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Modelling extracellular limitations for mediated versus direct interspecies electron transfer.

ABSTRACT: 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.

SUBMITTER: Storck T

PROVIDER: S-EPMC4817672 | biostudies-literature | 2016 Mar

REPOSITORIES: biostudies-literature

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Modelling extracellular limitations for mediated versus direct interspecies electron transfer.

Storck Tomas T Virdis Bernardino B Batstone Damien J DJ

The ISME journal 20151106 3

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 el ...[more]

PMID: 26545286

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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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Modelling extracellular limitations for mediated versus direct interspecies electron transfer.

Publications

Modelling extracellular limitations for mediated versus direct interspecies electron transfer.

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