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Review

Enhanced Anaerobic Digestion Using Conductive Materials through Mediation of Direct Microbial Interspecies Electron Transfer: A Review

by
Tianqi Kong
and
Wanli Zhang
*
School of Energy and Environment, Shenyang Aerospace University, No. 37 Daoyi South Avenue, Shenyang 110136, China
*
Author to whom correspondence should be addressed.
Fermentation 2023, 9(10), 884; https://doi.org/10.3390/fermentation9100884
Submission received: 29 August 2023 / Revised: 19 September 2023 / Accepted: 22 September 2023 / Published: 29 September 2023
(This article belongs to the Special Issue New Research on Biomethane Production)
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Abstract

:
The anaerobic digestion (AD) of organic matter is susceptible to the challenges posed by low-speed electron transfer between microorganisms and the limitation of low hydrogen partial pressure, resulting in low methane recovery efficiency and poor system stability. Numerous studies in recent years have shown that a variety of conductive materials can significantly increase the interspecies electron transfer (IET) rate, optimize the structure and function of anaerobic microbial communities, improve methane yield, and promote system stability by mediating the direct interspecies electron transfer (DIET) of reciprocal microorganisms. In this study, on the basis of investigating the IET mechanism of methanogenic microorganisms in the AD of organic matter, the effects of carbon-based conductive materials (activated carbon, biochar, carbon cloth, carbon fiber, graphite, graphite felt, graphene, and carbon nanotubes) and iron-based conductive materials (magnetite, Fe3O4, hematite, Fe2O3, goethite, and zero-valent iron) on AD performance and microbial community using DIET are reviewed. Future research should focus on establishing an evaluation system, identifying flora with DIET potential, and finding methods for engineering applications that increase recovery efficiency and reveal the principle of conductive materials to mediate DIET.

1. Introduction

Anaerobic digestion (AD) is a microbial process of breaking down biodegradable matter under anaerobic conditions, which can achieve pollution control and energy recovery [1]. Thus, AD has attracted significant attention in research surrounding renewable energy production (such as through biogas), reducing the greenhouse effect, and waste disposal. The consortium effect of various microorganisms ensures the progress of AD, that is, hydrolysis, acidogenesis, acetogenesis, and methanogenesis. Complex organic matter is initially converted into simple organic matter (carbohydrates, proteins, and fats) through hydrolytic bacteria, and then simple organic matter is converted into VFAs and alcohols and further transformed into acetate and hydrogen. Aceticlastic methanogens cleave acetate into methane and bicarbonate, and hydrogenotrophic methanogens oxidize hydrogen with CO2 as the terminal electron acceptor to produce methane. However, there are a series of problems in the AD process, including long lag time, unstable system, low biogas production, the accumulation of volatile fatty acids (VFAs), and an increase in hydrogen pressure [2]. Therefore, the question of how to improve AD performance and realize an efficient and steady process needs to be answered urgently.
The process of electron production and transfer is critical and determines the efficiency of methane production. The conventional electron transfer pathway is mediated by interspecies electron transfer (MIET), including interspecific hydrogen transfer (IHT) and interspecific formic acid transfer (IFT). Hydrogen or formate is used as the electron carrier in IHT and IFT. The efficiency of MIET is low due to low diffusion efficiency and long intercellular distance and is easily affected by hydrogen pressure [3]. The low efficiency of MIET leads to low methane production. DIET can overcome the inhibition of hydrogen pressure and formate concentration without intermediates and extra energy to realize a high-speed electron transfer process and increase the methane production rate. That is, CO2 is reduced to methane by directly accepting electrons [4]. DIET is mediated through three different mechanisms: conductive pili, C-type cytochrome (OmcC), and conductive materials. Among these, conductive materials function as an electronic conduit and participate in the process of electron transfer, thus facilitating the preservation of cell energy. To date, it has been established that conductive materials that can mediate DIET are either carbon-based conductive materials (biochar, activated carbon, carbon cloth, carbon fiber, graphite, graphite felt, graphene, and carbon nanotubes) [5] or iron-based conductive materials (magnetite (Fe3O4), hematite (Fe2O3), goethite, and zero-valent iron) [6]. Both types have electrical conductivity, biocompatibility, chemical stability, and large specific surface area, which can shorten the lag time, promote the stability of the system, increase biogas production and methane content, and inhibit VFA accumulation [7]. This paper mainly summarizes the mechanisms of DIET, as well as the application, specific mechanism, and promotion effect of conductive materials in AD, and thus provides a reference for using conductive materials to effectively enhance methane yield through DIET.

2. The Type and Mechanisms of IET in AD

AD includes four stages: hydrolysis, acidification, acetylation, and methanogenesis [6]. In the stages of hydrolysis and acidification, macromolecular organics are converted into micromolecular organics (glucose, amino acids, long-chain fatty acids, etc.) and are then further fermented into VFAs, alcohols, CO2, and H2. The above-mentioned products can be metabolized into acetate, CO2, and H2 using hydrogen-producing acetogen [5]. Secondary products are utilized by methanogens to produce methane. However, in the process of AD, the dynamic imbalance between the production of fermenting bacteria and hydrolytic bacteria easily leads to the accumulation of intermediates especially VFAs, further leading to system acidification and even collapse [8]. In conclusion, the degradation of VFAs is a “bottleneck” in methane formation. The reason is that the degradation process cannot be carried out spontaneously as the Gibbs free energy is positive in the standard state [7]. When methanogens eliminate final products such as acetate and H2, the thermodynamic barriers between symbiotic microorganisms can be overcome, leading to the degradation of intermediates. The generation and transfer of electrons is essential for AD, that is, IET. IET can be divided into two types: IHT and IFT [7]. The electron transfer pathways between different species during AD are shown in Figure 1 [9].

2.1. Mechanisms of MIET

The interspecific formic acid transfer was first suggested in the early 20th century; Methanobacillus omelianskii was the first strain to be identified as degrading CO2 to methane through H2. Then, Bryant [10] found a strain with the same function in a co-culture of acidogenic bacteria and methanogenic bacteria. However, the process can only take place spontaneously under low hydrogen partial pressure and hydrogen partial pressure was uncontrollable. On the other hand, methane production via MIET can use just a few substrates, only requiring small molecular compounds (CO2, formic acid, methanol, methylamine) hydrolyzed by macromolecular organic compounds. The schematic diagram of MIET is shown in Figure 2 [11].

2.2. Mechanisms of DIET

Summers et al. [12] deleted the key gene of OmcS or PilA by artificial means, so that microorganisms no longer proliferated in co-culture systems. Then, DIET via conductive pili and OmcC were discovered. Compared with MIET, DIET has higher electron transfer efficiency and a thermodynamic advantage. According to the electrochemical model of reaction diffusion, the electron transfer efficiency of DIET is 8–9 times that of IHT. Therefore, DIET could directly produce a high-speed electron transfer process without forming or consuming intermediates [13]. Schematic diagrams of DIET are shown in Figure 3 [11].

2.2.1. DIET via Conductive Pili

Conductive pili are polymeric protein microfilaments that are similar to cilia; they have electrical conductivity and grow around the cells [14]. Conductive pili can be used as molecular wires to realize electron transfer. Holmes et al. [15] found that high-Methanothrix-expressing genes were the dominant flora, and they were involved in the metabolism of CO2 through Meta transcriptome sequencing analysis of microbial communities and Geobacter. High expression of key genes encoding conductive hyphae proved that Geobacter and Methanothrix mediated DIET via the conductive pili. In addition, DIET can also be mediated by C-type cytochrome and conductive materials.

2.2.2. DIET via C-Type Cytochrome

Cytochrome is a redox protein with a special function on the surface of microbial cells and has the ability to transfer electrons directly to receptors. Summers et al. [12] discovered that Geobacter metallireducens and Geobacter sulfurreducens could form electrically conductive aggregates to mediate DIET in the ethanol mutual oxidation system. DIET was achieved using a C-type cytochrome. In addition to OmcC, proteins such as OmcB, OmcS and OmcE can also be used as intermediates to mediate DIET.

2.2.3. DIET via Conductive Materials

The addition of conductive materials can accelerate electron transfer between acidogenic bacteria and methanogen. Kato et al. [16] discovered that the production of methane increased significantly and Geobacter were enriched when a system was supplemented with magnetite. Rotaru et al. [17] demonstrated that activated carbon can replace pili to mediate DIET. The mechanism of DIET via conductive materials varies with the type of conductive material being used. Then conductive materials have a large specific surface area, microorganisms can attach to them, grow, and transfer electrons on their surfaces; nanoscale conductive materials can replace OmcS or serve as electron conduits in the acceleration of electron transfer.

3. Enhancing Methanogenesis through Conductive Materials Supplement via DIET

The electron transfer rate determines whether the process of organic matter degradation and methane production can be carried out efficiently. The electron transfer rate of DIET is evidently higher than that of MIET and more conducive to the methane production process [13]. It is difficult for DIET to store more energy and to be established in natural environments. Thus, it is particularly important to stimulate DIET by artificial means. The literature [18] shows that conductive materials can preserve cells’ energy and can also be used as electronic conduits or electronic conductors to mediate DIET, further increasing methane production and shortening lag time.

3.1. Enhanced AD by Carbon-Based Conductive Materials via DIET

Many studies in the field have reported an increase in methane formation and a shortening of the lag period in response to supplementation with carbon-based conductive materials. At present, carbon-based conductive materials include biochar, activated carbon, carbon cloth, carbon fiber, graphite, graphite felt, graphene, carbon nanotubes, and so on [5]. These carbon-based conductive materials possess high electron conductivity, bio-compatibility, chemical stability, light weight, and high economy. Although nanoscale conductive material are highly toxic to microorganisms, a proper concentration can accelerate the AD process [19]. Nanomaterials have higher mechanical strength, electrical conductivity, and thermal conductivity than other materials. This enables carbon-based conductive materials to be extensively used in establishing and accelerating DIET. Table 1 summarizes effects of carbon-based conductive materials on the AD of different substrates.

3.1.1. Activated Carbon

The characteristics of activated carbon include small particle size, large specific surface area, and high conductivity. These characteristics enhance AD performance by buffering pH and enriching methanogenic bacteria and CH4 production rate [20]. Smaller particle sizes induce a more uniform dispersion and better mass transfer in AD process [21]. Larger specific surface area provides more space for microorganisms. Zhang et al. [21] found that powdered activated carbon (PAC) was more effective than granular activated carbon (GAC) based on a shorter lag time, a higher utilization rate of soluble organic matter, and a higher hydrolysis rate. Meanwhile, PAC can adsorb inhibitors (such as VFAs and NH3) and provide a more suitable environment for microorganisms [22]. Apart from the characteristics of activated carbon, the addition concentration significantly affects the AD process. The optimum dosage of GAC was reported to be 8 g/L [23]. Exceeding this dosage can inhibit the effect of AD and reduce the maximum methane production by 20–50% [23]. The studies reported here have utilized a certain type of enriched microorganisms which allow researchers to speculate on the relationship between activated carbon and DIET. When adding 0.6 mm GAC into liquid and raw fractions of swine manure, the methane yield was increased by 11.5% and 37.8%, respectively, and Pseudomonas was enriched with an abundance of 31%. Therefore, Romero et al. [24] suggested that Pseudomonas may mediate DIET. When using food waste as a substrate, Zhang et al. [21] found that the methane yield was increased by 150% and the abundance of Methanosarcina was greatly increased with the addition of activated carbon under high-temperature conditions. Ma et al. [25] found that the cumulative methane yield was 22.0% higher and the lag phase was 62.5% shorter than those of reactors without activated carbon. Additionally, a high abundance of Geobacter was detected. Then, PAC acted as the electronic bridge, which mediated DIET, promoting the growth of Methanosarcina and Geobacter.

3.1.2. Biochar

Biochar is the carbonaceous product obtained by thermochemical conversion of biomass which has extensive sources and excellent performance [3]. The addition of biochar can enhance AD performance by accelerating DIET efficiency. Wang et al. [26] found that the maximum CH4 production rate increased from 4.0 mL/d to 10.4–13.9 mL/d with the addition of biochar. It is considered that the improvement of DIET efficiency is mainly related to the properties of biochar, including specific surface area, porous structure, conductivity, and surface-functional groups (such as quinone groups). The porous structure and rough surface morphology provide enough attachment sites for microorganisms, strengthen the attachment of microorganisms, and indirectly promote DIET [27]. Abundant surface groups can directly promote the electron transfer between electroactive microorganisms. Among these, alkaline surface-functional groups can improve the acidification of the system [28]. Lu et al. [29] discovered that the electrical conductivity of biochar can further enhance the affinity of Methanosarcina to the surface of biochar. In addition, the efficiency of electron transfer between acidogenic bacteria and methanogenic bacteria determines the rate of AD. The addition of biochar can accelerate the DIET, but the key mechanism of DIET via biochar remains uncertain. Some studies have suggested that biochar can be used as an electronic catheter between acidogenic bacteria and methanogenic bacteria to maintain the symbiosis [29]. In addition, some studies have suggested that biochar can be used as an electronic conductor or shuttle to mediate DIET [30].

3.1.3. Carbon Cloth

Carbon cloth, a type of widely used conductive material, has been used as an electrode in microbial electrochemical systems [31]. AD performance, hydrogen partial pressure tolerance, and methane production can be improved [32] due to the large specific surface area and high electrical conductivity of biochar. Jia et al. [33] found that five pieces of carbon cloth increases the removal efficiency of chemical oxygen demand (COD) to 98%. The large specific surface area is able to fix microorganisms to the surface of the carbon cloth, reducing the loss of microorganisms. The high electrical conductivity affects the electronic exchange between microorganisms further, leading to an improved AD performance via DIET. Researchers [34] have noted that Geobacter without conductive pili and OmcC can exchange electrons with Methanosarcina in the presence of carbon cloth, providing direct evidence for the advantages of carbon-cloth-mediated DIET. Surprisingly, the reactors can still run efficiently under high organic load with carbon cloth [35]; methane yield and organic-matter-removal efficiency were significantly improved. Meanwhile, a large number of Sporanaerobacter and Enterococcus—which are capable of metabolizing fermentable substrates and transferring these electrons to Methanosarcina—were found to be enriched on the carbon cloth; this was a new discovery, building on previous research that had accelerated the metabolism between acidogen and methanogen using DIET.

3.1.4. Carbon Fiber

As a carbon-based conductive material, carbon fiber possesses high electrical conductivity and a large specific surface area [36], which can accelerate the process of AD without causing clogging [37] or erosion loss [38]. Carbon fiber can enrich electroactive bacteria, which can promote DIET among symbiotic microorganisms. When using propionate and butyrate as co-substrates, tha addition of carbon fiber can increase the methane production rate by 6.7 times; in this process, carbon fiber can act as an electronic conduit, rather than producing conductive fimbriae or cytochrome to participate in DIET [38]. Similar findings were reported in an experiment which used ethanol as the substrate; here, the maximum methane production rate was shown to increase by 40% [39]. Thus, it has been speculated that methanogenic bacteria may produce methane by directly receiving electrons from microorganisms such as Geobacter.

3.1.5. Graphite and Graphite Felt

Graphite, a crystalline allotrope of carbon, is reported to stimulate DIET. It has a high adsorption ability and electrical conductivity and has a high specific surface area [40]. Graphite can increase methane production, inhibit VFAs accumulation, and increase electron transfer rates. Muratcobanoglu et al. [40] found that 1 g/L graphite increased the observed accumulative biogas production by 19.75%. High conductivity enables graphite to act as an electron conduit in electron transfer [41]. In addition, graphite plays the role of electron transporter, with a fimbriae-like structure enabling the promotion of DIET among symbiotic microorganisms [40].
Graphite felt is obtained by treating carbon felt at high temperatures above 2000 °C in a vacuum or an inert atmosphere. Compared with other carbon-based conductive materials, graphite felt has a higher economy. The excellent conductivity and high specific surface area of graphite felt are beneficial to the growth and metabolism of anaerobic microorganisms. Meanwhile, graphite felt also can be used as a permanent part of the design of a digester [42]. Zhang et al. [43] found that the average CH4 production rate increased by 16.7–19.1% with the use of graphite felt. In the process of treating artificial wastewater with AD, graphite felt provided a new metabolic pathway for propionate and butyrate under DIET [43]. Organic acid can still be degraded when the AD system is be maintained under steady high-H2 partial pressure.

