) was chosen as the filter for the membrane module because of its low cost, high specific surface area, good conductivity, and susceptibility to enrichment by anaerobic microorganisms. Titanium mesh (Baoji LiXing Titanium Group Co., Ltd., Baoji, China) (pore size = 0.6 mm × 1.0 mm, thickness = 0.12 mm) was used as the support material held together with carbon cloth to provide robustness for the module, and titanium wires (Baoji LiXing Titanium Group Co., Ltd., China) with a thickness of 0.10 mm were used as leads for the ECAMBR anode and cathode to facilitate the connection of external voltages to form a closed external circuit. The devices are sealed with a silicone plug, and two holes were drilled in the silicone plug for inlet/outlet and discharge, respectively.

2.2. Sources of Seed Sludge and Microplastics

Anaerobic sludge obtained from a sewage wastewater treatment plant in Tianjin was used directly as seed sludge for AMBR and ECAMBR because of its ability to manage high-strength organic wastes during wastewater treatment. Before use, the anaerobic sludge needs to be sieved to remove large impurities and then thickened by settling at 4 °C for 12 h. The main characteristics of the sludge after concentration were as follows: pH 6.9 ± 0.2, total solids 28,836 ± 321 mg/L, volatile solids 18,002 ± 175 mg/L. In addition, PE-MP and PVC-MP with the size of 5~15 µm were purchased from ball milling (Qinhuangdao Taiji Ring Nano Products Co., Ltd., Qinhuangdao, China). Currently, different kinds of microplastics are found in wastewater, of which PE-MP and PVC-MP were recognized as the most frequent types of polymers.

2.3. Reactor Operation and Physicochemical Characterization

This experiment explores electrochemically coupled anaerobic fermentation to remediate microplastic contamination in wastewater and is divided into AMBR and ECAMBR systems. Synthetic wastewater with the addition of microplastics was used to simulate microplastic contamination in real wastewater treatment. This synthesized wastewater was formulated in previous studies [24], and 2 g/L of glucose was used as a fermentation substrate for anaerobic microorganisms. Moreover, 5 mg/L of PE-MP and PVC-MP were added to the synthesized wastewater to explore the differences between AMBR and ECAMBR under the exposure of the two microplastics, respectively. During operation, sludge and synthesized wastewater were injected into the reactor at 1:1 and operated at room temperature for 48 days, with 50 mL of synthesized wastewater entering and departing every 3 days. Where a constant potentiostat was employed to provide a voltage of 0.7 V during the ECAMBR operation, resulting in an anode with a high electrode potential and a cathode with a low electrode potential. Since anaerobic microorganisms continuously attach to the carbon cloth to form biofilm during operation, two different microbial communities will form in AMBR and ECAMBR: biofilm (BF) attached to the module and anaerobic sludge (AS) at the reactor bottom.
Every three days, the biogas produced and the fermentation broth discharged were analyzed for physicochemical properties. Firstly, the biogas yield was measured using a graduated syringe, and then 2 mL was withdrawn and injected into the gas chromatograph (GC-2014, Shimadzu, Kyoto, Japan) for determination of component content (CH4, CO2), with a thermal conductivity detector (TCD) and helium as the carrier gas. Then, the pH, chemical oxygen demand (COD) concentration, and volatile fatty acid (VFAs: acetate, propionate, butyrate, and valerate) content of the fermentation broth were determined. The pH value of the fermentation broth was measured by a pH meter (FiveEasy Plus FP20, Mettler Toledo, Giesen, Germany). The COD concentration of the influent/effluent was then determined (water quality analyzer, ET99731, Lovibond, Amesbury, UK) by the acidic potassium dichromate method (K2Cr2O7), and the COD removal efficiency (COD% = (CODin − CODout)/CODin × 100%) was calculated. The VFAs content was determined by a gas chromatograph (GC, Agilent 7890B, Santa Clara, CA, US) equipped with a flame ionization detector (FID). The tests were conducted in triplicate, with results presented as the mean values.

