The Cell Envelope Structure of Cable Bacteria

Cable bacteria are long, multicellular micro-organisms that are capable of transporting electrons from cell to cell along the longitudinal axis of their centimeter-long filaments. The conductive structures that mediate this long-distance electron transport are thought to be located in the cell envelope. Therefore, this study examines in detail the architecture of the cell envelope of cable bacterium filaments by combining different sample preparation methods (chemical fixation, resin-embedding, and cryo-fixation) with a portfolio of imaging techniques (scanning electron microscopy, transmission electron microscopy and tomography, focused ion beam scanning electron microscopy, and atomic force microscopy). We systematically imaged intact filaments with varying diameters. In addition, we investigated the periplasmic fiber sheath that remains after the cytoplasm and membranes were removed by chemical extraction. Based on these investigations, we present a quantitative structural model of a cable bacterium. Cable bacteria build their cell envelope by a parallel concatenation of ridge compartments that have a standard size. Larger diameter filaments simply incorporate more parallel ridge compartments. Each ridge compartment contains a ~50 nm diameter fiber in the periplasmic space. These fibers are continuous across cell-to-cell junctions, which display a conspicuous cartwheel structure that is likely made by invaginations of the outer cell membrane around the periplasmic fibers. The continuity of the periplasmic fibers across cells makes them a prime candidate for the sought-after electron conducting structure in cable bacteria

The cell envelope structure of cable bacteria

Cable bacteria are long, multicellular micro-organisms that are capable of transporting electrons from cell to cell along the longitudinal axis of their centimeter-long filaments. The conductive structures that mediate this long-distance electron transport are thought to be located in the cell envelope. Therefore, this study examines in detail the architecture of the cell envelope of cable bacterium filaments by combining different sample preparation methods (chemical fixation, resin-embedding, and cryo-fixation) with a portfolio of imaging techniques (scanning electron microscopy, transmission electron microscopy and tomography, focused ion beam scanning electron microscopy, and atomic force microscopy). We systematically imaged intact filaments with varying diameters. In addition, we investigated the periplasmic fiber sheath that remains after the cytoplasm and membranes were removed by chemical extraction. Based on these investigations, we present a quantitative structural model of a cable bacterium. Cable bacteria build their cell envelope by a parallel concatenation of ridge compartments that have a standard size. Larger diameter filaments simply incorporate more parallel ridge compartments. Each ridge compartment contains a similar to 50 nm diameter fiber in the periplasmic space. These fibers are continuous across cell-to-cell junctions, which display a conspicuous cartwheel structure that is likely made by invaginations of the outer cell membrane around the periplasmic fibers. The continuity of the periplasmic fibers across cells makes them a prime candidate for the sought-after electron conducting structure in cable bacteria

Intrinsic electrical properties of cable bacteria reveal an Arrhenius temperature dependence

Filamentous cable bacteria exhibit long-range electron transport over centimetre-scale distances, which takes place in a parallel fibre structure with high electrical conductivity. Still, the underlying electron transport mechanism remains undisclosed. Here we determine the intrinsic electrical properties of the conductive fibres in cable bacteria from a material science perspective. Impedance spectroscopy provides an equivalent electrical circuit model, which demonstrates that dry cable bacteria filaments function as resistive biological wires. Temperature-dependent electrical characterization reveals that the conductivity can be described with an Arrhenius-type relation over a broad temperature range (− 195 °C to + 50 °C), demonstrating that charge transport is thermally activated with a low activation energy of 40–50 meV. Furthermore, when cable bacterium filaments are utilized as the channel in a field-effect transistor, they show n-type transport suggesting that electrons are the charge carriers. Electron mobility values are ~ 0.1 cm2/Vs at room temperature and display a similar Arrhenius temperature dependence as conductivity. Overall, our results demonstrate that the intrinsic electrical properties of the conductive fibres in cable bacteria are comparable to synthetic organic semiconductor materials, and so they offer promising perspectives for both fundamental studies of biological electron transport as well as applications in microbial electrochemical technologies and bioelectronics.BT/Environmental Biotechnolog

An Ordered and Fail-Safe Electrical Network in Cable Bacteria

Cable bacteria are an emerging class of electroactive organisms that sustain unprecedented long-range electron transport across centimeter-scale distances. The local pathways of the electrical currents in these filamentous microorganisms remain unresolved. Here, the electrical circuitry in a single cable bacterium is visualized with nanoscopic resolution using conductive atomic force microscopy. Combined with perturbation experiments, it is demonstrated that electrical currents are conveyed through a parallel network of conductive fibers embedded in the cell envelope, which are electrically interconnected between adjacent cells. This structural organization provides a fail-safe electrical network for long-distance electron transport in these filamentous microorganisms. The observed electrical circuit architecture is unique in biology and can inspire future technological applications in bioelectronics.BT/Environmental Biotechnolog

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

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.BT/Environmental BiotechnologyBN/Bertus Beaumont LabQN/van der Zant La

DataSheet1_Characterisation of Two Wood-Waste and Coffee Bean Husk Biochars for the Removal of Micropollutants from Water.docx

The inclusion of bioaugmented low-cost biochar in current wastewater treatment technologies is a promising way to enhance the removal and degradation of emerging contaminants. In this paper, the properties of two wood waste biochars (wood waste mix - AB, and date palm fiber wood - PDF), and coffee bean husks (COF), produced at four temperatures (350, 450, 500, 550°C) were compared, and investigated in the presence of Geobacter sulfurreducens or a mixed freshwater stream bacterial culture to understand their potential for the adsorption and biotransformation of two types of pesticides (thiacloprid, pirimicarb), and two pharmaceuticals (ibuprofen, diclofenac). Biochar yield was similar for all three biochars and ranged between 30 and 35%. The ash content of PDF and COF was significantly higher than AB. pH and electrical conductivity (EC) were initially high for COF (pH: 7.4–8; EC: 3–4.27 mS/cm) and PDF (pH: 7.7–10.1; EC: 4–6.24 mS/cm) after 24 h, but stabilized at neutral pH and − (550°C), and 846 mg/L sulphate (350°C). Lower pyrolysis temperatures reduced leachable anions. The biochars were highly (ultra)microporous with little meso- and macroporosity. The adsorption experiments showed that AB and COF biochars were both suited to sorb more than 90% of the initially spiked 10 ppm pirimicarb, AB removed 50.2% of the initial diclofenac concentration compared to only 5% for the no-biochar control, and both biochars could remove about 55% of the initially spiked thiacloprid, and 40% of the ibuprofen. In the presence of a mixed culture, on average 30% more thiacloprid and ibuprofen was removed from the supernatant by AB and COF than the sterile control. This work shows that selected wood-waste feedstocks and low pyrolysis temperature can produce environmentally-safe biochars that have suitable characteristics to sorb emergent pollutants from water. These materials could be further studied in multi-pollution sorption/competition experiments, and in larger environmental wastewater treatment systems.</p