3 - Electron transfer mechanisms in biofilms

Abstract

Understanding the mechanisms by which microorganisms transfer electrons to and from electrodes is essential for the development of the many potential applications of bioelectrochemical systems. The knowledge on the extracellular electron transfer (EET) mechanisms of microorganisms has steeply increased during the last decade(s) due to extensive fundamental research. In general, there are two types of EET mechanisms: (1) direct EET using outer surface redox molecules and/or conductive nanowires and (2) mediated EET using electron shuttles. Direct EET is best understood for the anode-respiring Geobacter sulfurreducens, which uses outer membrane cytochromes and pili nanowires to transport electrons to an anode. The other model electrogen, Shewanella oneidensis, mainly uses flavin shuttles to mediate its EET, but also has membrane extensions that can act as conductive nanowires. Electrogens are typically heterotrophic Fe(III) reducers, but a much wider diversity exists in electrotrophic microorganisms, as a cathode can be used as electron donor by oxygen-reducing, fumarate-reducing, nitrogen compound-reducing, hydrogen-producing, methanogenic, and acetogenic microorganisms. Nevertheless, microbial electron uptake from a cathode is still much less understood than electron transfer to anodes. Some model electrotrophs, including the acidophilic aerobe Acidithiobacillus ferrooxidans, the acetogen Clostridium ljungdahlii, and the methanogen Methanococcus maripaludis, have already been identified. Several studies have suggested a direct EET mechanism for these electrotrophs, but hydrogen-mediated EET likely also plays an important role. Besides exchanging electrons with electrodes, microorganisms can also exchange electrons between each other. Interspecies electron transfer (IET) usually relies on a mediated mechanism using hydrogen and/or formate as shuttling molecules, while cocultures with Geobacter species use a direct mechanism. Most EET mechanisms transport extracellular electrons only over micrometer-scale distances, but marine “cable bacteria” have been proven to have the exceptional capacity to transport electrons transport over centimeter-long distances. This chapter provides an overview of the current knowledge on EET mechanisms of anodic and cathodic biofilms, while also the mechanisms of IET are shortly discussed.