2.4. Enzyme Activity Determination

At the end of the experiment, the AS and BF were withdrawn from the reactors for the measure of cell viability, including reactive oxygen species (ROS), lactate dehydrogenase (LDH), adenosine triphosphate (ATP), cytochrome c (cyt c), and extracellular polymeric substances (EPS). ROS and LDH are used to characterize oxidative damage and cell membrane damage caused by exogenous pollutants. The ROS generation and LDH release were determined using the dichlorofluorescein (DCF) assay and LDH kit (Nanjing Jian-Cheng Technology Co., Nanjing, China) [22]. The ATP activity and cyt c activity were measured using commercial test kits (Beijing Solarbio, Beijing, China). Furthermore, EPS was extracted using a modified oscillation–-ultrasound combined cationic resin extraction method and analyzed for the components (polysaccharides, proteins, lipids, humic acids, and nucleic acids) by the standard substance method [25]. In addition, enzyme activities were measured using seed sludge as a control group to comparatively analyze the changes in cell viability after microplastic exposure.

2.5. Microbial Community Analysis and Functional Prediction

The AS and BF samples collected from reactors were used to analyze the microbial community structure and relative abundance by 16S-rRNA high-throughput sequencing. This study was carried out to efficiently extract DNA from the samples by liquid nitrogen milling combined with a kit (Fast DNA Spin Kit for soil, Qiagen, Hilden, Germany) and to inhibit the DNA enzyme activity using phenol chloroform-isoamyl alcohol [26]. Then, DNA was tested for purity and quantity by agarose gel electrophoresis and a NanoDrop-2000 Spectrophotometer (Thermo Fisher Scientific, Wilmington, DE, USA), and in compliance with the requirements, it was amplified by polymerase chain reaction (PCR) utilizing universal primers 338F and 806R targeting the V3–V4 region of the 16S rRNA gene [27]. Before pyrophosphate sequencing, the PCR amplification products of the samples were normalized in equimolar amounts in the final mixture for the construction of PCR amplicon libraries. Subsequently, high-quality sequences were screened by QIIME2 and clustered as amplicon sequence variation (ASV) at a 97% similarity level. The microbial community structure and relative abundance were obtained by these ASVs through an online data-processing platform (Shanghai Majorbio, Shanghai, China). Moreover, the metabolic functional features of the microbial community were characterized using PICRUSt2.