3.1.6. Graphene

Graphene is a kind of nanocarbon material formed by the close packing of carbon atoms connected by SP2 hybridization with a single-layer two-dimensional honeycomb lattice structure [44]. Graphene is micro-sized, has a large specific surface area, and has high electrical conductivity; therefore, it can be closely combined with many microorganisms [44]. Many studies have confirmed that graphene could participate in DIET by enriching DIET genus [44,45,46,47]. The methane yield was found to be increased by 17.0% and 51.4% in a system of synthetic wastewater with 30 mg/L and 120 mg/L graphene, respectively [48]. However, the toxicity of graphene has an inhibitory effect on microorganisms and even damages the bacterial cell membrane [46]. A proper amount of graphene can promote performance. A study performed by Lin et al. [45] showed that the methane production rate was significantly increased with the use of 1.0 g/L of graphene, whereas methane production rate decreased slightly when the concentration exceeded 2.0 g/L. And the inhibitory effect increased with the concentration of graphene, which indicated that cytotoxicity may be a limiting factor in the application of graphene nanomaterials.

3.1.7. Carbon Nanotubes

Carbon nanotubes are toxic to cells [49,50], but their stable tubular structure and high electrical conductivity can improve the AD process because of their mediation of DIET [51]. The organic matter decomposition rate and methane yield were increased with the acceleration of DIET. When the AD reactor was fed with livestock manure [52], 21,876.0 mL/g biogas and 7313.2 mL/g methane were produced following supplementation with multi-walled carbon nanotubes, in which methane production was increased by 12.6%. When the reactor was fed with beet sugar industrial wastewater [51], the addition of 500 mg/Kg multi-walled nanotubes increased methane production by 46.8% and decreased total solid content by 12.8%. In addition, carbon nanotubes can interact with extracellular polymers, provide cell protection, and prevent the nanoparticles from piercing through the membranes, and thus prevents the occurrence of cytotoxicity.

3.1.8. Magnetic Biochar

Magnetic biochar generally refers to the compounding of biochar and Fe3O4. Magnetic biochar improves the dispersibility of Fe3O4 and the surface properties of biochar. It was found that, after loading with Fe3O4, the specific surface area, surface-active sites, and surface-functional groups of magnetic biochar were improved; this information gives insight into magnetic biochar’s potential for mediating electron transfer [53]. During AD, magnetic biochar can exert the dual DIET effect of biochar and Fe3O4 at the same time [54]. Jin et al. [54] found that the optimal addition of magnetic biochar was 1 g/L; here, the methane production rate reached 208.7 mL/g VS, which was 22.1% higher than that of the control. Meanwhile, magnetic biochar improved the secretion of electroactive substances like humic substances and cytochrome C, which could promote extracellular electron transfer. Ni et al. [55] found that the addition of magnetic biochar changed the microbial community structure; here, Geobacter and Methanobacterium were highly enriched.
Table 1. Effects of carbon-based conductive materials on anaerobic digestion of different substrates.
Table 1. Effects of carbon-based conductive materials on anaerobic digestion of different substrates.
Carbon-Based Conductive MaterialsAD
Mode		AD SubstrateInoculum Ratio (Substrate: Inoculum)Organic LoadpHTemperature (°C)Effect on AD PerformanceReferences
TypeDosage
Biochar15 g/LBatchPhenol1:42.38 g COD/L-35The maximum CH4 production rate increased from 4.0 mL/d to 10.4–13.9 mL/d.[26]
Biochar10 g/LBatchGlucose6:16.00 g/L7.037The maximum methane production rate increased by 23.5–47.1%.[29]
Biochar25, 50 g/LBatchFood waste1.8:18.50 g VS/L-35The accumulative methane yield reached 110.3 mL CH4/g VS and 126.7 mL CH4/g VS.[56]
Biochar10 g/LBatchOil1:13.00 g/L7.055
35		CH4 production increased by 13.3–32.5% in thermophilic digesters.[27]
Biochar13 g/LBatchChicken
manure		4.2:149.77 g VS/L-35The highest cumulative methane yield obtained was 294 mL/g VS, which was 69% higher than that of the control.[57]
Biochar10 g/LBatchWheat straw2:1 (Based on VS)--50Twofold increment in the methane yield (223 L/kg VS) compared to the control (110 L/kg VS).[58]
Gasification biochar12 g/LSemi-continuousEthanol-3.20 g ethanol/L/d-36Methane yield content reached 742 mL CH4/g ethanol.[28]
Biochar10 g/LSemi-continuousKitchen wastes-6.74 g VS/L/d-37Methane production rates were increased by 42% (673.6 mL/d vs. 956.8 mL/d).[30]
Activated carbon5, 10 g/LBatchFood waste and fruit-vegetable waste1:120.90 g VS/L7.037Methane yield and shortest lag phase were observed in 5 g/L PAC and 10 g/L PAC group, 22.0% higher and 62.5% shorter than that without activated carbon supplementation, respectively.[25]
Granular Activated carbon15 g/LBatchLiquid of swine effluent1.65:16.83 g VS/L-40The methane production rates increased by 11.5% in relation to the controls.[24]
Raw fractions of swine effluent7.27:13.03 g VS/L-40The methane production rates increased by 37.8% in relation to the controls.
Granular activated carbon10 g/LBatchWaste activated sludg1:919.60 g VS/L7.035The methane yields of raw sludge were reduced by 6.5–36.9%; the lag phases of methanogenesis were shortened by 19.3–30.6%.[20]
Graphite felt Semi-continuousSyntrophic metabolism of propionate and butyrate-5.00 g COD/L7.037The final average CH4 production rate increased by 19.1% and 16.7%, respectively.[43]
Graphite0.75 g/LBatchCow manure2.02:1-7.3–7.535The accumulative biogas production increased by 18.61%.[40]
1 g/LFood waste1.66:135The accumulative biogas production increased by 19.75%.
1.5 g/LFood waste and cow manure1.89:135Maximum biogas production was 1471.1 mL/g VS; the accumulative biogas production was increased by 7.5%.
Graphene3 × 6 cmBatchSwine manure4.5:155.60 g VS/L7.2–7.538The biogas yield was 356.49 m3/t dry swine manure and the methane yield was 222.17 m3/t dry swine manure: these are 41.49% and 60.89% higher than those of the control group, respectively.[47]
Graphene0.5 g/LBatchCoal gasification
wastewater		-2.50 g COD/L7.5 ± 0.136Methane production rate achieved 64.7% and 180.5 mL/d, respectively.[44]
Activated carbon10 g/LMethane production rate achieved 54.2% and 162.1 mL/d, respectively.
Graphene1.0 g/LBatchEthanol1:1008.33 mL/L7.5 ± 0.135The highest biomethane yield was 695.0 ± 9.1 mL/g and production rates were 95.7 ± 7.6 mL/g/d.[45]
Carbon cloth5 piecesContinuousHigh-strength brewery wastewater-1.00–10.00 g COD/L7.835The COD removal efficiency reached 98%.[33]
Carbon cloth10 pieces (10 × 6 cm)Semi-continuousOrganic wastewater-10.00 g COD/L/d6.5 ± 0.535Methane yield increased by 200–260%.[32]
Carbon nanomaterials500 mg/KgBatchSheep manure-- 35The daily and accumulative production of methane increased by approximately 46.8% and 33.6%, and the total solid content decreased by approximately 12.8% and 10.4%.[52]
Carbon nanotubes1 g/LBatchAcetolactic10:120.00 mmol/L-37Cumulative methane production tripled with virtually no observed lag phase.[49]
5 g/L17-fold increase in initial methane yield and 1.5-fold increase in conversion of butyrate to methane.
Carbon nanotubes1.5 g/LContinuousBeet Sugar Industrial Wastewater-186.00 mg VS/L6.9 ± 0.236Cumulative biogas production increased by 12.6%.[51]
Carbon fiber93% carbon contentBatchEthanol1:81.50–3.00 kg/(m3·day)7.0–8.535Maximum methane production rate increased by 40%.[39]
Magnetic biochar1 g/LBatchWaste activated sludge1:4--35Methane yield reached 208.7 mL/g volatile suspended solids, increasing by 22.1% compared to that in control.[53]

3.2. Enhanced AD by Iron-Based Conductive Materials via DIET

Most studies have identified that iron-based conductive materials could stimulate DIET, based on the shortening of lag times and the increase in the methane formation rate. These conductive materials include magnetite, Fe3O4, hematite, Fe2O3, goethite, and zero-valent iron (ZVI) [6]. Iron-based conductive materials have reducibility, high conductivity, magnetism, excellent specific surface area, and high economic efficiency. They can form a symbiosis between bacteria and archaea to stimulate DIET and improve the efficiency of AD and methanogenic performance [6]. Table 2 summarizes the effects of iron-based conductive materials on anaerobic digestion of different substrates.

