Granular activated carbon (GAC) and GAC modified with anthraquinone-2-sulfonate (AQS) were used as conductive materials during the anaerobic digestion of swine wastewater (SW). The electron transfer capacity (ETC) in the GAC-AQS was 2.1-fold higher than the unmodified GAC. Despite the improvement in the ETC, the GAC-AQS cultures showed an inhibitory effect, evidenced by the lowest methane productivity. Indeed, the cultures with unmodified GAC achieved 236 mL CH4/g CODi (chemical oxygen demand, initial), representing an increment of 1.14- and 2.05-fold compared with the control (without conductive materials) and GAC-AQS, respectively. In addition, the methane production rate (Rmax) and yield were also improved with unmodified GAC, but they decreased with GAC-AQS. The role of solid-phase AQS (GAC-AQS) as a terminal electron acceptor during microbial respiration competes with methanogenesis for the electrons instead of serving as an electron conduit.

  • The electron transfer capacity of GAC was improved by quinone anchorage.

  • Immobilized quinone inhibit methanogenesis due to its role as electron acceptor.

  • GAC improved 2.05-fold the production of methane compared with GAC-AQS.

Alternative energy sources from biotechnological processes have gained significant attention in recent decades (Malik et al. 2024). Anaerobic digestion, the most widely applied environmental biotechnology, offers several advantages for resource recovery, including energy production from organic wastes by its conversion to methane, which can be further used as fuel for vehicles or converted to heat and power (Kleerebezem et al. 2015). The anaerobic digestion of organic wastes occurs in the absence of oxygen through four sequential steps: hydrolysis, acidogenesis, acetogenesis, and methanogenesis, by the syntrophic action of fermentative bacteria and methanogenic archaea (Adekunle & Okolie 2015).

Mediated interspecies electron transfer (MIET) is a syntrophic process between fermentative bacteria and methanogenic archaea, which is a key for the anaerobic degradation of organic substrates and methane production. The main redox mediators reported for methane production in the MIET are hydrogen and formate; other soluble molecules such as sulfide, cystine/cysteine, and quinone/hydroquinone moieties have also been reported for other relevant ecological processes (Lovley 2017). Indeed, it was documented that the model quinone anthraquinone-2,6-disulfonate (AQDS) acts as a redox mediator for the MIET during the syntrophic growth of Geobacter metallireducens and Geobacter sulfurreducens (Smith et al. 2015); nonetheless, it was believed that soluble quinones did not act as redox mediators for methane production. In fact, it was previously documented that the inhibition of methanogenesis occurs with soluble AQDS (5–25 mM), in part due to its role as an electron acceptor, which promotes a competence with methanogenesis for electrons during the anaerobic oxidation of substrates (Cervantes et al. 2000; Alvarez et al. 2015; Palacios et al. 2023). In addition, humic acids, which contain quinone groups, inhibited methanogenesis in different extents under doses of 2–10 g/L, but beneficial results were achieved at doses less than 1 g/L (He et al. 2023). Nevertheless, a recent study documented that soluble AQDS (100 μM) may act as a redox mediator to sustain the MIET for methane production under ammonia (5.0 g -N/L) stress, improving productivity by facilitating the generation and consumption of acetate (Xu et al. 2022).

Direct interspecies electron transfer (DIET) process is an alternative pathway for syntrophic metabolism, in which electron transfer occurs directly from electron donors (i.e., fermentative bacterium) to electron acceptors (i.e., methanogenic archaea) by the action of cell structures as conductive pili and c-type cytochromes with fewer biological enzymatic reactions (Lovley 2017). Solid-phase materials such as carbon- and metallic-based materials have also been documented to act as electron conduits to sustain the DIET, even in the absence of conductive cell structures (Martins et al. 2018). In addition, the contribution of quinone groups located on the surface of carbon-based materials, acting as redox functional groups, has been associated with methane production through the DIET process (Wang et al. 2020). In this sense, it is hypothesized that the chemical modification of GAC with quinone molecules and its use as a solid-phase electron conduit could sustain the DIET, even though it has been observed to inhibit methanogenesis using soluble quinones. Despite the immobilization of quinone molecules and its application as a solid-phase redox mediator has been conducted for the treatment of different recalcitrant pollutants under anaerobic conditions (Martinez et al. 2013), its application for methane production has not been previously studied. The aim of this study was to evaluate the effect of anthraquinone-2-sulfonate (AQS) immobilized on granular activated carbon (GAC) to act as a solid-phase electron conduit for methane production during the anaerobic digestion of swine wastewater (SW).