3. Results and Discussion

3.1. Fermentation Properties During Wastewater Treatment

The daily biogas yield, VFAs concentration, COD removal efficiency, and accumulation methane yield in both AMBR and ECAMBR under PE-MP and PVC-MP exposure were evaluated (Figure 2). Throughout the experimental phase, the methanogenic capacity of all reactors decreased with the addition of MPs. In terms of biogas production, the microplastic post-exposure was 113 ± 5 mL/d, 106 ± 5 mL/d, 281 ± 11 mL/d, and 253 ± 9 mL/d in PE-AMBR, PVC-AMBR, PE-ECAMBR, and PVC-ECAMBR, which decreased by 37.22%, 42.26%, 25.67%, and 30.13% compared to pre-exposure (Figure 2A). Electrochemistry stimulated an increase in biogas production, which increased by 25.89% and 20.48% for PE-MP and PVC-MP exposures, respectively. This suggests, on the one hand, that microplastic exposure inhibits the methanogenic performance of the system, but, on the other hand, indicates that electrochemistry can mitigate this inhibitory effect. Similarly, the results also showed that PVC-MP caused stronger inhibition of methanogenic properties than PE-MP. This result was consistent with previous studies, indicating that PVC-MP has stronger bioinhibitory effects [28]. Further, by accumulating methane yields, it was found that at the end of the run, the total production of PE-AMBR, PVC-AMBR, PE-ECAMBR, and PVC-ECAMBR systems reached 1065 ± 159 mL, 988 ± 142 mL, 2985 ± 281 mL, and 2456 ± 211 mL (Figure 2B). In comparison, accumulation methane yield was 7.79% higher for PE-MP exposure than PVC-MP in AMBR and 21.55% higher for PE-MP than PVC-MP in ECAMBR. Whereas, electrochemistry significantly contributed to the methane yield, which increased by 40.09% and 24.24% for PE and PVC, respectively. This further shows that PVC has stronger biological toxicity and electrochemical stimulation has a strong promoting effect. Similar experimental phenomena were found by Wang et al., who utilized a bioelectrochemical system to treat high concentrations of PE-MP (10 mg/L) and showed a 30.71% decrease in methane production, accompanied by a decrease in COD removal efficiency and accumulation of VFAs [29].
Furthermore, the fermentation broth from each discharge was analyzed in this study, including VFA components and their contents as well as COD concentration changes. Glucose, being the only organic matter in the synthesized wastewater, provides a carbon source and energy to all the microorganisms in the system. Under the effect of the microbial community, fermentation bacteria will convert glucose into pyruvate; this process will mainly consume energy, and pyruvate, in the role of acid-producing bacteria, on the one hand, will be converted to acetate to participate in the acetoclastic methanogenesis pathway or further production of other organic substances, on the other hand, to generate ATP and nicotinamide adenine dinucleotide (NADH) to take part in the tricarboxylic acid (TCA) cycle [30,31]. Therefore, the concentration of VFAs within a normal fermentation system always maintains a dynamic equilibrium to ensure the synergistic effect of the fermentation, the acid production, and the methanogenesis process. In this study, it was found that the accumulation of VFAs in the system after MP exposure occurred to varying degrees (60.16–121.89%), and the concentration of accumulated acetate (31.65 ± 5.68~76.62 ± 8.27 mg/L) was higher than that of propionate (13.42 ± 1.62~35.32 ± 3.22 mg/L), butyrate (0.58 ± 0.09~9.11 ± 0.87 mg/L), and valerate (0.05 ± 0.01~0.37 ± 0.06 mg/L), with a higher degree of accumulation under PVC-MP exposure than PE-MP (Figure 2C). In addition, under electrochemical action, the concentration of VFAs accumulated in ECAMBR was lower, which was 56.90% and 44.32% lower than AMBR under PE-MP and PVC-MP exposure, respectively. This further illustrates the important role of electrochemical action in the remediation of wastewater containing microplastics. Similarly, Wang et al.’s study also demonstrated that MP exposure could lead to 40.3~272.7% VFA accumulation in bioelectrochemical systems [29]. Acetate is the main substrate type for methane metabolism in the natural system, which is involved in more than 60% of the total methane production in nature [32]. Therefore, it can be inferred that the accumulation of acetate reduces the activity of the acetoclastic methanogenesis pathway, which may be the main reason for the inhibition of methanogenesis by MPs. Certainly, the accumulation of VFAs will inevitably lead to changes in the COD concentration of the system. Calculating the COD removal efficiency of the system from the COD concentrations of the influent and effluent water, it was found that the COD removal rates in PE-AMBR, PVC-AMBR, PE-ECAMBR, and PVC-ECAMBR were 56.42% ± 4.35%, 52.11% ± 3.56%, 65.02% ± 5.25%, and 59.11% ± 3.87%, respectively, which were decreased by 11.28~30.90% compared to the pre-exposure period (Figure 2D). Whereas, the COD removal of the system under electrochemical action increased by 14.97% and 11.95% under PE-MP and PVC-MP exposure, respectively. In summary, measurements of gas production performance and physicochemical properties of the fermentation broth showed that MP exposure inhibited methane production and was accompanied by more accumulation of VFAs and lower COD removal. Meanwhile, electrochemistry played a good role in the remediation of microplastic-containing wastewater.

