Filamentous cable bacteria display long-range electron transport

Long-distance electrical conductance in marine sediment in the ocean floor has been observed since a decade. While bacterial nanowires, humus particles and semi-conductive mineral grains were known to conduct electrons over nanometre to micrometre distances, in 2012 it was demonstrated that filamentous bacteria, now called cable bacteria, can transport electrons over centimetre distances, with a conductivity exceptionally high for a biological material. It was recently shown that the cable bacteria contain a conductive fiber network in their cell envelope, which is called fiber sheath (Figures 1a, 1b and 1c). This discovery has been a major surprise in the microbiology field. Indeed, the possibility and availability of bio-based materials with exceptional electrical properties could push material science and electronics far beyond their current limits. To do so, it is important to investigate the cable bacteria’s chemical structure and the underlying electron transport mechanism.
However, cable bacteria cannot be easily cultured, posing a limitation on the available biomass material to be studied, especially with traditional bulk techniques. In the present work, coordinated by the Department of Biotechnology of Delft University of Technology (Delft, The Netherlands) and by the Microbial Systems Technology Excellence Centre of the University of Antwerp (Belgium), a plethora of high sensitivity and high resolution analytical methods, including synchrotron Soft X-ray Microscopy and low energy X-ray Fluorescence at the TwinMic beamline of Elettra, was thus used to investigate the chemical structure and composition of such fascinating bacteria.
Even though the geometrical configuration of this fiber network was already known, the combination of High Angle Annular Dark Field–Scanning Transmission Electron Microscopy (HAADF-STEM), Atomic Force Microscopy–IR spectroscopy (AFM-IR) and Time of Flight-Secondary Ion Mass Spectrometry (ToF-SIMS) analysis provided further details, showing that the conductive fibers are positioned in a regular parallel pattern on the outside of the fiber sheath and these fibers consist of protein and the sheath is rich in polysaccharide. Raman microscopy, which was also applied to gain further insight into the composition of the conductive fibers, demonstrated the presence of a sulfur-ligated metal group in the fiber sheath.
Together, the STEM-EDX and LEXRF data suggested that Ni is the most likely candidate for the metal contained in the sulfur-ligated group. This conclusion was furtherly supported ToF-SIMS and high resolution NanoSIM.
In particular, Synchrotron Low-Energy X-ray Fluorescence (LEXRF) at TwinMic showed that Ni counts were similar in intact bacteria and fiber sheaths (Figure 1d and 1e), thus providing further support that Ni is concentrated in the fiber sheath.
Overall, the results indicate that electrical conductivity in cable bacteria occurs through proteins with Ni-dependent cofactors. The observation that Ni plays a crucial role in long-range biological conduction is remarkable and surprising, since biological electron transport typically involves Fe and Cu metalloproteins, while Nickel acts as a catalytic center in only nine enzymes, which are mostly involved in the metabolism of gases, but not in electron transport.
The exact mechanism of electron transport in the periplasmic fibers of cable bacteria remains still unclear and should be further investigated, but our results indicate that the novel Ni cofactor is definitely an essential component. A bio-material that presents these extraordinary electrical properties opens new potential applications in bio-electronics. 

Figure 1.  Schematic view of cable bacteria fiber sheath (a); Absorption (b) and differential phase (c) images of a bundle of cable bacteria fiber sheaths; Fe, Ni and scattering peak distribution in intact cable bacteria (d) and B fiber sheaths (e). Panel b, c, d and e were acquired at TwinMic beamline at 1.1 keV, with a spatial resolution of 200nm (b and c) and 400nm (d and e).

This research was conducted by the following research team:

Henricus T. S. Boschker^1,2, Perran L.M. Cook³, Nicole Geerlings⁴, Silvia Hidalgo Martinez², Raghavendran Thiruvallur Eachambadi⁵, Dmitry Khalenkow⁶, Valentina Spampinato⁷, Natalie Claes⁸, Paromita Kundu⁸, Da Wang⁸,  Sara Bals⁸, Karina K. Sand⁹, Francesca Cavezza¹⁰, Tom Hauffman¹⁰, Jesper Tataru Bjerg¹¹, Andre Skirtach⁶,Kamila Kochan³,Bayden Wood³, Diana Bedolla¹², Alessandra Gianoncelli¹², Lubos Polerecky⁴, Nani Van Gerven¹³, Han Remaut¹³, Jeanine Geelhoed², Lars-Peter Nielsen¹¹, Alexis Franquet⁷, Jean Manca⁵, Filip J. R. Meysman^2,1

¹ Department of Biotechnology, Delft University of Technology, Delft, The Netherlands
² ECOBE, Department of Biology, University of Antwerp, Wilrijk, Belgium
³ Water Studies Center, School of Chemistry, Monash University, Australia
⁴ Geochemistry, Department of Earth Sciences, Utrecht University, Utrecht, Netherlands
⁵ X-LAB, Hasselt University, Hasselt, Belgium
⁶ Department of Molecular Biotechnology, University of Ghent, Ghent, Belgium
⁷ IMEC, Kapeldreef 75, Leuven, Belgium 
⁸ Electron Microscopy for Materials Research (EMAT), University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium
⁹ Nano-Science Center, Department of Chemistry, University of Copenhagen, Copenhagen, Denmark
¹⁰ Department of Electrochemical and Surface Engineering, SURF Research Group, Vrije Universiteit Brussel, 2 Pleinlaan, B-1050, Brussels, Belgium
¹¹ Department of Biosciences-Microbiology and Center for Electromicrobiology, Department of Bioscience, Aarhus University, Aarhus C, Denmark
¹² Elettra-Sincrotrone Trieste S.C.p.A., Strada Statale 14 - km 163,5 in AREA Science Park, 34149 Trieste, Italy
¹³ VIB-VUB Center for Structural Biology, Vrije Universiteit Brussel, Building E, Pleinlaan 2, 1050 BRUSSEL

Contact persons:

Eric Boschker, email:
Filip Meysman, email:
Alessandra Gianoncelli, email:
Diana Bedolla, email: