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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 conduct electrical currents over centimeter distances through fibers embedded in their cell envelope. Here, Boschker et al. show that the fibers consist of a conductive core containing nickel proteins that is surrounded by an insulating protein shell.
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1 Delft University of Technology, Department of Biotechnology, Delft, The Netherlands (GRID:grid.5292.c) (ISNI:0000 0001 2097 4740); University of Antwerp, Microbial Systems Technology Excellence Centre, Wilrijk, Belgium (GRID:grid.5284.b) (ISNI:0000 0001 0790 3681)
2 Monash University, School of Chemistry, Clayton, Australia (GRID:grid.1002.3) (ISNI:0000 0004 1936 7857)
3 Faculty of Geosciences, Utrecht University, Department of Earth Sciences—Geochemistry, Utrecht, The Netherlands (GRID:grid.5477.1) (ISNI:0000000120346234)
4 Hasselt University, X-LAB, Faculty of Sciences, Diepenbeek, Belgium (GRID:grid.12155.32) (ISNI:0000 0001 0604 5662)
5 Nanoscale Bioelectrical Characterization, Institut de Bioenginyeria de Catalunya (IBEC), The Barcelona Institute of Science and Technology, Barcelona, Spain (GRID:grid.424736.0) (ISNI:0000 0004 0536 2369)
6 University of Antwerp, Microbial Systems Technology Excellence Centre, Wilrijk, Belgium (GRID:grid.5284.b) (ISNI:0000 0001 0790 3681)
7 University of Ghent, Department of Biotechnology, Ghent, Belgium (GRID:grid.5342.0) (ISNI:0000 0001 2069 7798)
8 IMEC, Leuven, Belgium (GRID:grid.15762.37) (ISNI:0000 0001 2215 0390)
9 University of Antwerp, Electron Microscopy for Materials Research (EMAT), Antwerp, Belgium (GRID:grid.5284.b) (ISNI:0000 0001 0790 3681)
10 University of Copenhagen, Department of Chemistry, Nano-Science Center, Copenhagen, Denmark (GRID:grid.5254.6) (ISNI:0000 0001 0674 042X)
11 Vrije Universiteit Brussel, Research Group Electrochemical and Surface Engineering, Department Materials and Chemistry, Brussels, Belgium (GRID:grid.8767.e) (ISNI:0000 0001 2290 8069)
12 University of Antwerp, Microbial Systems Technology Excellence Centre, Wilrijk, Belgium (GRID:grid.5284.b) (ISNI:0000 0001 0790 3681); Aarhus University, Microbiology, Department of Biology, Aarhus, Denmark (GRID:grid.7048.b) (ISNI:0000 0001 1956 2722); Aarhus University, Center for Electromicrobiology, Department of Biology, Aarhus, Denmark (GRID:grid.7048.b) (ISNI:0000 0001 1956 2722)
13 Elettra-Sincrotrone Trieste S.C.p.A., Trieste, Italy (GRID:grid.5942.a) (ISNI:0000 0004 1759 508X)
14 VIB-VUB Center for Structural Biology, Flanders Institute for Biotechnology (VIB), Brussels, Belgium (GRID:grid.11486.3a) (ISNI:0000000104788040); Structural Biology Brussels, Vrije Universiteit Brussel, Brussels, Belgium (GRID:grid.8767.e) (ISNI:0000 0001 2290 8069)
15 Nanoscale Bioelectrical Characterization, Institut de Bioenginyeria de Catalunya (IBEC), The Barcelona Institute of Science and Technology, Barcelona, Spain (GRID:grid.424736.0) (ISNI:0000 0004 0536 2369); Universitat de Barcelona, Departament d’Enginyeria Electrònica i Biomèdica, Barcelona, Spain (GRID:grid.5841.8) (ISNI:0000 0004 1937 0247)
16 University of Manchester, Department of Physics and Astronomy, Manchester, UK (GRID:grid.5379.8) (ISNI:0000000121662407); National Graphene Institute, University of Manchester, Manchester, UK (GRID:grid.5379.8) (ISNI:0000000121662407)
17 Aarhus University, Microbiology, Department of Biology, Aarhus, Denmark (GRID:grid.7048.b) (ISNI:0000 0001 1956 2722); Aarhus University, Center for Electromicrobiology, Department of Biology, Aarhus, Denmark (GRID:grid.7048.b) (ISNI:0000 0001 1956 2722)