3.2. Shifts in Cell Viability and Enzyme Activity

In this study, cell viability and functional enzyme activities on AS and BF were analyzed in AMBR and ECAMBR using seed sludge as a control (Figure 3). Previous studies have shown that the effect of MPs on the system’s methanogenic performance is mainly through the inhibition of microbial activity. In this process, MPs as an exogenous pollutant can induce excessive production of ROS (e.g., H2O2, O2−, and OH•) like other pollutants (e.g., persistent chemicals, antibiotics, heavy metals, and pathogens) in wastewater, and elevated ROS levels may lead to cellular oxidative damage and redox imbalance, resulting in inhibition and metabolic disorders [33]. This is mainly attributed to the reactive groups on the surface of MPs that can respond to molecular dioxygen and generate ROS via free radicals and catalytic reactions, and even under anaerobic conditions, sub-micromolar oxygen present in the reactor can react with the abundant reactive sites on the surface of MPs to generate ROS via mutation and Fenton reactions [34]. Zheng et al.’s study has found that MPs can adsorb to cell surfaces and disrupt the normal function of cell membranes, and even smaller NPs can enter directly into the interior of cells to impede DNA replication and protein function loss [35]. In this study, it was found that the ROS levels of the samples were all greatly elevated (40.08~96.99%) compared to the seeded sludge after MP exposure, and only PE-ECAMBR-AS and PVC-ECAMBR-AS showed a decrease (15.68%, 11.84%, respectively), which suggests that MPs do cause oxidative damage to the microbial cells to varying degrees. Further analysis revealed that PVC-MP induced higher ROS than PE-MP, and electrochemistry was effective in decreasing the level of ROS, but BF exhibited higher oxidative stress than AS. Normally, cells can counteract oxidative stress by secreting a variety of antioxidant enzymes (e.g., superoxide dismutase, superoxide reductase, catalase, and peroxidase) [36], suggesting that electrochemistry may promote the secretion of these enzymes and thus reduce cellular damage. Of course, these hypotheses need to be followed by further experimental investigation. Further, damage to the cell membrane will result in the release of intracellular LDH. Consistent with changes in intracellular ROS levels, measurements of extracellular LDH showed that MP exposure led to an increase (20.15~100.41%) in extracellular LDH content. Interestingly, LDH release was higher in AS than BF in AMBR but lower in AS than BF in ECAMBR, and electrical stimulation enhanced LDH release. This suggests that electrical stimulation may have promoted enhanced cell membrane permeability, allowing more intracellular LDH to be released into the extracellular space.
In addition, the presence of MPs can affect the normal physiological and metabolic activities of microbial cells, including energy metabolism and electron transfer. ATP is a multifunctional nucleotide that acts as an intracellular coenzyme and plays a key role in intracellular energy transfer and cellular metabolism; it serves as an important indicator for characterizing the rate of energy metabolism in microbial cells, which is mainly produced through glycolysis and the tricarboxylic acid cycle [37]. In this study, it was found that MP exposure promoted the enhancement of ATP activity (26.64~67.15%), with this effect being best under PVC-MP exposure in ECAMBR (63.50~67.15%). This demonstrates that microorganisms can enhance their activity in response to MPs by increasing their energy metabolism rate, and this promotion is higher when the contaminant is more biotoxic, and electrochemical stimulation also enhances ATP activity. Former studies have demonstrated that the concentration of ATP in a normal bioelectrochemical system is approximately 1.5 times higher than in conventional systems and that this amount of activity and metabolism in most microorganisms is attributable to electrical stimulation [38]. Another study found that with appropriate electrical stimulation, ATP levels and microbial activity on enzymes could be increased, thereby increasing microbial growth rates and metabolic activity [39]. As a central cofactor in cell membranes, cyt c mediates the electron exchange of many oxidoreductases and plays an important role in microbial extracellular electron transport [40,41]. In this study, the overall cyt c activity was found to show varying degrees of decrease (4.48~32.75%) under MP exposure, but AMBR (22.90~32.75%) showed a higher decrease than ECAMBR (4.48~19.94%). The decrease in cyt c activity led directly to a decline in the DIET efficiency of microorganisms, suggesting that electrochemical stimulation facilitated the extracellular electron transfer rate of microorganisms to a certain extent. Further analysis revealed that the cyt c activity of AS was lower than BF, and the cyt c activity of the cathode was lower than the anode, suggesting that the carrier and external voltage can directly increase the DIET of microorganisms, but the anode has a stronger promotion effect. In contrast, Zhang et al. found that a small amount of PE-MP exposure (50 particles/L) instead promoted cyt c production and increased cyt c-mediated direct electron transfer [42]. This further illustrates the important role of electrochemistry in the remediation of wastewater containing high concentrations of MPs.

