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Direct interspecies electron transfer mechanisms of a biochar-amended anaerobic digestion: a review.

ABSTRACT: This paper explores the mechanisms of biochar that facilitate direct interspecies electron transfer (DIET) among syntrophic microorganisms leading to improved anaerobic digestion. Properties such as specific surface area (SSA), cation exchange capacity (CEC), presence of functional groups (FG), and electrical conductivity (EC) were found favorable for increased methane production, reduction of lag phase, and adsorption of inhibitors. It is revealed that these properties can be modified and are greatly affected by the synthesizing temperature, biomass types, and residence time. Additionally, suitable biochar concentration has to be observed since dosage beyond the optimal range can create inhibitions. High organic loading rate (OLR), pH shocks, quick accumulation and relatively low degradation of VFAs, and the presence of heavy metals and toxins are the major inhibitors identified. Summaries of microbial community analysis show fermentative bacteria and methanogens that are known to participate in DIET. These are Methanosaeta, Methanobacterium, Methanospirillum, and Methanosarcina for the archaeal community; whereas, Firmicutes, Proteobacteria, Synergistetes, Spirochetes, and Bacteroidetes are relatively for bacterial analyses. However, the number of defined cocultures promoting DIET is very limited, and there is still a large percentage of unknown bacteria that are believed to support DIET. Moreover, the instantaneous growth of participating microorganisms has to be validated throughout the process.

SUBMITTER: Valentin MT

PROVIDER: S-EPMC10546780 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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Direct interspecies electron transfer mechanisms of a biochar-amended anaerobic digestion: a review.

Valentin Marvin T MT Luo Gang G Zhang Shicheng S Białowiec Andrzej A

Biotechnology for biofuels and bioproducts 20231003 1

This paper explores the mechanisms of biochar that facilitate direct interspecies electron transfer (DIET) among syntrophic microorganisms leading to improved anaerobic digestion. Properties such as specific surface area (SSA), cation exchange capacity (CEC), presence of functional groups (FG), and electrical conductivity (EC) were found favorable for increased methane production, reduction of lag phase, and adsorption of inhibitors. It is revealed that these properties can be modified and are g ...[more]

PMID: 37784139

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Project description:Direct interspecies electron transfer (DIET) between bacteria and methanogenic archaea appears to be an important syntrophy in both natural and engineered methanogenic environments. However, the electrical connections on the outer surface of methanogens and the subsequent processing of electrons for carbon dioxide reduction to methane are poorly understood. Here, we report that the genetically tractable methanogen Methanosarcina acetivorans can grow via DIET in coculture with Geobacter metallireducens serving as the electron-donating partner. Comparison of gene expression patterns in M. acetivorans grown in coculture versus pure-culture growth on acetate revealed that transcripts for the outer-surface multiheme c-type cytochrome MmcA were higher during DIET-based growth. Deletion of mmcA inhibited DIET. The high aromatic amino acid content of M. acetivorans archaellins suggests that they might assemble into electrically conductive archaella. A mutant that could not express archaella was deficient in DIET. However, this mutant grew in DIET-based coculture as well as the archaellum-expressing parental strain in the presence of granular activated carbon, which was previously shown to serve as a substitute for electrically conductive pili as a conduit for long-range interspecies electron transfer in other DIET-based cocultures. Transcriptomic data suggesting that the membrane-bound Rnf, Fpo, and HdrED complexes also play a role in DIET were incorporated into a charge-balanced model illustrating how electrons entering the cell through MmcA can yield energy to support growth from carbon dioxide reduction. The results are the first genetics-based functional demonstration of likely outer-surface electrical contacts for DIET in a methanogen. IMPORTANCE The conversion of organic matter to methane plays an important role in the global carbon cycle and is an effective strategy for converting wastes to a useful biofuel. The reduction of carbon dioxide to methane accounts for approximately a third of the methane produced in anaerobic soils and sediments as well as waste digesters. Potential electron donors for carbon dioxide reduction are H2 or electrons derived from direct interspecies electron transfer (DIET) between bacteria and methanogens. Elucidating the relative importance of these electron donors has been difficult due to a lack of information on the electrical connections on the outer surfaces of methanogens and how they process the electrons received from DIET. Transcriptomic patterns and gene deletion phenotypes reported here provide insight into how a group of Methanosarcina organisms that play an important role in methane production in soils and sediments participate in DIET.

