Novel Outlook in Microbial Ecology: Nonmutualistic Interspecies Electron Transfer

The development of bioelectrochemistry has revealed a wide diversity of electroactive microorganisms able to exchange electrons with electrodes through mechanisms of extracellular electron transfer. In nature, these mechanisms can be used by electron-donating microbes to reach distant or nonsoluble terminal electron acceptors such as iron oxides or other microorganisms. So far, research on microbe-to-microbe electron transfer has exclusively been focused on mutualistic interactions. It has been experimentally demonstrated that some fermentative species can accept extracellular electrons, even when it is detrimental to their growth yield, which supports the existence of nonmutualistic interspecies electron transfer. Recent advances in microbial electrochemical technologies have revealed the existence of numerous and highly diverse microorganisms able to exchange electrons with electrodes. This diversity could reflect the capacity of microorganisms to release and/or retrieve electrons with each other in natural environments. So far, this interspecies electron transfer has been studied with a special focus on syntrophy and was successfully demonstrated for several couples of species. In this article we argue that electron exchange between microbes exists beyond syntrophy or mutualism and could also promote competitive and even parasitic behaviour. Based on three interesting case studies identified from the literature, we also highlight that such nonmutualistic interactions could be widespread and of particular significance for the survival of pathogens or the shaping of complex microbial communities. Recent advances in microbial electrochemical technologies have revealed the existence of numerous and highly diverse microorganisms able to exchange electrons with electrodes. This diversity could reflect the capacity of microorganisms to release and/or retrieve electrons with each other in natural environments. So far, this interspecies electron transfer has been studied with a special focus on syntrophy and was successfully demonstrated for several couples of species. In this article we argue that electron exchange between microbes exists beyond syntrophy or mutualism and could also promote competitive and even parasitic behaviour. Based on three interesting case studies identified from the literature, we also highlight that such nonmutualistic interactions could be widespread and of particular significance for the survival of pathogens or the shaping of complex microbial communities. pili or extension of the outer membrane which is electrically conductive and can be used by microorganisms to physically reach distant terminal electron acceptors. fermentation process in which polarized electrodes are employed as a driving tool. soluble redox-active compounds (e.g., H2, flavins) which can be used to reach distant terminal electron acceptors. a mechanism that allows electron transfer from a microorganism to an extracellular electron acceptor, or from an extracellular electron donor to a microorganism. a mechanism that allows electron transfer between different species of microbes. Transfer can be either direct or mediated by electron shuttles. electrochemical processes in which at least one reaction is catalysed by microorganisms. theoretical redox reference which corresponds to the H+/H2 couple under standard conditions (i.e., 25°C and 1 atm). the last electron acceptor in an electron transport chain.