3.3. Changes in Microbial Resistance

When confronted with exogenous pollutant exposure, microorganisms can increase their resistance to unfavorable external environments by secreting EPS, which is a change in microbial resistance. EPS are macromolecular polymers produced by microorganisms, more than 90% of which are organics, including mainly polysaccharides, humic acids, proteins, lipids, and nucleic acids [43]. EPS has a variety of structural and functional benefits, such as improved cellular adsorption, surface characterization, enzyme retention, mass transfer stability, structural stability, and digestion [25]. Although EPS has a protective effect, the attachment of MPs to biomolecules on the cell surface increases the opportunity for MPs to contact with key enzymes, which may lead to a reduction and inactivation of enzyme activity, thus affecting the fermentation performance of the wastewater [44]. In this study, it was found that the secretion of total EPS under microplastic exposure showed different degrees of decrease (0.95~73.30%), with the lowest EPS concentration in AMBR (265.75 ± 28.56~289.08 ± 24.16 mg/L) and the highest concentration in ECAMBR (280.36 ± 21.37~341.16 ± 26.32 mg/L) (Figure 4). Further analysis revealed that the EPS content of AS in AMBR was lower than BF, whereas in ECAMBR the AS content was higher than BF. This suggests that high-concentration microplastic exposure inhibits EPS secretion, but electrical stimulation alters its content in AS and BF. Similarly, Zhang et al. demonstrated that PVC-MP exposure inhibited EPS secretion, resulting in anaerobic granular sludge and internal microorganisms being deprived of EPS protection, which led to particle rupture and decreased cell viability [45].
Further analysis of the content of each component of EPS showed that the content changed significantly under microplastic exposure. Firstly, the analysis of the protein content revealed that all the proteins in AMBR showed a slight decrease (0.05~13.28 mg/L), whereas in ECAMBR the protein content decreased under PE-MP exposure (29.11~41.96 mg/L), whereas it showed an increase under PVC exposure (5.09~20.54 mg/L). Previous studies have found that during microbial aggregation, the contaminants mainly react with the proteins in the EPS, thus serving to protect the microbial cells [44]. This suggests that electrical stimulation promotes an increase in the protein content of microorganisms under PVC-MP exposure, which helps mitigate the toxic effects caused by PVC on microbial cells. In contrast, the decrease in protein concentration in PE-MP exposure under electrochemical action suggests that the mechanism of microbial resistance to PE may be different from PVC, and this needs to be further explored. Polysaccharide is another important constituent of EPS, and in the present study, it was found that MP exposure resulted in different decreases (10.68~40.96 mg/L) in its content in AMBR and ECAMBR (PVC-MP exposure). In contrast, the polysaccharide concentration in PE-MP exposed to electrochemistry showed an increased concentration (50.17~74.16 mg/L), which further suggests that microorganisms exposed to PE-MP have a biological response mechanism different from PVC-MP. In addition, humic acid concentration under MP exposure presented a decrease (36.50~52.39 mg/L) in both AMBR and ECAMBR, while nucleic acids and lipids presented a reduction (4.98~9.98 mg/L, 4.40~9.43 mg/L, respectively) in BF under PE-MP exposure only in ECAMBR. Overall, electrochemical stimulation has an important augmenting effect on microbial resistance enhancement under high MP concentration exposure.