Wastewater sample and inoculum

SW sample was collected from a finishing farm located in the Yaqui Valley, Mexico. The sample was centrifuged at 3,000 rpm for 5 min to remove a fraction of solids. The SW was analyzed for COD and pH determination using standard methods (APHA 2005). The anaerobic granular sludge used as inoculum was collected from a full-scale up-flow anaerobic sludge blanket (UASB) reactor installed in a local brewery factory. The content of volatile suspended solids (VSS) in the sludge was 9.5% wet weight. Before being inoculated, the sludge was disintegrated with a sieve of 425 μm to promote a high interaction between microorganisms and GAC.

Chemical modification of GAC with AQS

According to the supplier (Carbotecnia, Mexico), the GAC used was produced from bituminous coal. The GAC was sieved to obtain particle sizes between 250 and 450 μm. Then, the particles were water-washed three times to remove the fine powder particles and dried overnight in an oven at 60 °C. A portion of GAC was submerged for 24 h in 100 mL of Lukas reagent, composed of ZnCl2 (100 g/L) dissolved in concentrated HCl, followed by three washed with HCl to remove Zn traces. Then, the GAC-Cl was added to a 2 g/L of AQS solution at pH 7.0, allowing it to react for 24 h in a shaker. The initial and final concentrations of AQS were measured spectrophotometrically at 310 nm to determine the adsorption capacity with Equation (1) (Vences-Alvarez et al. 2022):
(1)
where q is the adsorption capacity (mg/g), Co and Ce are the initial and equilibrium concentration (mg/L) of AQS, V is the volume (L) of AQS solution, and m is the mass (g) of GAC. The modified material (GAC-AQS) was exposed to three desorption cycles with distilled water to evaluate the anchorage strength. The adsorption capacity was determined after each desorption cycle (qd), using the previous adsorption capacity (qe), with Equation (2) (Alvarez et al. 2017):
(2)

Electrons transfer capacity of GAC

Electron transfer capacity (ETC) in GAC-AQS was determined using an anaerobic sludge with a proven capacity to use quinones and humic substances as electron acceptors. The cultures were prepared in triplicate in serum bottles (60 mL) with 10 mL of a basal medium at pH 7 consisted in (g/L): NaHCO3 (3), NH4Cl (0.3), K2HPO4 (0.2), MgCl2·6H2O (0.03), CaCl2 (0.01), and 1 mL/L of trace elements solution composed of (g/L): FeCl2·4H2O (2), H3BO3 (0.05), ZnCl2 (0.05), CuCl2·2H2O (0.038), MnCl2·4H2O (0.5), (NH4)6Mo7O24·4H2O (0.05), AlCl3·6H2O (0.09), CoCl2·6H2O (2), NiCl2·6H2O (0.092), Na2SeO·5H2O (0.162), EDTA (1), and 1 mL/L of HCl (36%). The vials were supplemented with 1 g VSS/L of anaerobic sludge, 2 g/L of glucose as a sole energy source, and 1 g/L of GAC-AQS. Then, the vials were sealed with rubber stoppers and aluminum caps and flushed with N2 to promote anaerobic conditions. Controls with unmodified GAC and without GAC (only anaerobic sludge) were also included. All vials were incubated for 48 h at 150 rpm and 37 °C. The ETC was determined following the ferrozine technique (Lovley et al. 1996). All ETC measurements were corrected for the intrinsic capacity of anaerobic sludge to reduce Fe(III); thus, interference of redox-active molecules from the sludge can be diminished.