3.2.1. Magnetite and Fe3O4

Fe3O4 has been widely used in AD with excellent magnetic properties, electrical conductivity, and specific surface area [59]. Low redox potential can establish a reduced anaerobic microenvironment and enhance methanogenic performance [60]. Meanwhile, iron ions can be released in the presence of Fe3O4 [61,62,63] and act as nutrient for anaerobic microorganisms to increase their methane production and reduce the lag time. Xiang et al. [61] found that biogas production increased by 24.44% with a supplementation of 0.5 g/L Fe3O4. Noonari et al. [62] carried out AD with 0.81 mg and 0.5 mg of magnetite nanoparticles; the maximum methane yields were 256.0 mL/gVS and 202.3 mL/gVS, respectively. In addition to releasing iron ions, Fe3O4 can stimulate the growth of microorganisms, alter the pathway of methane production [64,65], establish DIET, and improve the efficiency of electron transfer [66]. The study by Lu et al. [64] found that the addition of 75 mmol Fe3O4 increased cumulative methane production by 11.06%, based on precipitation of iron–sulphur and the enrichment of Methanosarcina and Methanobrevibacter. In addition, magnetite can promote the formation and utilization of VFAs, reduce acid inhibition, and significantly accelerate IET among acid-forming bacteria, methanogenic bacteria, and other synergistic microorganisms [67,68]. However, when mediated by Fe3O4, the DIET mechanism is different than when it is mediated by other non-bioconductive materials [69,70]. Most studies have shown that Fe3O4 acta as an electron catheter rather than an electron receptor [16,71,72].

3.2.2. Hematite and Fe2O3

Fe2O3, a magnetic semi-conductor material, has excellent specific surface area and good catalytic performance, which can increase methane production. Fe3O4- and Fe2O3-simulated DIET appear to be similar in AD reactors, including the release of iron ions and the stimulation of bacteria and enzyme activity. Farghali et al. [73] found that methane yields improved by 39.36% with 500 mg/L nano Fe2O3. In addition, methane content was increased and H2S content was decreased through the formation of FeS and S0. However, Lu et al. [64] found that Fe2O3 enhanced methane production mainly though the acceleration of electron transfer via DIET, rather than acting as a nutrient. Based on the extracellular polymeric substance that stores electroactive substances, which can be improved by Fe2O3, reduced Fe(Ⅲ) became an electron acceptor for methanogens [74]; additionally, IET was promoted among methanogens and the rate of the methanation process increased. A study using an inanaerobic reactor supplied with swine manure which is enriched with Methanobrecibacter, Methanosarcina, and Methanosphaera proved the DIET capability of Fe2O3 [64].

3.2.3. Goethite

Most studies have demonstrated that supplementation with goethite can effectively improve AD performance and significantly affect methane production and the bacterial communities present [75]. The reason that goethite can promote AD performance varies from study to study. Fe2+ produced through the reduction in goethite enhanced the activity of methanogens and increased methane yield to 263.00 ± 5.00 mL/g VS [76] in goethite incubations with algae; here, soluble Fe2+ can be used as microbial nutrient [77]. Goethite can potentially also act as a biocatalyst for boosting methane production. Yue et al. [77] used algae as a substrate; here, the productions of biogas and methane were increased by 16.1% and 24.1%, respectively. In these studies, the same speculation was raised that DIET was the main reason for the acceleration of the AD process. The electrical conductivity of goethite can promote the synthetic trophic effect of fatty acid oxidizing bacteria and methanogenic archaea, and then promote the electron transfer rate through DIET [76]. Goethite can also enrich functional microorganisms, which is the reason for enhancing the electron transfer rate and extracellular electron transfer capacity. The high electron-donating capacity of goethite may be a key factor in the growth of Pseudomonas, which can interact with Methanosarcina via DIET [75].

3.2.4. Zero-Valent Iron

Zero-value iron (ZVI) is a type of low-cost and long-life-conductive material, and its effectiveness and feasibility in AD of solid waste has been extensively demonstrated. When adding 10 g/L ZVI to the system of food waste, the maximum methane production reached 778.2 mL/g VS [78]. ZVI can affect the growth of microorganism, thereby increasing methane production and the degradation rate of organic matter [79]. (1) ZVI can reduce the redox potential and increase enzyme activity to create more favourable conditions for methanogens; (2) ZVI can promote the conversion of butyrate and propionate to acetate, effectively inhibiting the excessive acidification of the system, and increasing the rate of methane production. Most studies have attributed this positive effect of ZVI to the promotion of IHT by reducing hydrogen partial pressure [78]. Zhu et al. [78] found that IHT was not sufficient in overcoming acid inhibition under high organic loading; they also found that ZVI acted as an electron bridge in DIET. When 10 g/L ZVI was added to AD based on food waste, the abundance of electroactive bacteria (such as Methanosarcina) was increased, in which ZVI formed DIET to serve as a conductive medium linking the exchange of electrons between microorganisms. As noted previously, ZVI played a double role [80].
Table 2. Effects of iron-based conductive materials on anaerobic digestion of different substrates.
Table 2. Effects of iron-based conductive materials on anaerobic digestion of different substrates.
Iron-Based Conductive MaterialsAD
Mode		AD SubstrateInoculum Ratio (Substrate: Inoculum)Organic LoadpHTemperature
(°C)		Effect on AD PerformanceReferences
TypeDosageSize
Nano Fe3O41.5 g/L-ContinuousBeet Sugar Industrial Wastewater-186.00 mg VS/L6.9 ± 0.236Generated 12.6% more mL/g VS CH4 than the control reactor.[51]
Fe2O375 mmol-BatchSwine manure3:1--37The accumulative methane production improved by a maximum of 11.06%.[64]
Nano Fe3O40.5 g/L20 nmSemi-continuousSludge-31.80 g/L7.37–7.8135Biogas production increased by 24.44%.[61]
Nano Fe3O440 mg/L-Batchcabbage 3.2:114.56 g VS/L-37Biomethane production was enhanced by 123%.[81]
40 mg/LcabbageBiomethane production was enhanced by 79%.
60 mg/Lcauliflower biowaste4.8:121.86 g VS/LBiomethane production was enhanced by 138%.
60 mg/Lcauliflower biowasteBiomethane production was enhanced by 106%.
Nano Fe3O420 mg/L-BatchManure2:1--37The highest specific biogas and methane production were 584 mL biogas/g VS and 351.8 mL CH4 g/VS, respectively, compared with the control which yielded only 352.6 mL biogas/g VS and 179.6 mL CH4 g/VS.[63]
Nano Fe2O3100 mg/L20–40 nmBatchCattle manure1:315.50 mL/L-38Methane yields improved by 19.74%.[73]
500 mg/LMethane yields improved by 18.14%.
1000 mg/LMethane yields improved by 21.11%.
85%Fe3O4100 mg/LMethane yields improved by 36.99%.
500 mg/LMethane yields improved by 39.36%.
1000 mg/LMethane yields improved by 56.89%.
Nano Fe3O42.20 mg/L-Continuousbanana plant wastes and buffalo dung-12.50 g VS/L6.8–7.637The highest methane yield was increased by 33.0%.[62]
1.25 mg/Lcanola straw and buffalo dungThe highest methane yield was increased by 39.4%.
Nano Fe3O4100 mg/L20–30 nmBatchWaste sludge1:17.40 g VS/L7.036Hydrogen yield was 11.9 mL/g and methane yield was 109.8 mL CH4/g, which increased by 15.1% and 58.7%, respectively, compared with those of the control.[68]
Nano Fe3O420 mg/L15–20 nmBatchdairy manure and corn stover2.5:1147.65 g VS/L6.7–9.535The methane yield was 191.2 L/kg VS.[82]
Magnetite1.5 g/L-BatchGlycerol2.5:17.50 g COD/L7.5 ± 0.1376% increase in CH4 production compared to the control.[65]
Nano Fe3O410 g/L-BatchSynthetic wastewater1:22.00 g COD/L-35The maximum methane production rate increased by 78.3%.[83]
Nano Magnetite2.5 g/L-BatchWastewater39:1--35The maximum CH4 production rate was increased 2.3 ± 0.3-fold accompanied by an almost delay-free start-up.[84]
Goethite20 mM<200 nmBatchBlue-algae biomass10:110.00 gVS/L7.0 ± 0.135The methane yield reached 263 ± 5 mL/g VS.[76]
Goethite20 mM-ContinuousBlue-algae biomass-0.50 g VS/L/d7.0 ± 0.135Biogas and methane production was increased by 16.1% and 24.1%, respectively.[77]
Zero-valent iron10 g/L-Semi-continuousFood wastes-7.44 g VS/L/d7.2–7.537The maximum methane production was 778.2 mL/g VS.[78]