3.4. Microbial Community Structure and Function Predictive Analysis

At the end of the experiment, changes in microbial community structure and relative abundance were analyzed. From the result of sequencing, an average of 65,378 sequences per sample was achieved, and a total of 679 ASVs were assigned at a 97% similarity. Alpha diversity indexes from the microbial community under MP exposure were summarized and visualized in Table 1. Both Ace and Chao indexes were reduced compared to seed sludge, indicating that bacterial richness was decreased by MP exposure. However, the Ace and Chao indexes of ECAMBR increased compared to AMBR, which suggests that electrochemistry promotes the increase in bacterial richness. Meanwhile, a higher Shannon and high Simpson index of ECAMBR showed that electrochemical stimulation increased community diversity, which implies that ECAMBR selects for certain bacteria. Similar microbial diversity was reflected by the high PD whole-tree. These results indicate that electrochemical stimulation can reshape the microbial community structure to a higher diversity and richness without considering its significance.
To reveal changes in functional bacteria under the influence of electrochemistry, the microbial community composition of bacteria and archaea at the phylum and genus levels were characterized (Figure 5). The main phyla were Firmicutes (22.55~39.48%), Bacteroidota (12.68~26.99%), Synergistota (5.54~12.12%), Proteobacteria (0.35~10.66%), Thermotogota (3.96~7.92%), Spirochaetota (3.45~9.35%), and Cloacimonadota (2.57~6.97%) (Figure 5A). Interestingly, no archaea were found at the phylum level. As the most predominant phyla, the relative abundance of Firmicutes increased (12.09~75.09%) by MP exposure for the seed sludge, where electrical stimulation promotes its enrichment, and the abundance was higher at the anode than the cathode. In addition, the relative abundance of Firmicutes was lower under PE-MP exposure in AMBR than under PVC-MP exposure, whereas this difference narrowed in ECAMBR but showed a higher anodic than AS than cathodic. However, for the phylum of Bacteroidota, the percentage increased from 16.72% in the seed sludge to 17.28~26.99% except for PE-BF-Cathode (12.68%) with exposure to MPs. It has been shown that Bacteroidota and Firmicutes belong to the group of hydrolytic–acidogenic bacteria that promote metabolic synergies between dissolved organic matter (e.g., proteins and amino sugars), leading to increased production of VFAs [46]. For the phylum of Synergistota, the percentage decreased from 15.12% in the seed sludge to 5.54~10.26%, which suggests that it was intolerant to MP exposure. In addition, the relative abundance of Proteobacteria, Thermotogota, and Cloacimonadota was significantly elevated after MP exposure compared to seed sludge.
The relative abundance of domain genus from bacteria was calculated and illustrated in Figure 5B. It was found that most of the dominant genera were Christensenellaceae_R-7_group (5.27~27.85%), Lentimicrobium (0.63~9.01%), Mesotoga (2.73~5.59%), WCHB1-41 (0.60~16.49%), Bacteroidetes_vadinHA17 (1.55~7.13%), and Syner-01 (2.04~5.55%). As the most abundant bacteria, the relative abundance of Christensenellaceae_R-7_group under MP exposure was 7.25~22.58% higher compared to seed sludge (5.27%). In addition, the abundance of the bacteria was higher under PVC-MP exposure in AMBR, whereas it was higher under PE-MP exposure in ECAMBR. This suggests that electrochemistry affects the abundance level of the bacterium and that this effect manifests itself as higher at the anode than at the cathode. Previous studies have demonstrated that the Christensenellaceae_R-7_group can participate in the metabolism of refractory wastes [22], and the fact that the only refractory substance in this study was MPs suggests that the increase in its abundance may be related to the degradation of MPs. Lentimicrobium, the second most abundant bacterium in relative abundance, had an abundance of only 0.63% in the seed sludge, and MP exposure significantly increased its enrichment (2.28~9.01%). Further studies revealed that electrochemical stimulation reduced its relative abundance, but the abundance was still higher at the anode than at the cathode. From the microbial functional analysis, Lentimicrobium could convert polysaccharides into intermediate metabolites such as acetate and hydrogen, suggesting that the presence of MPs inhibited its activity but stimulated its enrichment. Additionally, the relative abundance of Mesotoga increased slightly in AMBR while it decreased in ECAMBR. In contrast, both Bacteroidetes_vadinHA17 and Syner-01 showed a decreasing trend in abundance after MP exposure and exhibited higher AS than BF. Further, analysis at the Archaea genus level revealed that the methanogens in the system were mainly Methylomonas, Methyloversatilis, and Methylobacter (Figure 6). It was found that the relative abundance of Methylomonas increased after microplastic exposure, that this increase occurred mainly in the BF, and that electrical stimulation could also promote its enrichment. It was found that Methylomona is capable of degrading trichloroethylene through methane monooxygenase co-metabolism, and it was hypothesized that it may play an important role in MP degradation and transformation [47]. In contrast, the relative abundance of Methyloversatilis showed a decrease after microplastic exposure, and the BF was overall lower than AS. Meanwhile, the relative abundance of Methylobacter was also lower in BF than in AS. Earlier studies have found Methylobacter to have the ability to degrade polypropylene [48], so this difference in abundance may be related to the breakdown of microplastics in the system. However, due to the lack of absolute quantification, it is not possible to accurately assess their enrichment in the groups, and the corresponding analyses will have to be carried out in subsequent studies.
In this study, functional gene prediction was also performed by classifying ASVs (Figure 7). Among them, the most important were carbohydrate metabolism, amino acid metabolism, energy metabolism, metabolism of cofactors and vitamins, and translation. In this study, glucose was used as the only fermentation substrate, so all the substance metabolism and energy generation of the microorganisms in the system were related to carbohydrate metabolism. It was found that carbohydrate metabolism levels showed an overall decrease (2.75~8.31%) after MP exposure and an increase under PVC-MP exposure in ECAMBR (1.94~5.89%). This further demonstrates that the presence of MPs has an inhibitory effect on glucose conversion and that electrical stimulation promotes glucose metabolism in PVC-MP. Amino acid metabolism, the second highest metabolic pathway, also showed slight inhibition of its expression level by MPs, whereas it showed promotion at PVC-MP, especially by electrochemical action (2.60~6.39%). Other studies have also shown that the amino acid metabolism of cofactors and vitamins can be significantly different under MP exposure [49]. These two metabolic pathways are closely related to the degradation of sugars such as alanine, aspartic acid, and glutamic acid [50], and thus the presence of MPs affects the metabolic performance and potentially the nutrient metabolism of specific communities. Furthermore, energy metabolism plays an important role in microbial physiological activities, and in this study, we found that this pathway was inhibited in AMBR (0.74~4.76%), whereas this inhibition was attenuated in ECAMBR and even showed enhancement under PVC-MP exposure (3.88~7.13%). These results further demonstrate the important role of electrochemistry in the remediation of microplastic-containing wastewater.

