Henricus T S Boschker1,2, Perran L M Cook3, Lubos Polerecky4, Raghavendran Thiruvallur Eachambadi5, Helena Lozano6, Silvia Hidalgo-Martinez7, Dmitry Khalenkow8, Valentina Spampinato9, Nathalie Claes10, Paromita Kundu10, Da Wang10, Sara Bals10, Karina K Sand11, Francesca Cavezza12, Tom Hauffman12, Jesper Tataru Bjerg7,13,14, Andre G Skirtach8, Kamila Kochan3, Merrilyn McKee3, Bayden Wood3, Diana Bedolla15, Alessandra Gianoncelli15, Nicole M J Geerlings4, Nani Van Gerven16,17, Han Remaut16,17, Jeanine S Geelhoed7, Ruben Millan-Solsona6,18, Laura Fumagalli19,20, Lars Peter Nielsen13,14, Alexis Franquet9, Jean V Manca5, Gabriel Gomila6,18, Filip J R Meysman21,22. 1. Department of Biotechnology, Delft University of Technology, Delft, The Netherlands. h.t.s.boschker@tudelft.nl. 2. Microbial Systems Technology Excellence Centre, University of Antwerp, Wilrijk, Belgium. h.t.s.boschker@tudelft.nl. 3. School of Chemistry, Monash University, Clayton, Australia. 4. Department of Earth Sciences-Geochemistry, Faculty of Geosciences, Utrecht University, Utrecht, The Netherlands. 5. X-LAB, Faculty of Sciences, Hasselt University, Diepenbeek, Belgium. 6. Nanoscale Bioelectrical Characterization, Institut de Bioenginyeria de Catalunya (IBEC), The Barcelona Institute of Science and Technology, Barcelona, Spain. 7. Microbial Systems Technology Excellence Centre, University of Antwerp, Wilrijk, Belgium. 8. Department of Biotechnology, University of Ghent, Ghent, Belgium. 9. IMEC, Leuven, Belgium. 10. Electron Microscopy for Materials Research (EMAT), University of Antwerp, Antwerp, Belgium. 11. Department of Chemistry, Nano-Science Center, University of Copenhagen, Copenhagen, Denmark. 12. Research Group Electrochemical and Surface Engineering, Department Materials and Chemistry, Vrije Universiteit Brussel, Brussels, Belgium. 13. Microbiology, Department of Biology, Aarhus University, Aarhus, Denmark. 14. Center for Electromicrobiology, Department of Biology, Aarhus University, Aarhus, Denmark. 15. Elettra-Sincrotrone Trieste S.C.p.A., Trieste, Italy. 16. VIB-VUB Center for Structural Biology, Flanders Institute for Biotechnology (VIB), Brussels, Belgium. 17. Structural Biology Brussels, Vrije Universiteit Brussel, Brussels, Belgium. 18. Departament d'Enginyeria Electrònica i Biomèdica, Universitat de Barcelona, Barcelona, Spain. 19. Department of Physics and Astronomy, University of Manchester, Manchester, UK. 20. National Graphene Institute, University of Manchester, Manchester, UK. 21. Department of Biotechnology, Delft University of Technology, Delft, The Netherlands. filip.meysman@uantwerpen.be. 22. Microbial Systems Technology Excellence Centre, University of Antwerp, Wilrijk, Belgium. filip.meysman@uantwerpen.be.
Abstract
Filamentous cable bacteria display long-range electron transport, generating electrical currents over centimeter distances through a highly ordered network of fibers embedded in their cell envelope. The conductivity of these periplasmic wires is exceptionally high for a biological material, but their chemical structure and underlying electron transport mechanism remain unresolved. Here, we combine high-resolution microscopy, spectroscopy, and chemical imaging on individual cable bacterium filaments to demonstrate that the periplasmic wires consist of a conductive protein core surrounded by an insulating protein shell layer. The core proteins contain a sulfur-ligated nickel cofactor, and conductivity decreases when nickel is oxidized or selectively removed. The involvement of nickel as the active metal in biological conduction is remarkable, and suggests a hitherto unknown form of electron transport that enables efficient conduction in centimeter-long protein structures.
Filamentous cable bacteria display long-range electron transport, generating electricnclass="Chemical">alclass="Chemical">n class="Chemical">currents over centimeter distances through a highly ordered network of fibers embedded in their cell envelope. The conductivity of these periplasmic wires is exceptionally high for a biological material, but their chemical structure and underlying electron transport mechanism remain unresolved. Here, we combine high-resolution microscopy, spectroscopy, and chemical imaging on individual cable bacterium filaments to demonstrate that the periplasmic wires consist of a conductive protein core surrounded by an insulating protein shell layer. The core proteins contain a sulfur-ligated nickelcofactor, and conductivity decreases when nickel is oxidized or selectively removed. The involvement of nickel as the active metal in biologicalconduction is remarkable, and suggests a hitherto unknown form of electron transport that enables efficient conduction in centimeter-long protein structures.
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