4. Conclusions

Carbon-based conductive materials such as biochar, activated carbon, carbon cloth, and carbon fiber mostly tend to have small particle size, large specific surface area, and high conductivity. They provide a more stable anaerobic environment, immobilize microbials, and act as electronic conductors or electronic conduits to establish DIET. The optimum dosage of biochar and activated carbon is 10–15 g/L; here, biochar can increase the maximum methane production by 23.5–47.1% and can increase the cumulative methane production by 13.3–32.5%. Activated carbon can increase the methane production rate by 11.5–37.8%, increase the cumulative methane production by 62.5%, and shorten the methane lag time by 19.3–30.6%. Although nanomaterials such as graphite, graphene, and carbon nanotubes are toxic to microorganisms, their special structure, high electrical conductivity, and enrichment for microorganisms can increase methane production with appropriate concentrations. The principle of iron-based conductive materials promoting AD is different from carbon-based materials and nanomaterials. In addition to creating a reducing anaerobic environment, it can also release iron ions as microbial nutrients and further promote microbial growth. Simultaneously, high electrical conductivity and good catalytic properties of magnetism enable iron-based materials to mediate DIET as electron conductors. The cumulative methane production can be increased by 79–138% with the addition of 40–60 mg/L Fe3O4; the methane yield can be increased by 19.74–21.11% with the addition of 0.1–1.5 g/L Fe2O3; the methane yield can be increased by 36% and the cumulative biogas and methane yields can be increased by 16.1% and 27.1%, respectively, with the addition of 20 mM goethite. The dosage and characteristics of conductive materials determine the cost. Among carbon-based conductive materials, activated carbon and biochar are more suitable for large-scale applications; magnetite and hematite are more stable and economical than zero-valent iron among iron-based conductive materials. However, the research of conductive materials for AD is still at an early stage, and further research and development are required. The main issues remaining are as follows: (1) It is difficult to distinguish the relative contribution of DIET mechanism to AD. (2) Few microbiota are known to be applicable in DIET. (3) Further research is necessary on the effect and recycling method of conductive materials in practical engineering. (4) The mechanism of DIET has not yet been identified. Therefore, future research should focus on establishing a quantitative relationship evaluation system between electron transfer efficiency and performance of AD, identifying microbial flora with DIET potential, finding the most suitable method of engineering application, increasing recovery efficiency, and revealing the principle of conductive materials to mediate DIET.

Author Contributions

Data curation, T.K.; formal analysis, T.K.; methodology, T.K.; writing—original draft, T.K.; resources, T.K.; investigation, W.Z.; supervision, W.Z.; validation, W.Z.; writing—review and editing, W.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Science and Technology Project of Shenyang Bureau of Science and Technology grant number [NO. 22-322-3-16] and Science, Technology Project of Department of Science and Technology of Liaoning Province [NO. 2023JH2/101600010] and Scientific Research Program of Department of Education of Liaoning Province [NO. LJKZ0215]. And The APC was funded by [NO. 2023JH2/101600010].