3.5. Environmental Impacts and Future Perspectives

Anaerobic membrane bioreactors (AMBR) have the advantages of efficient solid–liquid separation, low sludge yield, and high biomass concentration in the treatment of high-strength organic wastewater, but the large number of new pollutants (MPs, heavy metals, antibiotics, etc.) present in the wastewater can directly interact with the microorganisms to affect the wastewater treatment performance. From the technical feasibility analysis, the coupled electrochemical system not only enhances the degradation and transformation of difficult-to-degrade wastes (MPs) but also improves the resistance of microorganisms to exogenous pollutants, which has a wide potential for application in wastewater remediation. Meanwhile, electrical stimulation can elevate the abundance and metabolic ability of some functional microorganisms in the microbial communities, promoting the cleavage and mineralization of MPs rather than transforming them into NPs, exacerbating the contamination effect [51]. From the economic feasibility analysis, this enhanced microbial DIET efficiency is environmentally friendly compared to conventional methods by saving significant carbon sources, electricity, and labor inputs and reducing subsequent treatment costs. Moreover, due to the low applied external voltage, long-term operation and sustainability can be achieved by incorporating photovoltaic conversion equipment to feed the system [52,53]. This study investigated the microbial response and community changes in microorganisms facing microplastic exposure by electrochemistry and demonstrated the technological potential of utilizing electrochemical remediation of wastewater containing high concentrations of microplastics. Insufficiently, however, the cracking and mineralization of microplastics themselves by electrochemical action has not been studied, as has the change in abundance of microplastic-degrading bacteria in the system, which lacks in-depth analysis. Furthermore, there is still a gap in the abundance of functional genes associated with microplastic degradation and changes in their expression levels, which requires subsequent in-depth studies.

4. Conclusions

This study demonstrated the feasibility of electrochemically coupled AMBR for the remediation of highly concentrated microplastic wastewater. Analyzing the fermentation performance, although the high concentration of MPs exposed inhibited methane production, aggravated the accumulation of VFAs, and reduced the COD removal efficiency, the electrochemical effect effectively mitigated this inhibitory effect. Cell viability and enzyme activity analyses revealed that electrochemistry alleviated oxidative damage (ROS) in microorganisms but increased LDH release. Further, ATP activity associated with energy metabolism was enhanced, but cyt c activity associated with electron transport was reduced. Also, electrical stimulation affected the secretion of microbial EPS and changes in the content of its components (proteins, polysaccharides, etc.). The microbial community structure revealed that the highest abundance of hydrolytic–acidogenic bacteria Firmicutes and Bacteroidota was found at the phylum level, whereas at the genus level, it was Christensenellaceae_R-7_group, and methanogens were dominated by Methylomonas, Methyloversatilis, and Methylobacter. Functional prediction analyses further revealed that carbohydrate metabolism, amino acid metabolism, and energy metabolism are the major metabolic pathways of the microorganisms in the system and that electrochemical actions all contribute to their activities.
This study demonstrated the feasibility of electrochemical stimulation for the remediation of microplastic-containing contaminated wastewater, but the actual wastewater is often a composite pollutant system, including antibiotics, heavy metals, and agriculture. Therefore, it is necessary to explore the remediation effect of electrochemical action in the situation of multiple pollutants acting in combination in future studies to lay the foundation for the practical application of this technology.

