Cable bacteria are centimeter-long multicellular bacteria conducting electricity through periplasmic conductive fibers (PCFs). Using single-strain enrichments of the genera Electrothrix and Electronema we systematically investigate variations and similarities in morphology and electrical properties across both genera. Electrical conductivity of different PCFs spans three orders of magnitude warranting further investigations of the plasticity of their conduction machinery. Using electron microscopy and elemental analyses, we show that the two cable bacteria genera have similar cell envelopes and cell-cell junction ultrastructures. Iron, sulfur, and nickel signals are co-localized with the PCFs, indicating key functional roles of these elements. The PCFs are organized as stranded rope-like structures composed of multiple strands. Furthermore, we report lamellae-like structures formed at the cell-cell junctions with a core layer connecting to the PCFs, and intriguing vesicle-like inner membrane invaginations below the PCFs. Finally, using bioinformatic tools, we identify a cytochrome family with predicted structural homology to known multi-heme nanowire proteins from other electroactive microorganisms and suggest that these cytochromes can play a role in the extra- or intercellular electron conduction of cable bacteria.