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to privacy.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kang, H.-J.; Lee, S.-H.; Lim, T.-G.; Park, J.-H.; Kim, B.; Buffière, P.; Park, H.-D. Recent advances in methanogenesis through direct interspecies electron transfer via conductive materials: A molecular microbiological perspective. Bioresour. Technol. 2021, 322, 124587. [Google Scholar] [CrossRef] [PubMed]
  2. Gahlot, P.; Ahmed, B.; Tiwari, S.B.; Aryal, N.; Khursheed, A.; Kazmi, A.A.; Tyagi, V.K. Conductive material engineered direct interspecies electron transfer (DIET) in anaerobic digestion: Mechanism and application. Environ. Technol. Innov. 2020, 20, 101056. [Google Scholar] [CrossRef]
  3. Kundu, R.; Kunnoth, B.; Pilli, S.; Polisetty, V.R.; Tyagi, R.D. Biochar symbiosis in anaerobic digestion to enhance biogas production: A comprehensive review. J. Environ. Manag. 2023, 344, 118743. [Google Scholar] [CrossRef] [PubMed]
  4. Chen, Y.; Cheng, J.J.; Creamer, K.S. Inhibition of anaerobic digestion process: A review. Bioresour. Technol. 2008, 99, 4044–4064. [Google Scholar] [CrossRef]
  5. Yin, Q.; Gu, M.; Wu, G. Inhibition mitigation of methanogenesis processes by conductive materials: A critical review. Bioresour. Technol. 2020, 317, 123977. [Google Scholar] [CrossRef]
  6. Ajay, C.M.; Mohan, S.; Dinesha, P.; Rosen, M.A. Review of impact of nanoparticle additives on anaerobic digestion and methane generation. Fuel 2020, 277, 118234. [Google Scholar] [CrossRef]
  7. Wang, W.; Lee, D.J. Direct interspecies electron transfer mechanism in enhanced methanogenesis: A mini-review. Bioresour. Technol. 2021, 330, 124980. [Google Scholar] [CrossRef]
  8. Kunatsa, T.; Xia, X. A review on anaerobic digestion with focus on the role of biomass co-digestion, modelling and optimisation on biogas production and enhancement. Bioresour. Technol. 2022, 344, 126311. [Google Scholar] [CrossRef]
  9. Xu, H.; Chang, J.; Wang, H.; Liu, Y.; Zhang, X.; Liang, P.; Huang, X. Enhancing direct interspecies electron transfer in syntrophic-methanogenic associations with (semi)conductive iron oxides: Effects and mechanisms. Sci. Total Environ. 2019, 695, 133876. [Google Scholar] [CrossRef]
  10. Bryant, M.P. Microbial methane production—Theoretical aspects. J. Anim. Sci. 1979, 48, 193–201. [Google Scholar] [CrossRef]
  11. Yin, Q.; Wu, G. Advances in direct interspecies electron transfer and conductive materials: Electron flux, organic degradation and microbial interaction. Biotechnol. Adv. 2019, 37, 107443. [Google Scholar] [CrossRef] [PubMed]
  12. Summers, Z.M.; Fogarty, H.E.; Leang, C.; Franks, A.E.; Malvankar, N.S.; Lovley, D.R. Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 2010, 330, 1413–1415. [Google Scholar] [CrossRef] [PubMed]
  13. Rotaru, A.-E.; Shrestha, P.M.; Liu, F.; Markovaite, B.; Chen, S.; Nevin, K.P.; Lovley, D.R.; Voordouw, G. Direct Interspecies Electron Transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl. Environ. Microbiol. 2014, 80, 4599–4605. [Google Scholar] [CrossRef] [PubMed]
  14. Reguera, G.; McCarthy, K.D.; Mehta, T.; Nicoll, J.S.; Tuominen, M.T.; Lovley, D.R. Extracellular electron transfer via microbial nanowires. Nature 2005, 435, 1098–1101. [Google Scholar] [CrossRef]
  15. Holmes, D.E.; Shrestha, P.M.; Walker, D.J.F.; Dang, Y.; Nevin, K.P.; Woodard, T.L.; Lovley, D.R. Metatranscriptomic Evidence for Direct Interspecies Electron Transfer between Geobacter and Methanothrix Species in Methanogenic Rice Paddy Soils. Appl. Environ. Microbiol. 2017, 83, e00223-17. [Google Scholar] [CrossRef]
  16. Kato, S.; Hashimoto, K.; Watanabe, K. Methanogenesis facilitated by electric syntrophy via (semi)conductive iron-oxide minerals. Environ. Microbiol. 2012, 14, 1646–1654. [Google Scholar] [CrossRef]
  17. Rotaru, A.-E.; Shrestha, P.M.; Liu, F.; Shrestha, M.; Shrestha, D.; Embree, M.; Zengler, K.; Wardman, C.; Nevin, K.P.; Lovley, D.R. A new model for electron flow during anaerobic digestion: Direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energy Environ. Sci. 2014, 7, 408–415. [Google Scholar] [CrossRef]
  18. Zhao, Z.; Zhang, Y.; Li, Y.; Dang, Y.; Zhu, T.; Quan, X. Potentially shifting from interspecies hydrogen transfer to direct interspecies electron transfer for syntrophic metabolism to resist acidic impact with conductive carbon cloth. Chem. Eng. J. 2017, 313, 10–18. [Google Scholar] [CrossRef]
  19. Hassanein, A.; Naresh Kumar, A.; Lansing, S. Impact of electro-conductive nanoparticles additives on anaerobic digestion performance—A review. Bioresour. Technol. 2021, 342, 126023. [Google Scholar] [CrossRef]
  20. Jiang, Q.; Liu, H.; Zhang, Y.; Cui, M.H.; Fu, B.; Liu, H.B. Insight into sludge anaerobic digestion with granular activated carbon addition: Methanogenic acceleration and methane reduction relief. Bioresour. Technol. 2021, 319, 124131. [Google Scholar] [CrossRef]
  21. Zhang, J.; Tian, H.; Wang, X.; Tong, Y.W. Effects of activated carbon on mesophilic and thermophilic anaerobic digestion of food waste: Process performance and life cycle assessment. Chem. Eng. J. 2020, 399, 125757. [Google Scholar] [CrossRef]
  22. Dastyar, W.; Mirsoleimani Azizi, S.M.; Meshref, M.N.A.; Dhar, B.R. Powdered activated carbon amendment in percolate tank enhances high-solids anaerobic digestion of organic fraction of municipal solid waste. Process Saf. Environ. Prot. 2021, 151, 63–70. [Google Scholar] [CrossRef]
  23. Tan, L.C.; Lin, R.; Murphy, J.D.; Lens, P.N.L. Granular activated carbon supplementation enhances anaerobic digestion of lipid-rich wastewaters. Renew. Energy 2021, 171, 958–970. [Google Scholar] [CrossRef]
  24. Romero, R.M.; Valenzuela, E.I.; Cervantes, F.J.; Garcia-Reyes, R.B.; Serrano, D.; Alvarez, L.H. Improved methane production from anaerobic digestion of liquid and raw fractions of swine manure effluent using activated carbon. J. Water Process Eng. 2020, 38, 101576. [Google Scholar] [CrossRef]
  25. Ma, J.; Wei, H.; Su, Y.; Gu, W.; Wang, B.; Xie, B. Powdered activated carbon facilitates methane productivity of anaerobic co-digestion via acidification alleviating: Microbial and metabolic insights. Bioresour. Technol. 2020, 313, 123706. [Google Scholar] [CrossRef]
  26. Wang, G.; Gao, X.; Li, Q.; Zhao, H.; Liu, Y.; Wang, X.C.; Chen, R. Redox-based electron exchange capacity of biowaste-derived biochar accelerates syntrophic phenol oxidation for methanogenesis via direct interspecies electron transfer. J. Hazard. Mater. 2020, 390, 121726. [Google Scholar] [CrossRef]
  27. Lü, F.; Liu, Y.; Shao, L.; He, P. Powdered biochar doubled microbial growth in anaerobic digestion of oil. Appl. Energy 2019, 247, 605–614. [Google Scholar] [CrossRef]
  28. Qi, Q.; Sun, C.; Cristhian, C.; Zhang, T.; Zhang, J.; Tian, H.; He, Y.; Tong, Y.W. Enhancement of methanogenic performance by gasification biochar on anaerobic digestion. Bioresour. Technol. 2021, 330, 124993. [Google Scholar] [CrossRef]
  29. Lu, F.; Luo, C.; Shao, L.; He, P. Biochar alleviates combined stress of ammonium and acids by firstly enriching Methanosaeta and then Methanosarcina. Water Res. 2016, 90, 34–43. [Google Scholar] [CrossRef]
  30. Wang, J.; Zhao, Z.; Zhang, Y. Enhancing anaerobic digestion of kitchen wastes with biochar: Link between different properties and critical mechanisms of promoting interspecies electron transfer. Renew. Energy 2021, 167, 791–799. [Google Scholar] [CrossRef]
  31. Feng, D.; Xia, A.; Huang, Y.; Zhu, X.; Zhu, X.; Liao, Q. Effects of carbon cloth on anaerobic digestion of high concentration organic wastewater under various mixing conditions. J. Hazard. Mater. 2022, 423, 127100. [Google Scholar] [CrossRef] [PubMed]
