Promoting interspecies electron transfer with biochar.
Ontology highlight
ABSTRACT:
SUBMITTER: Chen S
PROVIDER: S-EPMC4028902 | biostudies-other | 2014
REPOSITORIES: biostudies-other
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Project description: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.
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Project description:Anaerobic digestion was one of the first bioenergy strategies developed, yet the interactions of the microbial community that is responsible for the production of methane are still poorly understood. For example, it has only recently been recognized that the bacteria that oxidize organic waste components can forge electrical connections with methane-producing microbes through biologically produced, protein-based, conductive circuits. This direct interspecies electron transfer (DIET) is faster than interspecies electron exchange via diffusive electron carriers, such as H2. DIET is also more resilient to perturbations such as increases in organic load inputs or toxic compounds. However, with current digester practices DIET rarely predominates. Improvements in anaerobic digestion associated with the addition of electrically conductive materials have been attributed to increased DIET, but experimental verification has been lacking. This deficiency may soon be overcome with improved understanding of the diversity of microbes capable of DIET, which is leading to molecular tools for determining the extent of DIET. Here we review the microbiology of DIET, suggest molecular strategies for monitoring DIET in anaerobic digesters, and propose approaches for re-engineering digester design and practices to encourage DIET.
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Project description:Microbial phototrophs, key primary producers on Earth, use H2O, H2, H2S and other reduced inorganic compounds as electron donors. Here we describe a form of metabolism linking anoxygenic photosynthesis to anaerobic respiration that we call 'syntrophic anaerobic photosynthesis'. We show that photoautotrophy in the green sulfur bacterium Prosthecochloris aestaurii can be driven by either electrons from a solid electrode or acetate oxidation via direct interspecies electron transfer from a heterotrophic partner bacterium, Geobacter sulfurreducens. Photosynthetic growth of P. aestuarii using reductant provided by either an electrode or syntrophy is robust and light-dependent. In contrast, P. aestuarii does not grow in co-culture with a G. sulfurreducens mutant lacking a trans-outer membrane porin-cytochrome protein complex required for direct intercellular electron transfer. Syntrophic anaerobic photosynthesis is therefore a carbon cycling process that could take place in anoxic environments. This process could be exploited for biotechnological applications, such as waste treatment and bioenergy production, using engineered phototrophic microbial communities.
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Project description:Direct interspecies electron transfer (DIET) is an effective mechanism for microbial species to exchange electrons cooperatively during syntrophic metabolism. It is generally accepted that DIET is mainly mediated by electrically conductive pili and outer surface c-type cytochromes (c-Cyts). However, as an extracellular matrix is ubiquitous and abundant on the surface of microorganisms, the effect and mechanism of exopolysaccharides on DIET are still unclear. This study constructed a co-culture of exopolysaccharides-deficient Geobacter sulfurreducens with Geobacter metallireducens to explore the role of exopolysaccharides in DIET. Results revealed that the deficiency of exopolysaccharides extended the metabolic period of the co-culture by 44.4% and changed the proportions of each species in the co-culture. The exopolysaccharides-deficient co-culture failed to form large, tight spherical aggregates and the expression of c-Cyts and pili was decreased. The addition of magnetite and granular activated carbon (GAC), respectively, might compensate for the functions of c-Cyts and pili in the first generation of co-culture, but the stimulatory effect on the metabolic stable period co-culture was fairly limited. These findings demonstrate that non-conductive exopolysaccharides are an important component of DIET aggregates and an extracellular matrix for DIET-required c-Cyts.
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Project description:The possibility that metatranscriptomic analysis could distinguish between direct interspecies electron transfer (DIET) and H2 interspecies transfer (HIT) in anaerobic communities was investigated by comparing gene transcript abundance in cocultures in which Geobacter sulfurreducens was the electron-accepting partner for either Geobacter metallireducens, which performs DIET, or Pelobacter carbinolicus, which relies on HIT. Transcript abundance for G. sulfurreducens uptake hydrogenase genes was 7-fold lower in cocultures with G. metallireducens than in cocultures with P. carbinolicus, consistent with DIET and HIT, respectively, in the two cocultures. Transcript abundance for the pilus-associated cytochrome OmcS, which is essential for DIET but not for HIT, was 240-fold higher in the cocultures with G. metallireducens than in cocultures with P. carbinolicus. The pilin gene pilA was moderately expressed despite a mutation that might be expected to repress pilA expression. Lower transcript abundance for G. sulfurreducens genes associated with acetate metabolism in the cocultures with P. carbinolicus was consistent with the repression of these genes by H2 during HIT. Genes for the biogenesis of pili and flagella and several c-type cytochrome genes were among the most highly expressed in G. metallireducens. Mutant strains that lacked the ability to produce pili, flagella, or the outer surface c-type cytochrome encoded by Gmet_2896 were not able to form cocultures with G. sulfurreducens. These results demonstrate that there are unique gene expression patterns that distinguish DIET from HIT and suggest that metatranscriptomics may be a promising route to investigate interspecies electron transfer pathways in more-complex environments.
