Long-Distance Electron Transport in Multicellular Freshwater Cable Bacteria

Abstract Filamentous multicellular cable bacteria perform centimeter-scale electron transport in a process that couples oxidation of an electron donor (sulfide) in deeper sediment to the reduction of an electron acceptor (oxygen or nitrate) near the surface. While this electric metabolism is prevalent in both marine and freshwater sediments, detailed electronic measurements of the conductivity previously focused on the marine cable bacteria ( Candidatus Electrothrix), rather than freshwater cable bacteria, which form a separate genus ( Candidatus Electronema) and contribute essential geochemical roles in freshwater sediments. Here, we characterize the electron transport characteristics of Ca. Electronema cable bacteria from Southern California freshwater sediments. Current-voltage measurements of intact cable filaments bridging interdigitated electrodes confirmed their persistent conductivity under a controlled atmosphere and the variable sensitivity of this conduction to air exposure. Electrostatic and conductive atomic force microscopies mapped out the characteristics of the cell envelope’s nanofiber network, implicating it as the conductive pathway in a manner consistent with previous findings in marine cable bacteria. Four-probe measurements of microelectrodes addressing intact cables demonstrated nanoampere currents up to 200 μm lengths at modest driving voltages, allowing us to quantify the nanofiber conductivity at 0.1 S/cm for freshwater cable bacteria filaments under our measurement conditions. Such a high conductivity can support the remarkable sulfide-to-oxygen electrical currents mediated by cable bacteria in sediments. These measurements expand the knowledgebase of long-distance electron transport to the freshwater niche while shedding light on underlying conductive network of cable bacteria. Significance Cable bacteria are multicellular filaments composed of up-to-thousands of end-to-end cells and are found worldwide in both marine and freshwater sediments. Remarkably, these cells gain energy from a long-distance electron transport process that carries electrons generated by sulfide oxidation in deeper sediment layers to drive oxygen reduction near the sediment-water interface. This electric metabolism requires an unusually high electronic conductivity, previously thought impossible in natural biological materials. However, the underlying mechanism(s) remain poorly understood, and previous characterization of the conductivity largely focused on marine cable bacteria. Here, we characterize and quantify the electronic conductivity of freshwater cable bacteria from sediments in Southern California, with emphasis on the role of the conductive periplasmic fiber network in routing electron transport along cables.