  32. Feng, D.; Xia, A.; Liao, Q.; Nizami, A.S.; Sun, C.; Huang, Y.; Zhu, X.; Zhu, X. Carbon cloth facilitates semi-continuous anaerobic digestion of organic wastewater rich in volatile fatty acids from dark fermentation. Environ. Pollut. 2021, 272, 116030. [Google Scholar] [CrossRef] [PubMed]
  33. Jia, R.; Sun, D.; Dang, Y.; Meier, D.; Holmes, D.E.; Smith, J.A. Carbon cloth enhances treatment of high-strength brewery wastewater in anaerobic dynamic membrane bioreactors. Bioresour. Technol. 2020, 298, 122547. [Google Scholar] [CrossRef] [PubMed]
  34. Chen, S.; Rotaru, A.E.; Liu, F.; Philips, J.; Woodard, T.L.; Nevin, K.P.; Lovley, D.R. Carbon cloth stimulates direct interspecies electron transfer in syntrophic co-cultures. Bioresour. Technol. 2014, 173, 82–86. [Google Scholar] [CrossRef]
  35. Dang, Y.; Holmes, D.E.; Zhao, Z.; Woodard, T.L.; Zhang, Y.; Sun, D.; Wang, L.Y.; Nevin, K.P.; Lovley, D.R. Enhancing anaerobic digestion of complex organic waste with carbon-based conductive materials. Bioresour. Technol. 2016, 220, 516–522. [Google Scholar] [CrossRef] [PubMed]
  36. Baek, G.; Saikaly, P.E.; Logan, B.E. Addition of a carbon fiber brush improves anaerobic digestion compared to external voltage application. Water Res. 2021, 188, 116575. [Google Scholar] [CrossRef] [PubMed]
  37. Logan, B.; Cheng, S.; Watson, V.; Estadt, G. Graphite Fiber Brush Anodes for Increased Power Production in Air-Cathode Microbial Fuel Cells. Environ. Sci. Technol. 2007, 41, 9. [Google Scholar] [CrossRef]
  38. Barua, S.; Zakaria, B.S.; Dhar, B.R. Enhanced methanogenic co-degradation of propionate and butyrate by anaerobic microbiome enriched on conductive carbon fibers. Bioresour. Technol. 2018, 266, 259–266. [Google Scholar] [CrossRef]
  39. Du, J.; Gu, M.; Yin, Q.; Wu, G. Temporary addition of carbon fibers facilitates methanogenic degradation of ethanol during anaerobic treatment. Sci. Total Environ. 2021, 765, 142724. [Google Scholar] [CrossRef]
  40. Muratcobanoglu, H.; Gokcek, O.B.; Mert, R.A.; Zan, R.; Demirel, S. Simultaneous synergistic effects of graphite addition and co-digestion of food waste and cow manure: Biogas production and microbial community. Bioresour. Technol. 2020, 309, 123365. [Google Scholar] [CrossRef]
  41. Wang, P.; Zheng, Y.; Lin, P.; Li, J.; Dong, H.; Yu, H.; Qi, L.; Ren, L. Effects of graphite, graphene, and graphene oxide on the anaerobic co-digestion of sewage sludge and food waste: Attention to methane production and the fate of antibiotic resistance genes. Bioresour. Technol. 2021, 339, 125585. [Google Scholar] [CrossRef] [PubMed]
  42. Zhao, Z.; Zhang, Y.; Woodard, T.L.; Nevin, K.P.; Lovley, D.R. Enhancing syntrophic metabolism in up-flow anaerobic sludge blanket reactors with conductive carbon materials. Bioresour. Technol. 2015, 191, 140–145. [Google Scholar] [CrossRef] [PubMed]
  43. Zhang, M.; Ma, Y.; Ji, D.; Li, X.; Zhang, J.; Zang, L. Synergetic promotion of direct interspecies electron transfer for syntrophic metabolism of propionate and butyrate with graphite felt in anaerobic digestion. Bioresour. Technol. 2019, 287, 121373. [Google Scholar] [CrossRef] [PubMed]
  44. Zhu, H.; Han, Y.; Ma, W.; Han, H.; Ma, W.; Xu, C. New insights into enhanced anaerobic degradation of coal gasification wastewater (CGW) with the assistance of graphene. Bioresour. Technol. 2018, 262, 302–309. [Google Scholar] [CrossRef]
  45. Lin, R.; Cheng, J.; Zhang, J.; Zhou, J.; Cen, K.; Murphy, J.D. Boosting biomethane yield and production rate with graphene: The potential of direct interspecies electron transfer in anaerobic digestion. Bioresour. Technol. 2017, 239, 345–352. [Google Scholar] [CrossRef]
  46. Lin, R.; Deng, C.; Cheng, J.; Xia, A.; Lens, P.N.L.; Jackson, S.A.; Dobson, A.D.W.; Murphy, J.D. Graphene Facilitates Biomethane Production from Protein-Derived Glycine in Anaerobic Digestion. iScience 2018, 10, 158–170. [Google Scholar] [CrossRef]
  47. Liu, Y.; Li, Y.; Gan, R.; Jia, H.; Yong, X.; Yong, Y.-C.; Wu, X.; Wei, P.; Zhou, J. Enhanced biogas production from swine manure anaerobic digestion via in-situ formed graphene in electromethanogenesis system. Chem. Eng. J. 2020, 389, 124510. [Google Scholar] [CrossRef]
  48. Tian, T.; Qiao, S.; Li, X.; Zhang, M.; Zhou, J. Nano-graphene induced positive effects on methanogenesis in anaerobic digestion. Bioresour. Technol. 2017, 224, 41–47. [Google Scholar] [CrossRef]
  49. Salvador, A.F.; Martins, G.; Melle-Franco, M.; Serpa, R.; Stams, A.J.M.; Cavaleiro, A.J.; Pereira, M.A.; Alves, M.M. Carbon nanotubes accelerate methane production in pure cultures of methanogens and in a syntrophic coculture. Environ. Microbiol. 2017, 19, 2727–2739. [Google Scholar] [CrossRef]
  50. Yan, W.; Lu, D.; Liu, J.; Zhou, Y. The interactive effects of ammonia and carbon nanotube on anaerobic digestion. Chem. Eng. J. 2019, 372, 332–340. [Google Scholar] [CrossRef]
  51. Ambuchi, J.J.; Zhang, Z.; Shan, L.; Liang, D.; Zhang, P.; Feng, Y. Response of anaerobic granular sludge to iron oxide nanoparticles and multi-wall carbon nanotubes during beet sugar industrial wastewater treatment. Water Res. 2017, 117, 87–94. [Google Scholar] [CrossRef]
  52. Hao, Y.; Wang, Y.; Ma, C.; White, J.C.; Zhao, Z.; Duan, C.; Zhang, Y.; Adeel, M.; Rui, Y.; Li, G.; et al. Carbon nanomaterials induce residue degradation and increase methane production from livestock manure in an anaerobic digestion system. J. Clean. Prod. 2019, 240, 118257. [Google Scholar] [CrossRef]
  53. Jin, H.-Y.; Yang, L.; Ren, Y.-X.; Tang, C.-C.; Zhou, A.-J.; Liu, W.; Li, Z.; Wang, A.; He, Z.-W. Insights into the roles and mechanisms of a green-prepared magnetic biochar in anaerobic digestion of waste activated sludge. Sci. Total Environ. 2023, 896, 165170. [Google Scholar] [CrossRef] [PubMed]
  54. Ruan, R.; Wu, H.; Yu, C.; Zhao, C.; Zhou, D.; Shi, X.; Cao, J.; Huang, B.; Luo, J. Impacts of magnetic biochar from reed straw on anaerobic digestion of pigment sludge: Biomethane production and the transformation of heavy metals speciation. Process Biochem. 2023, 125, 96–103. [Google Scholar] [CrossRef]
  55. Ni, Z.; Zhou, L.; Lin, Z.; Kuang, B.; Zhu, G.; Jia, J.; Wang, T. Iron-modified biochar boosts anaerobic digestion of sulfamethoxazole pharmaceutical wastewater: Performance and microbial mechanism. J. Hazard. Mater. 2023, 452, 131314. [Google Scholar] [CrossRef]
  56. Zhang, J.; Cui, Y.; Zhang, T.; Hu, Q.; Wah Tong, Y.; He, Y.; Dai, Y.; Wang, C.H.; Peng, Y. Food waste treating by biochar-assisted high-solid anaerobic digestion coupled with steam gasification: Enhanced bioenergy generation and porous biochar production. Bioresour. Technol. 2021, 331, 125051. [Google Scholar] [CrossRef] [PubMed]
  57. Pan, J.; Ma, J.; Liu, X.; Zhai, L.; Ouyang, X.; Liu, H. Effects of different types of biochar on the anaerobic digestion of chicken manure. Bioresour. Technol. 2018, 275, 258–265. [Google Scholar] [CrossRef]
  58. Paritosh, K.; Vivekanand, V. Biochar enabled syntrophic action: Solid state anaerobic digestion of agricultural stubble for enhanced methane production. Bioresour. Technol. 2019, 289, 121712. [Google Scholar] [CrossRef]
  59. Di, L.; Wang, F.; Li, S.; Wang, H.; Zhang, D.; Yi, W.; Shen, X. Influence of nano-Fe3O4 biochar on the methanation pathway during anaerobic digestion of chicken manure. Bioresour. Technol. 2023, 377, 128979. [Google Scholar] [CrossRef]
  60. Wang, D.; Han, Y.; Han, H.; Li, K.; Xu, C.; Zhuang, H. New insights into enhanced anaerobic degradation of Fischer-Tropsch wastewater with the assistance of magnetite. Bioresour. Technol. 2018, 257, 147–156. [Google Scholar] [CrossRef]
