Extracellular electron transfer: From early life to modern biogeochemistry and applications

Extracellular electron transfer (EET) may well have been the earliest form of microbial respiration, but it is also one of the most recently discovered. EET plays an important role in the biogeochemical cycling of carbon, metals, and nutrients; corrosion of metals; the conversion of organic wastes to methane; and the bioremediation of subsurface contaminants. A broad diversity of bacteria and archaea, inhabiting a wide range of environments, are capable of EET. Limited study of just a few model microbes has already revealed multiple divergent EET mechanisms for electron transfer to the outer cell surface. Although most EET studies have focused on microbes that form electrical contacts at their outer surface, intracellularly reduced electron shuttles may also be widespread. Effective growth with minerals like Fe(III) oxides as the electron acceptor also requires solubilization with chelators; redox-active electron shuttles to ferry electrons from the cell surface to electron acceptors; or the expression of outer-surface nanowires to extend the electronic reach of the cells. Functional studies on nanowires have been restricted to Geobacter species, which produce electrically conductive pili that are required for long-range EET, and cytochrome filaments. Promoting direct interspecies electron transfer to improve the conversion of organic wastes to methane is an emerging focus of applied EET research, as is the prevention of EET associated with microbial metal corrosion. Microbes' ability to exchange electrons with electrodes have inspired multiple bioelectrochemical technologies. Electroactive microbes are the sensing component of novel living electronic sensors. e-Pili have been incorporated in electronic devices with unique sensing, electricity generation, and neuromorphic functions. However, most EET-related applications are in early phases of development. Future research opportunities in diverse aspects of EET are highlighted throughout.