Project description:Cytochrome-to-cytochrome electron transfer and electron transfer along conduits of multiple extracellular magnetite grains are often proposed as strategies for direct interspecies electron transfer (DIET) that do not require electrically conductive pili (e-pili). However, physical evidence for these proposed DIET mechanisms has been lacking. To investigate these possibilities further, we constructed Geobacter metallireducens strain Aro-5, in which the wild-type pilin gene was replaced with the aro-5 pilin gene that was previously shown to yield poorly conductive pili in Geobacter sulfurreducens strain Aro-5. G. metallireducens strain Aro-5 did not reduce Fe(III) oxide and produced only low current densities, phenotypes consistent with expression of poorly conductive pili. Like G. sulfurreducens strain Aro-5, G. metallireducens strain Aro-5 displayed abundant outer surface cytochromes. Cocultures initiated with wild-type G. metallireducens as the electron-donating strain and G. sulfurreducens strain Aro-5 as the electron-accepting strain grew via DIET. However, G. metallireducens Aro-5/G. sulfurreducens wild-type cocultures did not. Cocultures initiated with the Aro-5 strains of both species grew only when amended with granular activated carbon (GAC), a conductive material known to be a conduit for DIET. Magnetite could not substitute for GAC. The inability of the two Aro-5 strains to adapt for DIET in the absence of GAC suggests that there are physical constraints on establishing DIET solely through cytochrome-to-cytochrome electron transfer or along chains of magnetite. The finding that DIET is possible with electron-accepting partners that lack highly conductive pili greatly expands the range of potential electron-accepting partners that might participate in DIET.IMPORTANCE DIET is thought to be an important mechanism for interspecies electron exchange in natural anaerobic soils and sediments in which methane is either produced or consumed, as well as in some photosynthetic mats and anaerobic digesters converting organic wastes to methane. Understanding the potential mechanisms for DIET will not only aid in modeling carbon and electron flow in these geochemically significant environments but will also be helpful for interpreting meta-omic data from as-yet-uncultured microbes in DIET-based communities and for designing strategies to promote DIET in anaerobic digesters. The results demonstrate the need to develop a better understanding of the diversity of types of e-pili in the microbial world to identify potential electron-donating partners for DIET. Novel methods for recovering as-yet-uncultivated microorganisms capable of DIET in culture will be needed to further evaluate whether DIET is possible without e-pili in the absence of conductive materials such as GAC.

Project description:Conductive materials are known to promote direct interspecies electron transfer (DIET) by electrically bridging microbial cells. Previous studies have suggested that supplementation of graphene oxide (GO) based materials, including GO, and reduced GO (rGO), to anaerobic microbial communities, can promote DIET. This promotion mechanism is thought to be involved in electron transfer via rGO or biologically formed rGO. However, concrete evidence that rGO directly promotes DIET is still lacking. Furthermore, the effects of the physicochemical properties of GO-based materials on DIET efficiency have not been elucidated. In the current work, we investigated whether chemically and biologically reduced GO compounds can promote DIET in a defined model coculture system, and also examined the effects of surface properties on DIET-promoting efficiency. Supplementation of GO to a defined DIET coculture composed of an ethanol-oxidizing electron producer Geobacter metallireducens and a methane-producing electron consumer Methanosarcina barkeri promoted methane production from ethanol. X-ray photoelectron spectroscopy revealed that GO was reduced to rGO during cultivation by G. metallireducens activity. The stoichiometry of methane production from ethanol and the isotope labeling experiments clearly showed that biologically reduced GO induced DIET-mediated syntrophic methanogenesis. We also assessed the DIET-promoting efficiency of chemically reduced GO and its derivatives, including hydrophilic amine-functionalized rGO (rGO-NH2) and hydrophobic octadecylamine-functionalized rGO (rGO-ODA). While all tested rGO derivatives induced DIET, the rGO derivatives with higher hydrophilicity showed higher DIET-promoting efficiency. Optical microscope observation revealed that microbial cells, in particular, G. metallireducens, more quickly adhered to more hydrophilic GO-based materials. The superior ability to recruit microbial cells is a critical feature of the higher DIET-promoting efficiency of the hydrophilic materials. This study demonstrates that biologically and chemically reduced GO can promote DIET-mediated syntrophic methanogenesis. Our results also suggested that the surface hydrophilicity (i.e., affinity toward microbial cells) is one of the important determinants of the DIET-promoting efficiencies. These observations will provide useful guidance for the selection of conductive particles for the improvement of methanogenesis in anaerobic digesters.

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Direct interspecies electron transfer mechanisms of a biochar-amended anaerobic digestion: a review.

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Direct interspecies electron transfer mechanisms of a biochar-amended anaerobic digestion: a review.

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