Revealing extracellular electron transfer mediated parasitism: energetic considerations

Extracellular electron transfer (EET) is a mechanism that allows energetic coupling between two microorganisms or between a microorganism and an electrode surface. EET is either supported by direct physical contacts or mediated by electron shuttles. So far, studies dealing with interspecies EET (so-called IET) have mainly focused on possible syntrophic interactions between microorganisms favoured by this mechanism. In this article, the case of fermentative bacteria receiving extracellular electrons while fermenting a substrate is considered. A thermodynamical analysis based on metabolic energy balances was applied to re-investigate experimental data from the literature. Results suggest that the observations of a decrease of cell biomass yields of fermentative electron-accepting species, as mostly reported, can be unravelled by EET energetics and correspond to parasitism in case of IET. As an illustration, the growth yield decrease of Propionibacterium freudenreichii (-14%) observed in electro-fermentation experiments was fully explained by EET energetics when electrons were used by this species at a potential of -0.12 ± 0.01 V vs SHE. Analysis of other cases showed that, in addition to EET energetics in Clostridium pasteurianum, biological regulations can also be involved in such biomass yield decrease (-33% to -38%). Interestingly, the diminution of bacterial biomass production is always concomitant with an increased production of reduced compounds making IET-mediated parasitism and electro-fermentation attractive ways to optimize carbon fluxes in fermentation processes.