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Carbon capture and utilization has been proposed as one strategy to combat global warming. Microbial electrolysis cells (MECs) combine the biological conversion of carbon dioxide (CO2) with the formation of valuable products such as methane. This study was motivated by the surprising gap in current knowledge about the utilization of real exhaust gas as a CO2 source for methane production in a fully biocatalyzed MEC. Therefore, two steel mill off-gases differing in composition were tested in a two-chamber MEC, consisting of an organic substrate-oxidizing bioanode and a methane-producing biocathode, by applying a constant anode potential. The methane production rate in the MEC decreased immediately when steel mill off-gas was tested, which likely inhibited anaerobic methanogens in the presence of oxygen. However, methanogenesis was still ongoing even though at lower methane production rates than with pure CO2. Subsequently, pure CO2 was studied for methanation, and the cathodic biofilm successfully recovered from inhibition reaching a methane production rate of 10.8 L m−2d−1. Metagenomic analysis revealed Geobacter as the dominant genus forming the anodic organic substrate-oxidizing biofilms, whereas Methanobacterium was most abundant at the cathodic methane-producing biofilms.

Bioelectrochemical power-to-gas represents a novel solution for electrical energy storage, currently under development. It allows storing renewable energy surplus in the form of methane (CH4), while treating wastewater, therefore bridging the electricity and natural gas (and wastewater) grids. The technology can be coupled with membrane contactors for carbon dioxide (CO2) capture, dissolving the CO2 in wastewater before feeding it to the bioelectrochemical system. This way, the integrated system can achieve simultaneous carbon capture and energy storage objectives, in the scenario of a wastewater treatment plant application. In this study, such technology was developed in a medium-scale prototype (32 L volume), which was operated for 400 days in different conditions of temperature, voltage and CO2 capture rate. The prototype achieved the highest CH4 production rate (147 ± 33 L m–3 d–1) at the lowest specific energy consumption (1.0 ± 0.3 kWh m–3 CH4) when operated at 25°C and applying a voltage of 0.7 V, while capturing and converting 22 L m–3 d–1 of CO2. The produced biogas was nearer to biomethane quality (CH4 > 90% v/v) when CO2 was not injected in the wastewater. Traces of hydrogen (H2) in the biogas, detectable during the periods of closed electrical circuit operation, indicated that hydrogenotrophic methanogenesis was taking place at the cathode. On the other hand, a relevant CH4 production during the periods of open electrical circuit operation confirmed the presence of acetoclastic methanogenic microorganisms in the microbial community, which was dominated by the archaeal genus Methanothrix (Euryarchaeota). Different operational taxonomic units belonging to the bacterial Synergistes phylum were found at the anode and the cathode, having a potential role in organic matter degradation and H2 production, respectively. In the panorama of methanation technologies currently available for power-to-gas, the performances of this bioelectrochemical prototype are not yet competitive, especially in terms of volumetric CH4 production rate and power density demand. However, the possibility to obtain a high-quality biogas (almost reaching biomethane quality standards) at a minimal energy consumption represents a potentially favorable business scenario for this technology.

Microbial electrosynthesis (MES) has been gaining considerable interest as the next step in the evolution of microbial electrochemical technologies. Understanding the niche biocathode environment and microbial community is critical for further developing this technology as the biocathode is key to product formation and efficiency. MES is generally operated to enrich a specific functional group (e.g., methanogens or homoacetogens) from a mixed-culture inoculum. However, due to differences in H2 and CO2 availability across the cathode surface, competition and syntrophy may lead to overall variability and significant beta-diversity within and between replicate reactors, which can affect performance reproducibility. Therefore, this study aimed to investigate the distribution and potential spatial variability of the microbial communities in MES methanogenic biocathodes. Triplicate methanogenic biocathodes were enriched in microbial electrolysis cells for 5 months at an applied voltage of 0.7 V. They were then transferred to triplicate dual-chambered MES reactors and operated at -1.0 V vs. Ag/AgCl for six batches. At the end of the experiment, triplicate samples were taken at different positions (top, center, bottom) from each biocathode for a total of nine samples for total biomass protein analysis and 16S rRNA gene amplicon sequencing. Microbial community analyses showed that the biocathodes were highly enriched with methanogens, especially the hydrogenotrophic methanogen family Methanobacteriaceae, Methanobacterium sp., and the mixotrophic Methanosarcina sp., with an overall core community representing > 97% of sequence reads in all samples. There was no statistically significant spatial variability (p > 0.05) observed in the distribution of these communities within and between the reactors. These results suggest deterministic community assembly and indicate the reproducibility of electromethanogenic biocathode communities, with implications for larger-scale reactors.

Direct electron uptake by prokaryotes is a recently described mechanism with a potential application for energy and CO2 storage into value added chemicals. Members of Methanosarcinales, an environmentally and biotechnologically relevant group of methanogens, were previously shown to retrieve electrons from an extracellular electrogenic partner performing Direct Interspecies Electron Transfer (DIET) and were therefore proposed to be electroactive. However, their intrinsic electroactivity has never been examined. In this study, we tested two methanogens belonging to the genus Methanosarcina, M. barkeri, and M. horonobensis, regarding their ability to accept electrons directly from insoluble electron donors like other cells, conductive particles and electrodes. Both methanogens were able to retrieve electrons from Geobacter metallireducens via DIET. Furthermore, DIET was also stimulated upon addition of electrically conductive granular activated carbon (GAC) when each was co-cultured with G. metallireducens. However, when provided with a cathode poised at −400 mV (vs. SHE), only M. barkeri could perform electromethanogenesis. In contrast, the strict hydrogenotrophic methanogen, Methanobacterium formicicum, did not produce methane regardless of the type of insoluble electron donor provided (Geobacter cells, GAC or electrodes). A comparison of functional gene categories between the two Methanosarcina showed differences regarding energy metabolism, which could explain dissimilarities concerning electromethanogenesis at fixed potentials. We suggest that these dissimilarities are minimized in the presence of an electrogenic DIET partner (e.g., Geobacter), which can modulate its surface redox potentials by adjusting the expression of electroactive surface proteins.

Microbial electrosynthesis (MES) has been gaining considerable interest as the next step in the evolution of microbial electrochemical technologies. Understanding the niche biocathode environment and microbial community is critical for further developing this technology as the biocathode is key to product formation and efficiency. MES is generally operated to enrich a specific functional group (e.g., methanogens or homoacetogens) from a mixed-culture inoculum. However, due to differences in H2 and CO2 availability across the cathode surface, competition and syntrophy may lead to overall variability and significant beta-diversity within and between replicate reactors, which can affect performance reproducibility. Therefore, this study aimed to investigate the distribution and potential spatial variability of the microbial communities in MES methanogenic biocathodes. Triplicate methanogenic biocathodes were enriched in microbial electrolysis cells for 5 months at an applied voltage of 0.7 V. They were then transferred to triplicate dual-chambered MES reactors and operated at -1.0 V vs. Ag/AgCl for six batches. At the end of the experiment, triplicate samples were taken at different positions (top, center, bottom) from each biocathode for a total of nine samples for total biomass protein analysis and 16S rRNA gene amplicon sequencing. Microbial community analyses showed that the biocathodes were highly enriched with methanogens, especially the hydrogenotrophic methanogen family Methanobacteriaceae, Methanobacterium sp., and the mixotrophic Methanosarcina sp., with an overall core community representing > 97% of sequence reads in all samples. There was no statistically significant spatial variability (p > 0.05) observed in the distribution of these communities within and between the reactors. These results suggest deterministic community assembly and indicate the reproducibility of electromethanogenic biocathode communities, with implications for larger-scale reactors. [ABSTRACT FROM AUTHOR]