Methane production with GAC and GAC-AQS

Methane cultures were prepared in triplicate using serum bottles (60 mL). First, a portion of the SW sample was bubbled with N2 for 10 min to create strictly anaerobic conditions and prevent oxidation of redox functional groups of the two materials. Then, 30 mL of SW was added to the bottles with 10 g/L of GAC or GAC-AQS and 1 g VSS/L of methanogenic sludge. The bottles were hermetically sealed with rubber stoppers and aluminum caps, and the headspace was flushed with N2 to remove the air traces. Controls were also prepared under the same conditions but without materials. The cultures were incubated in an orbital shaker at 37 °C and 110 rpm. Periodically, the methane produced was measured by the liquid displacement method using a 2% w/v NaOH solution, which can act as a barrier for the CO2 and quantify the total volume of methane in the biogas (Casallas-Ojeda et al. 2022). In addition, the initial and final COD concentrations were measured following the standard methods (APHA 2005) to determine the removal and conversion rates. Both methane production and COD removal were statistically evaluated with analysis of variance (ANOVA) and multiple comparisons of means using the Tukey test at 95% confidence level.

Since GAC is the most used adsorbent material (Hu et al. 2024), it was also used to evaluate its capacity to adsorb the organic matter present in the SW and identify possible effects on methane production. The conditions for the adsorption on GAC and GAC-AQS (in triplicated) were similar to the methanogenic cultures but without inoculum; even so, the bottles were analyzed to verify that methane was not produced due to the possible presence of microorganisms from the SW. The adsorption was conducted for 48 h until the equilibrium was reached, and then, the adsorption capacity was determined using Equation (1).

Kinetics model for methane production

Experimental data from methane production assays were used to obtain the kinetics parameters from the modified Gompertz model described by Lin & Lay (2004) with the following equation:
(3)
where P(t) is the cumulative methane production (mL), t is the time (h), λ is the time for lag phase (day), Pmax is the maximum methane production (mL/g initial chemical oxygen demand (CODi)), and Rmax is the methane production rate (mL/g CODi·day). STATISTICA 8.0 was used to calculate the kinetic parameters from the Gompertz model.

Modification and characterization of GAC

Chemical modification of GAC-AQS promotes an adsorption capacity of 0.298 mmol/g, decreasing slightly to 0.295 mmol/g after the three desorption cycles, representing an AQS desorption of only 1% (Figure 1), which evidences the anchorage strength. This result indicates that the Lukas reagent procedure was suitable for immobilizing AQS. This procedure was previously used to attach AQS on the GAC surface to be used in a UASB reactor operated for 250 days, maintaining the redox capacity of AQS for the biotransformation of azo dye (Alvarez et al. 2017). The immobilization occurred in two steps: (1) the replacement of hydroxyl groups by chloride on the GAC surface and (2) the substitution of chloride by AQS through the anchorage with the sulfonic group. The effectiveness of the immobilization was also evidenced by the increment of the ETC in the GAC-AQS material (Figure 2), which was 2.1-fold higher than the unmodified GAC.
Figure 1

Initial adsorption capacity of AQS on GAC and remaining adsorption after the washing cycles.

Figure 1

Initial adsorption capacity of AQS on GAC and remaining adsorption after the washing cycles.

Close modal
Figure 2

Electron transfer capacity (ETC) microbially determined in GAC and GAC-AQS.

Figure 2

Electron transfer capacity (ETC) microbially determined in GAC and GAC-AQS.

Close modal

COD adsorption on GAC

The adsorption of organic matter expressed as COD occurred in the two materials (Figure 3). The highest adsorption capacity was observed with the unmodified GAC with a value of 45.5 mg/g, which is 3.5-fold higher than the value obtained with GAC-AQS (12.8 mg/g). These values correspond to adsorption rates of 22.1% for GAC and 2.7% for GAC-AQS, considering the initial COD concentration (2,766 mg/L) in the SW, hence the COD concentration after the adsorption period decreased to 2,153 and 2,692 mg/L, respectively.
Figure 3

Adsorption of organic matter (as COD) from swine wastewater on GAC and GAC-AQS. The adsorption percentage corresponds to the fraction of COD adsorbed, considering the initial COD concentration.

Figure 3

Adsorption of organic matter (as COD) from swine wastewater on GAC and GAC-AQS. The adsorption percentage corresponds to the fraction of COD adsorbed, considering the initial COD concentration.

Close modal

The organic matter composition in SW is highly variable and includes particulate, dissolved, and colloid fractions. Microbial constituents represent the bulk of the organic matter subfractionated into lipids, proteins, and their degradation products. Volatile acids (e.g., acetic acid) represent the most significant fraction of the dissolved components (Leenheer & Rostad 2004). The acidic nature of these constituents is mainly due to the presence of carboxylic groups in their structures, which promotes negative charges above pH 5 (Xia et al. 2019). The presence of positive charges in the GAC could be responsible for promoting the adsorption of organic matter by electrostatic interactions, but the pore size distribution may also play a relevant role (Newcombe et al. 2002). The low adsorption of organic matter from SW observed with the GAC-AQS compared with GAC (Figure 3) could be explained by the presence of AQS molecules, which limits the electrostatic interactions between organic matter and GAC, but also by blocking their pores. Moreover, a similar adsorption capacity of organic matter from swine effluents was observed using GAC (Burboa & Alvarez 2020).

Methane production and COD consumption

Microbial kinetics revealed the impact of GAC-AQS and GAC on methane production (Figure 4). The unmodified GAC promoted the production of 263 mL CH4/g CODi, which was the highest production observed, followed by the control with 230 mL CH4/g CODi, and by the GAC-AQS with 128 mL CH4/g CODi. The response with GAC represents increments of 1.14- and 2.05-fold compared with the control and GAC-AQS cultures, respectively. The daily methane production values indicate that the highest productive period was between days 1 and 4. The control and GAC-AQS cultures registered their maximum peaks of methane production on day 2, with unmodified GAC on day 3 (Figure 4). The COD consumption was also influenced by the presence of the conductive materials (Table 1). The GAC cultures achieved a COD consumption of 89%, followed by the control with 71%, reaching the lowest with GAC-AQS (66%). COD consumption followed the same trend as methane production. Regarding the efficiency of COD conversion to methane, the values were 95, 80, and 75% for GAC, control, and GAC-AQS, respectively (Table 1). Moreover, even though the GAC promoted higher adsorption than GAC-AQS (Figure 3), which may limit the bioavailability of substrates for microorganisms, the highest methane productivity was observed with the unmodified material. The conversion rate of COD is related to the methane yield. The GAC culture was the highest with 382 mL CH4/g CODc (consumed chemical oxygen demand), followed by the control (322 mL CH4/g CODc) and GAC-AQS (301 mL CH4/g CODc) (Figure 5). The statistical analysis revealed a significant difference between the results obtained with GAC and the other two tested conditions (GAC-AQS and control) for the COD consumption, COD conversion, and yield (Table 1 and Figure 5).
Table 1

Response from methanogenic cultures regarding pH, COD consumption, and COD conversion

ConditionFinal pHaCOD consumption (%)COD conversion (%)b
Control 7.7 71.6 ± 6.7 a 80.5 ± 5.1 a 
GAC 7.6 89.6 ± 0.5 b 95.5 ± 8.3 b 
GAC-AQS 7.6 66.9 ± 10.9 a 75.8 ± 6.2 a 
ConditionFinal pHaCOD consumption (%)COD conversion (%)b
Control 7.7 71.6 ± 6.7 a 80.5 ± 5.1 a 
GAC 7.6 89.6 ± 0.5 b 95.5 ± 8.3 b 
GAC-AQS 7.6 66.9 ± 10.9 a 75.8 ± 6.2 a 

Different letters indicate a significant difference in means (Tukey test, 95% confidence level).

aThe initial pH was 7.33.

bConversion efficiency was calculated considering 400 mL of methane produced per gram of COD consumed (Metcalf & Eddy et al. 2013).

Figure 4

Profiles showing the effect of GAC and GAC-AQS on the accumulated methane production.

Figure 4

Profiles showing the effect of GAC and GAC-AQS on the accumulated methane production.

Close modal
Figure 5

Methane yield obtained in GAC and GAC-AQS cultures. Different letters indicate a significant difference in means (Tukey test, 95% confidence level).

Figure 5

Methane yield obtained in GAC and GAC-AQS cultures. Different letters indicate a significant difference in means (Tukey test, 95% confidence level).

