Highly efficient bio-catalytic oxygen reduction coupled to long-range electron transport in cable bacteria

Multicellular cable bacteria are capable of transferring electrons over centimeter distances through an internal array of conductive fibers. These long, filamentous bacteria function as a living electrochemical cell, performing sulfide reduction at one end and oxygen reduction at the other end. To investigate how O2 reduction is linked to the long-distance electron transport along the conductive fibers, we performed a detailed electrochemical characterization of native filaments as well as extracted "fiber skeletons" without membranes or cytoplasm. Our data show that fibers skeletons only perform longitudinal electron transport and are not electrochemically active towards oxygen. This opposes a previous proposition that the conductive fiber network displays electrocatalytic behavior towards oxygen. Still, native cable bacterium filaments are capable of high oxygen reduction rates, thus demonstrating that dedicated enzyme systems in the periplasm or inner membrane are responsible for O2 reduction. Together, our data provide empirical support for a model in which diffusible c-type cytochromes mediate electron transport through the periplasm, shuttling electrons between separate respiratory complexes and the conductive fiber network. As such, our study resolves a crucial aspect of the unique electrogenic metabolism in cable bacteria, and clarifies the application potential of the highly conductive fibers in Bio-electrochemical System technologies.