In subsurface anoxic environments, microbial communities generally produce methane as an end-product to consume organic compounds. This metabolic function is a source of biogenic methane in coastal natural gas aquifers, submarine mud volcanoes, and methane hydrates. Within the methanogenic communities, hydrogenotrophic methanogens, and syntrophic bacteria are converting volatile fatty acids to methane syntrophically via interspecies hydrogen transfer. Recently, direct interspecies electron transfer (DIET) between fermentative/syntrophic bacteria and electrotrophic methanogens has been proposed as an effective interspecies metabolite transfer process to enhance methane production. In this study, in order to stimulate the DIET-associated methanogenic process at deep biosphere-aquifer systems in a natural gas field, we operated a bioelectrochemical system (BES) to apply voltage between an anode and a cathode. Two single-chamber BESs were filled with seawater-based formation water collected from an onshore natural gas well, repeatedly amended with acetate, and operated with 600 mV between electrodes for 21 months, resulting in a successful conversion of acetate to methane via electrical current consumption. One reactor yielded a stable current of ~200 mA/m2 with a coulombic efficiency (CE) of >90%; however, the other reactor, which had been incidentally disconnected for 3 days, showed less electromethanogenic activity with a CE of only ~10%. The 16S rRNA gene-based community analyses showed that two methanogenic archaeal families, Methanocalculaceae and Methanobacteriaceae, were abundant in cathode biofilms that were mainly covered by single-cell-layered biofilm, implicating them as key players in the electromethanogenesis. In contrast, family Methanosaetaceae was abundant at both electrodes and the electrolyte suspension only in the reactor with less electromethanogenesis, suggesting this family was not involved in electromethanogenesis and became abundant only after the no-electron-flow event. The anodes were covered by thick biofilms with filamentous networks, with the family Desulfuromonadaceae dominating in the early stage of the operation. The family Geobacteraceae (mainly genus Geoalkalibacter) became dominant during the longer-term operation, suggesting that these families were correlated with electrode-respiring reactions. These results indicate that the BES reactors with voltage application effectively activated a subsurface DIET-related methanogenic microbiome in the natural gas field, and specific electrogenic bacteria and electromethanogenic archaea were identified within the anode and/or cathode biofilms.

High current densities in microbial electrolysis cells (MECs) result from the predominance of various Geobacter species on the anode. MECs inoculated from different sources often converge in terms of current production and predominance of Geobacter species despite variability in the inoculum community. Relatively less is known about the effects of inoculum source on methane gas production in MECs, and specifically whether archaeal communities similarly converge to one specific genus. MECs were examined here on the basis of maximum methane production and current density relative to the inoculum community structure. We used anaerobic digester (AD) sludge dominated by acetoclastic Methanosaeta species, and an anaerobic bog sediment where hydrogenotrophic methanogens were detected. Inoculation using solids to medium ratio of 25% w/v resulted in the highest methane production rates (0.27 mL mL–1 cm–2, gas volume normalized by liquid volume and cathode projected area) and highest peak current densities (0.5 mA cm–2) for the bog sample. Methane production was independent of solid to medium ratio when AD sludge was used as the inoculum. 16S rRNA gene community analysis using pyrosequencing and qPCR confirmed the convergence of Archaea to Methanobacterium and Methanobrevibacter, and of Bacteria to Geobacter, despite their absence in AD sludge. Combined with other studies, these findings suggest that Archaea of the hydrogenotrophic genera Methanobacterium and Methanobrevibacter are the most important microorganisms for methane production in MECs and that their presence in the inoculum improves the performance.

High current densities in microbial electrolysis cells (MECs) result from the predominance of various Geobacter species on the anode, but it is not known if archaeal communities similarly converge to one specific genus. MECs were examined here on the basis of maximum methane production and current density relative to the inoculum community structure. We used anaerobic digester (AD) sludge dominated by acetoclastic Methanosaeta, and an anaerobic bog sediment where hydrogenotrophic methanogens were detected. Inoculation using solids to medium ratio of 25% (w/v) resulted in the highest methane production rates (0.27 mL mL-1 cm-2, gas volume normalized by liquid volume and cathode projected area) and highest peak current densities (0.5 mA cm-2) for the bog sample. Methane production was independent of solid to medium ratio when AD sludge was used as the inoculum. 16S rRNA gene community analysis using pyrosequencing and quantitative PCR confirmed the convergence of Archaea to Methanobacterium and Methanobrevibacter, and of Bacteria to Geobacter, despite their absence in AD sludge. Combined with other studies, these findings suggest that Archaea of the hydrogenotrophic genera Methanobacterium and Methanobrevibacter are the most important microorganisms for methane production in MECs and that their presence in the inoculum improves the performance. [ABSTRACT FROM AUTHOR]