  61. Xiang, Y.; Yang, Z.; Zhang, Y.; Xu, R.; Zheng, Y.; Hu, J.; Li, X.; Jia, M.; Xiong, W.; Cao, J. Influence of nanoscale zero-valent iron and magnetite nanoparticles on anaerobic digestion performance and macrolide, aminoglycoside, beta-lactam resistance genes reduction. Bioresour. Technol. 2019, 294, 122139. [Google Scholar] [CrossRef] [PubMed]
  62. Noonari, A.A.; Mahar, R.B.; Sahito, A.R.; Brohi, K.M. Anaerobic co-digestion of canola straw and banana plant wastes with buffalo dung: Effect of Fe3O4 nanoparticles on methane yield. Renew. Energy 2019, 133, 1046–1054. [Google Scholar] [CrossRef]
  63. Abdelsalam, E.; Samer, M.; Attia, Y.A.; Abdel-Hadi, M.A.; Hassan, H.E.; Badr, Y. Influence of zero valent iron nanoparticles and magnetic iron oxide nanoparticles on biogas and methane production from anaerobic digestion of manure. Energy 2017, 120, 842–853. [Google Scholar] [CrossRef]
  64. Lu, T.; Zhang, J.; Wei, Y.; Shen, P. Effects of ferric oxide on the microbial community and functioning during anaerobic digestion of swine manure. Bioresour. Technol. 2019, 287, 121393. [Google Scholar] [CrossRef] [PubMed]
  65. Im, S.; Yun, Y.-M.; Song, Y.-C.; Kim, D.-H. Enhanced anaerobic digestion of glycerol by promoting DIET reaction. Biochem. Eng. J. 2019, 142, 18–26. [Google Scholar] [CrossRef]
  66. Qiu, C.; Feng, Y.; Wu, M.; Liu, M.; Li, W.; Li, Z. NanoFe3O4 accelerates methanogenic straw degradation by improving energy metabolism. Bioresour. Technol. 2019, 292, 121930. [Google Scholar] [CrossRef]
  67. Lu, X.; Wang, H.; Ma, F.; Zhao, G.; Wang, S. Improved process performance of the acidification phase in a two-stage anaerobic digestion of complex organic waste: Effects of an iron oxide-zeolite additive. Bioresour. Technol. 2018, 262, 169–176. [Google Scholar] [CrossRef]
  68. Zhang, Z.; Guo, L.; Wang, Y.; Zhao, Y.; She, Z.; Gao, M.; Guo, Y. Application of iron oxide (Fe3O4) nanoparticles during the two-stage anaerobic digestion with waste sludge: Impact on the biogas production and the substrate metabolism. Renew. Energy 2020, 146, 2724–2735. [Google Scholar] [CrossRef]
  69. Baek, G.; Jung, H.; Kim, J.; Lee, C. A long-term study on the effect of magnetite supplementation in continuous anaerobic digestion of dairy effluent—Magnetic separation and recycling of magnetite. Bioresour. Technol. 2017, 241, 830–840. [Google Scholar] [CrossRef]
  70. Liu, F.; Rotaru, A.E.; Shrestha, P.M.; Malvankar, N.S.; Nevin, K.P.; Lovley, D.R. Magnetite compensates for the lack of a pilin-associated c-type cytochrome in extracellular electron exchange. Environ. Microbiol. 2015, 17, 648–655. [Google Scholar] [CrossRef]
  71. Aulenta, F.; Fazi, S.; Majone, M.; Rossetti, S. Electrically conductive magnetite particles enhance the kinetics and steer the composition of anaerobic TCE-dechlorinating cultures. Process Biochem. 2014, 49, 2235–2240. [Google Scholar] [CrossRef]
  72. Lovley, D.R. Reach out and touch someone: Potential impact of DIET (direct interspecies energy transfer) on anaerobic biogeochemistry, bioremediation, and bioenergy. Rev. Environ. Sci. BioTechnol. 2011, 10, 101–105. [Google Scholar] [CrossRef]
  73. Farghali, M.; Andriamanohiarisoamanana, F.J.; Ahmed, M.M.; Kotb, S.; Yamamoto, Y.; Iwasaki, M.; Yamashiro, T.; Umetsu, K. Prospects for biogas production and H2S control from the anaerobic digestion of cattle manure: The influence of microscale waste iron powder and iron oxide nanoparticles. Waste Manag. 2020, 101, 141–149. [Google Scholar] [CrossRef] [PubMed]
  74. Ye, J.; Hu, A.; Ren, G.; Chen, M.; Tang, J.; Zhang, P.; Zhou, S.; He, Z. Enhancing sludge methanogenesis with improved redox activity of extracellular polymeric substances by hematite in red mud. Water Res. 2018, 134, 54–62. [Google Scholar] [CrossRef]
  75. Zhu, M.-Y.; Peng, S.-C.; Tao, W.; Wang, J.; Tang, T.; Chen, T.-H.; Yue, Z.-B. Response of methane production and microbial community to the enrichment of soluble microbial products in goethite-dosed anaerobic reactors. Fuel 2017, 191, 495–499. [Google Scholar] [CrossRef]
  76. Yue, Z.-b.; Ma, D.; Wang, J.; Tan, J.; Peng, S.-C.; Chen, T.-H. Goethite promoted anaerobic digestion of algal biomass in continuous stirring-tank reactors. Fuel 2015, 159, 883–886. [Google Scholar] [CrossRef]
  77. Tan, J.; Wang, J.; Xue, J.; Liu, S.-Y.; Peng, S.-C.; Ma, D.; Chen, T.-H.; Yue, Z. Methane production and microbial community analysis in the goethite facilitated anaerobic reactors using algal biomass. Fuel 2015, 145, 196–201. [Google Scholar]
  78. Zhu, Y.; Zhao, Z.; Yang, Y.; Zhang, Y. Dual roles of zero-valent iron in dry anaerobic digestion: Enhancing interspecies hydrogen transfer and direct interspecies electron transfer. Waste Manag. 2020, 118, 481–490. [Google Scholar] [CrossRef]
  79. Ye, W.; Lu, J.; Ye, J.; Zhou, Y. The effects and mechanisms of zero-valent iron on anaerobic digestion of solid waste: A mini-review. J. Clean. Prod. 2021, 278, 123567. [Google Scholar] [CrossRef]
  80. Yuan, T.; Shi, X.; Sun, R.; Ko, J.H.; Xu, Q. Simultaneous addition of biochar and zero-valent iron to improve food waste anaerobic digestion. J. Clean. Prod. 2021, 278, 123627. [Google Scholar] [CrossRef]
  81. Faisal, S.; Salama, E.-S.; Malik, K.; Lee, S.-h.; Li, X. Anaerobic digestion of cabbage and cauliflower biowaste: Impact of iron oxide nanoparticles (IONPs) on biomethane and microbial communities alteration. Bioresour. Technol. Rep. 2020, 12, 100567. [Google Scholar] [CrossRef]
  82. Ajayi-Banji, A.A.; Rahman, S. Efficacy of magnetite (Fe3O4) nanoparticles for enhancing solid-state anaerobic co-digestion: Focus on reactor performance and retention time. Bioresour. Technol. 2021, 324, 124670. [Google Scholar] [CrossRef] [PubMed]
  83. Yin, Q.; Yang, S.; Wang, Z.; Xing, L.; Wu, G. Clarifying electron transfer and metagenomic analysis of microbial community in the methane production process with the addition of ferroferric oxide. Chem. Eng. J. 2018, 333, 216–225. [Google Scholar] [CrossRef]
  84. Ren, G.; Chen, P.; Yu, J.; Liu, J.; Ye, J.; Zhou, S. Recyclable magnetite-enhanced electromethanogenesis for biomethane production from wastewater. Water Res. 2019, 166, 115095. [Google Scholar] [CrossRef] [PubMed]
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Figure 1. Electron transfer pathways between different species during AD [9].
Figure 1. Electron transfer pathways between different species during AD [9].
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Figure 2. Schematic diagram of MIET [11].
Figure 2. Schematic diagram of MIET [11].
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Figure 3. Schematic diagram of DIET: (a) DIET via conductive pili; (b) DIET via C-type cytochrome; (c) DIET via conductive materials [11].
Figure 3. Schematic diagram of DIET: (a) DIET via conductive pili; (b) DIET via C-type cytochrome; (c) DIET via conductive materials [11].
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Kong, T.; Zhang, W. Enhanced Anaerobic Digestion Using Conductive Materials through Mediation of Direct Microbial Interspecies Electron Transfer: A Review. Fermentation 2023, 9, 884. https://doi.org/10.3390/fermentation9100884

AMA Style

Kong T, Zhang W. Enhanced Anaerobic Digestion Using Conductive Materials through Mediation of Direct Microbial Interspecies Electron Transfer: A Review. Fermentation. 2023; 9(10):884. https://doi.org/10.3390/fermentation9100884

Chicago/Turabian Style

Kong, Tianqi, and Wanli Zhang. 2023. "Enhanced Anaerobic Digestion Using Conductive Materials through Mediation of Direct Microbial Interspecies Electron Transfer: A Review" Fermentation 9, no. 10: 884. https://doi.org/10.3390/fermentation9100884

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