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 × 103 e− cp−1 s−1) compared with DIET (44.9 × 103 e− cp−1 s−1) or hydrogen-MIET (5.24 × 103 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.