End-to-end contact enables long-distance electron transport between filaments in cable bacteria

Filamentous cable bacteria are capable of centimeter-scale long-distance electron transport and play crucial roles in the biogeochemistry of aquatic sediments. However, the mechanisms underlying long-distance electron transport remain incompletely understood. This study reports dynamic contacts between separate filaments of cable bacteria, enabling them to relay electrons between sulfidic and oxic zones. Video microscopy of motile filaments in a microchamber slide setup revealed that some filaments did not fully bridge the gap between the sulfidic and oxic zone, but made transient contact with each other. Contacts were always end-to-end and often occurred repeatedly, in which filaments always followed the same trajectory back and forth. The contact frequency gradually increased over the first 20 days, and then declined afterwards. About 5.5% of cable bacterium filaments were observed to engage in contact events during a 2-hour observation window on day 20. Confocal microscopy confirmed the presence of extracellular polymer substance trails between filaments, which appear to guide consecutive end-to-end contacts. In situ Raman spectroscopy showed that connections enabled redox continuity between reduced and oxidized filaments, thus suggesting inter-filament electron transfer during physical contact. This inter-filament electron transport represents a novel type of microbial cooperation, and appears to be a strategy for establishing optimal connections between spatially separated electron donors and acceptors in a dynamic sedimentary environment.