A highly conductive fibre network enables centimetre-scale electron transport in multicellular cable bacteria

Abstract

Biological electron transport is classically thought to occur over nanometre distances, yet recent studies suggest that electrical currents can run along centimetre-long cable bacteria. The phenomenon remains elusive, however, as currents have not been directly measured, nor have the conductive structures been identified. Here we demonstrate that cable bacteria conduct electrons over centimetre distances via highly conductive fibres embedded in the cell envelope. Direct electrode measurements reveal nanoampere currents in intact filaments up to 10.1 mm long (>2000 adjacent cells). A network of parallel periplasmic fibres displays a high conductivity (up to 79 S cm−1), explaining currents measured through intact filaments. Conductance rapidly declines upon exposure to air, but remains stable under vacuum, demonstrating that charge transfer is electronic rather than ionic. Our finding of a biological structure that efficiently guides electrical currents over long distances greatly expands the paradigm of biological charge transport and could enable new bio-electronic applications.

Inducing the attachment of cable bacteria on oxidizing electrodes

“…A 3 mM standard solution was made from crystal Na 2 S9H 2 O (> 98.0 %, MilliporeSigma, Burlington, MA) in an anoxic glove box. Total sulfide concentration at each profile depth was derived from pH and H 2 S according to equilibrium relationships given in Millero et al (1988).…”

Challenges in engineering conductive protein fibres: Disentangling the knowledge

“…Microbial species have been shown to wire their intracellular metabolic processes to external electron sinks such as metal ions or other microorganisms. [5][6][7][8][9][10][11][12][13] While some microorganisms, such as Shewanella, are believed to use mobile charge shuttles, [14][15][16] others produce intrinsically conductive extracellular protein structures that enable long-range conduction. [5,6,12,17] Of particular interest are the protein fibres of Geobacter, also referred to as pili, with conductivity comparable to that of organic conductive polymers.…”

Cable Bacteria as Long-Range Biological Semiconductors

“…Microscopy investigations reveal that all cells within a cable bacterium filament share a common space within the cell envelope, and that a network of parallel fibres run within this periplasmic space along the whole filament 12,13 . These fibres were confirmed as the primary conductive structures inside cable bacteria 4 and their conductivity exceeds 10 S/cm ( Figure 1a). Yet, the underlying electron transport mechanism remains currently undisclosed.…”

“…For all electrical measurements, the substrate was placed at a probe station with two needle probes connecting to the two electrodes. In the Direct Current measurements, the probe station was connected to a Keithley 2450A sourcemeter (Keithley, USA) with triax cables, driven by the multi-tool control software SweepMe, as described in Meysman et al 4 . For AC impedance measurements, the sample is probed with a VersaSTAT3F potentiostat (Ametek, USA), allowing impedance measurements in the range 1 MHz to 100 mHz.…”