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.

Details

Title
Efficient long-range conduction in cable bacteria through nickel protein wires
Author
Boschker Henricus T S 1   VIAFID ORCID Logo  ; Cook Perran L M 2   VIAFID ORCID Logo  ; Polerecky Lubos 3   VIAFID ORCID Logo  ; Eachambadi Raghavendran Thiruvallur 4   VIAFID ORCID Logo  ; Lozano, Helena 5   VIAFID ORCID Logo  ; Hidalgo-Martinez, Silvia 6 ; Khalenkow Dmitry 7 ; Spampinato Valentina 8 ; Claes Nathalie 9   VIAFID ORCID Logo  ; Kundu Paromita 9 ; Wang, Da 9 ; Bals, Sara 9   VIAFID ORCID Logo  ; Sand, Karina K 10   VIAFID ORCID Logo  ; Cavezza Francesca 11 ; Hauffman, Tom 11   VIAFID ORCID Logo  ; Bjerg, Jesper Tataru 12 ; Skirtach, Andre G 7   VIAFID ORCID Logo  ; Kochan Kamila 2 ; McKee Merrilyn 2 ; Wood Bayden 2   VIAFID ORCID Logo  ; Bedolla, Diana 13   VIAFID ORCID Logo  ; Gianoncelli Alessandra 13   VIAFID ORCID Logo  ; Geerlings Nicole M J 3 ; Nani, Van Gerven 14 ; Han, Remaut 14 ; Geelhoed, Jeanine S 6   VIAFID ORCID Logo  ; Millan-Solsona Ruben 15   VIAFID ORCID Logo  ; Fumagalli, Laura 16   VIAFID ORCID Logo  ; Nielsen, Lars Peter 17   VIAFID ORCID Logo  ; Franquet Alexis 8 ; Manca, Jean V 4   VIAFID ORCID Logo  ; Gomila Gabriel 15 ; Meysman Filip J R 1   VIAFID ORCID Logo 

 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) 
 Monash University, School of Chemistry, Clayton, Australia (GRID:grid.1002.3) (ISNI:0000 0004 1936 7857) 
 Faculty of Geosciences, Utrecht University, Department of Earth Sciences—Geochemistry, Utrecht, The Netherlands (GRID:grid.5477.1) (ISNI:0000000120346234) 
 Hasselt University, X-LAB, Faculty of Sciences, Diepenbeek, Belgium (GRID:grid.12155.32) (ISNI:0000 0001 0604 5662) 
 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) 
 University of Antwerp, Microbial Systems Technology Excellence Centre, Wilrijk, Belgium (GRID:grid.5284.b) (ISNI:0000 0001 0790 3681) 
 University of Ghent, Department of Biotechnology, Ghent, Belgium (GRID:grid.5342.0) (ISNI:0000 0001 2069 7798) 
 IMEC, Leuven, Belgium (GRID:grid.15762.37) (ISNI:0000 0001 2215 0390) 
 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) 
Publication year
2021
Publication date
2021
Publisher
Nature Publishing Group
e-ISSN
20411723
Source type
Scholarly Journal
Language of publication
English
ProQuest document ID
2545794957
Copyright
© The Author(s) 2021. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.