Author Contributions

Conceptualization, K.Z. and N.X.; methodology, investigation, writing—original draft preparation, and writing—review and editing, N.X. and Z.D.; funding acquisition, H.Y. and Y.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The data presented in this study are available upon request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Structure of anaerobic membrane bioreactor and electrochemically coupled anaerobic membrane bioreactor (ECAMBR) devices.
Figure 1. Structure of anaerobic membrane bioreactor and electrochemically coupled anaerobic membrane bioreactor (ECAMBR) devices.
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Figure 2. Analysis of methanogenic performance during operation. (A) Daily biogas yield; (B) accumulative methane yield; (C) volatile fatty acid concentration (acetate, propionate, butyrate, and valerate) in the fermentation broth; and (D) COD removal efficiency.
Figure 2. Analysis of methanogenic performance during operation. (A) Daily biogas yield; (B) accumulative methane yield; (C) volatile fatty acid concentration (acetate, propionate, butyrate, and valerate) in the fermentation broth; and (D) COD removal efficiency.
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Figure 3. The determination of cell viability and enzyme activity of AS and BF in AMBR and ECAMBR reactors and seed sludge were used as controls.
Figure 3. The determination of cell viability and enzyme activity of AS and BF in AMBR and ECAMBR reactors and seed sludge were used as controls.
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Figure 4. Content of extracellular polymeric substances (EPS) secreted by microorganisms and concentration of each component.
Figure 4. Content of extracellular polymeric substances (EPS) secreted by microorganisms and concentration of each component.
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Figure 5. The microbial community structure and relative abundance of bacteria based on 16S-rRNA sequencing analysis. (A,B) represented the phylum level and genus level, respectively.
Figure 5. The microbial community structure and relative abundance of bacteria based on 16S-rRNA sequencing analysis. (A,B) represented the phylum level and genus level, respectively.
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Figure 6. The microbial community structure and relative abundance of methanogenic archaea at genus level based on 16S-rRNA sequencing analysis.
Figure 6. The microbial community structure and relative abundance of methanogenic archaea at genus level based on 16S-rRNA sequencing analysis.
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Figure 7. The PICRUSt2 analysis by number of ASV expression and KEGG pathway.
Figure 7. The PICRUSt2 analysis by number of ASV expression and KEGG pathway.
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Table 1. Alpha diversity of AS and BF samples, including the richness, diversity, and coverage index.
Table 1. Alpha diversity of AS and BF samples, including the richness, diversity, and coverage index.
α-IndexSeed SludgePE-ASPE-BFPVC-ASPVC-BFPE-ECAMBR-ASPE-BF-AnodePE-BF-CathodePVC-ECAMBR-ASPVC-BF-AnodePVC-BF-Cathode
PD53.6689147.5655545.9512247.8437945.8555759.8774250.7743653.1406659.4197947.9515351.16805
Chao447.5831388.6456373.6525397.0422363.7217525.8259444.0042469.3273535.8279400.6781425.9901
Shannon6.9274946.8454066.5939826.8863266.6222417.2493176.9373316.7428477.3934046.8623426.862443
Simpson0.9813320.9818390.9778340.9818960.9795710.9855610.9808860.9782890.9879620.9824580.982439
Coverage0.9996330.9996710.9997070.9997610.9997980.9995350.9996910.9995530.9996170.9996880.999622
Ace446.8139385.5495372.6485396.3976360.9708523.4619441.0679465.1366531.8799398.0596421.3268
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Zhou, K.; Yin, H.; Ding, Z.; Xu, N.; Fan, Y. Electrochemically Coupled Anaerobic Membrane Bioreactor Facilitates Remediation of Microplastic-Containing Wastewater. Water 2024, 16, 3236. https://doi.org/10.3390/w16223236

AMA Style

Zhou K, Yin H, Ding Z, Xu N, Fan Y. Electrochemically Coupled Anaerobic Membrane Bioreactor Facilitates Remediation of Microplastic-Containing Wastewater. Water. 2024; 16(22):3236. https://doi.org/10.3390/w16223236

Chicago/Turabian Style

Zhou, Kunpeng, Huilin Yin, Zhenyu Ding, Nuchao Xu, and Yun Fan. 2024. "Electrochemically Coupled Anaerobic Membrane Bioreactor Facilitates Remediation of Microplastic-Containing Wastewater" Water 16, no. 22: 3236. https://doi.org/10.3390/w16223236

APA Style

Zhou, K., Yin, H., Ding, Z., Xu, N., & Fan, Y. (2024). Electrochemically Coupled Anaerobic Membrane Bioreactor Facilitates Remediation of Microplastic-Containing Wastewater. Water, 16(22), 3236. https://doi.org/10.3390/w16223236

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