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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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Project description:In anaerobic biota, reducing equivalents (electrons) are transferred between different species of microbes [interspecies electron transfer (IET)], establishing the basis of cooperative behaviors and community functions. IET mechanisms described so far are based on diffusion of redox chemical species and/or direct contact in cell aggregates. Here, we show another possibility that IET also occurs via electric currents through natural conductive minerals. Our investigation revealed that electrically conductive magnetite nanoparticles facilitated IET from Geobacter sulfurreducens to Thiobacillus denitrificans, accomplishing acetate oxidation coupled to nitrate reduction. This two-species cooperative catabolism also occurred, albeit one order of magnitude slower, in the presence of Fe ions that worked as diffusive redox species. Semiconductive and insulating iron-oxide nanoparticles did not accelerate the cooperative catabolism. Our results suggest that microbes use conductive mineral particles as conduits of electrons, resulting in efficient IET and cooperative catabolism. Furthermore, such natural mineral conduits are considered to provide ecological advantages for users, because their investments in IET can be reduced. Given that conductive minerals are ubiquitously and abundantly present in nature, electric interactions between microbes and conductive minerals may contribute greatly to the coupling of biogeochemical reactions.
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Project description:Interspecies electron transfer (IET) is important for many anaerobic processes, but is critically dependent on mode of transfer. In particular, direct IET (DIET) has been recently proposed as a metabolically advantageous mode compared with mediated IET (MIET) via hydrogen or formate. We analyse relative feasibility of these IET modes by modelling external limitations using a reaction-diffusion-electrochemical approach in a three-dimensional domain. For otherwise identical conditions, external electron transfer rates per cell pair (cp) are considerably higher for formate-MIET (317 × 10(3) e(-)?cp(-1)?s(-1)) compared with DIET (44.9 × 10(3) e(-)?cp(-1)?s(-1)) or hydrogen-MIET (5.24 × 10(3) e(-)?cp(-1)?s(-1)). MIET is limited by the mediator concentration gradient at which reactions are still thermodynamically feasible, whereas DIET is limited through redox cofactor (for example, cytochromes) activation losses. Model outcomes are sensitive to key parameters for external electron transfer including cofactor electron transfer rate constant and redox cofactor area, concentration or count per cell, but formate-MIET is generally more favourable for reasonable parameter ranges. Extending the analysis to multiple cells shows that the size of the network does not strongly influence relative or absolute favourability of IET modes. Similar electron transfer rates for formate-MIET and DIET can be achieved in our case with a slight (0.7?kJ?mol(-1)) thermodynamic advantage for DIET. This indicates that close to thermodynamic feasibility, external limitations can be compensated for by improved metabolic efficiency when using direct electron transfer.
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Project description:Mechanisms for electron transfer within microbial aggregates derived from an upflow anaerobic sludge blanket reactor converting brewery waste to methane were investigated in order to better understand the function of methanogenic consortia. The aggregates were electrically conductive, with conductivities 3-fold higher than the conductivities previously reported for dual-species aggregates of Geobacter species in which the two species appeared to exchange electrons via interspecies electron transfer. The temperature dependence response of the aggregate conductance was characteristic of the organic metallic-like conductance previously described for the conductive pili of Geobacter sulfurreducens and was inconsistent with electron conduction through minerals. Studies in which aggregates were incubated with high concentrations of potential electron donors demonstrated that the aggregates had no significant capacity for conversion of hydrogen to methane. The aggregates converted formate to methane but at rates too low to account for the rates at which that the aggregates syntrophically metabolized ethanol, an important component of the reactor influent. Geobacter species comprised 25% of 16S rRNA gene sequences recovered from the aggregates, suggesting that Geobacter species may have contributed to some but probably not all of the aggregate conductivity. Microorganisms most closely related to the acetate-utilizing Methanosaeta concilii accounted for more than 90% of the sequences that could be assigned to methane producers, consistent with the poor capacity for hydrogen and formate utilization. These results demonstrate for the first time that methanogenic wastewater aggregates can be electrically conductive and suggest that direct interspecies electron transfer could be an important mechanism for electron exchange in some methanogenic systems.
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Project description:Direct interspecies electron transfer (DIET) has been identified as an efficient metabolism between symbiotically interacting organisms. One method of DIET uses conductive materials (e.g., granular activated carbon (GAC)) as a medium to shuttle electrons from electron donating organisms (eg., Geobacter metallireducens) to electron accepting organisms (e.g., Geobacter sulfurreducens and Methanosarcina barkeri). Conductive materials such as GAC, become negatively charged in DIET processes due to reduction by electron donating organisms. This high excess electron density in GAC leads to quantum tunnelling of electrons being a significant electron transfer mechanism for DIET. Thus, a theoretical model obeying the Wentzel-Kramers-Brillouin (WKB) approximation and Fermi-Dirac statistics was developed and simulated. In the model, the electron tunnelling transfer barrier was described by an effective rectangular barrier. The result of our 1D tunnelling simulations indicates that within 29.4 nm of the GAC, tunnelling can sufficiently supply electrons from GAC to G. sulfurreducens and M. barkeri. The phenomenon of tunnelling may also have significance as a stimulant of chemotaxis for G. sulfurreducens and other electron accepting microbes when attempting to adsorb onto GAC. This study sheds light on quantum tunnelling's significant potential in both bacterium and archaeon DIET-centric processes.
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