Cable bacteria form centimeter-long, multicellular filaments than can consist of ten thousands of cells. They evolved a unique energy metabolism that involves co-operation among cells that separately perform oxidation of the electron donor (sulfide, H2S) and reduction of the electron acceptor (oxygen, O2). This division of labor is facilitated via long-range electrical currents that run from cell to cell along a network of conductive fibers. This research provides further insights into the metabolism of these peculiar organisms. It was discovered that only the cells that oxidize sulfide have the capacity for growth whereas the cells that reduce oxygen serve to dispense electrons as quickly as possible without any growth. Thus, these oxygen-reducing cells appear to provide a kind of “community service” to the filament by ensuring an electron current without any capacity for growth. However, access to oxygen is essential for the survival of the filament and it appears to pace the cycles of growth and cell division among a filament where cell division is synchronized among cells within a filament. Cells residing in the oxic zone are believed to (temporarily) rely on storage compounds of which polyphosphate (poly-P) is most ubiquitously found in cable bacteria. Poly-P is an inorganic biopolymer that consists of tens to hundreds of phosphate residues linearly linked together by high-energy phosphoanhydride bonds. We found poly-P activity in almost all cable bacteria cells and it appears to have an essential role in the metabolic regulation of cable bacteria.