Close modal

Activated carbon has been used in anaerobic digestion for different purposes, including adsorption of microbial inhibitors, pH buffering, electrodes, biofilm support, substrate enrichment, and redox mediators (Xiao et al. 2022). The capacity of carbon-based materials to act as a conductive material to improve the DIET process has been associated with electrical conductivity (Chen et al. 2014), ETC (Burboa & Alvarez 2020), and redox potential (Salvador et al. 2017). Nonetheless, the mechanism of GAC to act as an electron conduit to promote methanogenesis and the breakdown of organic matter is still unclear. The unmodified GAC used in this study enhanced the methane production up to 2.05-fold compared with the GAC-AQS, even though its ETC increased by 2.1-fold after the anchorage of quinone molecules. The improvement in methane production by GAC could be associated with its capacity to transfer electrons by two mechanisms: (1) the presence of redox functional groups (e.g., quinones, phenolic, and hydroquinone moieties) in its structure, which is responsible for the electron accepting–donating capacity and (2) the conjugated π-electron contained concentrated aromatic secondary structure, which is responsible for conductivity (Klüpfel et al. 2014). For instance, the presence of quinone structures has been associated with the improvement of Rmax of methanogenesis (Wang et al. 2020).

The low methane production in the GAC-AQS cultures could be associated with a competition between methanogenesis and quinone respiration, previously demonstrated with soluble quinones acting as electron acceptors, which inhibits methane production (Cervantes et al. 2000; Alvarez et al. 2015; Palacios et al. 2023). The inhibition of methane was also demonstrated by adding different doses of soluble humic acids acting as terminal electron acceptors during microbial respiration (Li et al. 2019). Quinone respiration (AQDS, E 0′ = −184 mV) is the preferable pathway by the fact that it is thermodynamically more favorable than methanogenesis (E 0′ of CO2/CH4 = −240 mV) using H2 (E 0′ = −414 mV) as an energy source (Palacios et al. 2023). In addition, humic substances with a high content of redox mediating groups (e.g., quinones) also showed a negative effect on methane production (Alvarez & Cervantes 2012) due to inhibition of the F420-reducing hydrogenase, a key enzyme for methanogenesis (Li et al. 2019). The evidence of methanogenesis inhibition with immobilized redox mediators was documented using particulate organic matter (e.g., humic acids) contained in peatland soils (Keller & Takagi 2013), which can accept between 33 and 61% of the electrons released from anaerobic respiration (Keller & Takagi 2013). Thus, it is assumed that the high ETC obtained with GAC-AQS (1.35 mEq/g vs. 0.643 mEq/g with GAC; Figure 2) is responsible for the low methane production (Figure 4), yield (Figure 5), and rate (Rmax in Figure 6) achieved, by acting as a terminal electron acceptor instead to act as an electron conduit to favor the DIET to improve methanogenesis. In addition, the Pmax was also affected with GAC-AQS, evidenced by the lowest value obtained; nonetheless, the lag phase with GAC-AQS was statistically similar to the control but lower than the value obtained with unmodified GAC (Figure 6).
Figure 6

Kinetic parameters, Pmax (maximum methane production), Rmax (maximum methane production rate), and lag phase obtained from the Gompertz model with the experimental data collected from GAC and GAC-AQS cultures. Different letters indicate a significant difference in means (Tukey test, 95% confidence level).

Figure 6

Kinetic parameters, Pmax (maximum methane production), Rmax (maximum methane production rate), and lag phase obtained from the Gompertz model with the experimental data collected from GAC and GAC-AQS cultures. Different letters indicate a significant difference in means (Tukey test, 95% confidence level).

Close modal

Anaerobic digestion was used to break down the organic matter contained in the SW and convert it into energy in the form of methane. Nonetheless, the solid-phase quinone (GAC-AQS) competed for electrons, inhibiting the methanogenesis, evidenced by the low methane production compared with the control and unmodified GAC cultures. The results indicated that methane production with the unmodified GAC was 2.05-fold higher than the volume of methane obtained with GAC-AQS. The inhibition promoted by GAC-AQS can be attributable to its role as a terminal electron acceptor, evidenced by the high ETC determined. Future studies may include the use of solid-phase quinones (GAC-AQS) at different doses to elucidate their effect not only on methanogenesis stages but also on hydrolysis, acidogenesis, and acetogenesis stages.

The authors acknowledge the financial support from CONAHCYT and Programa de Fomento y Apoyo a Proyectos de Investigación (PROFAPI-ITSON).

All relevant data are included in the paper or its Supplementary Information.

The authors declare there is no conflict.

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