Efficient long-range conduction in cable bacteria through nickel protein wires

Author:

Boschker Henricus T. S.ORCID,Cook Perran L. M.ORCID,Polerecky LubosORCID,Eachambadi Raghavendran ThiruvallurORCID,Lozano HelenaORCID,Hidalgo-Martinez Silvia,Khalenkow Dmitry,Spampinato Valentina,Claes NathalieORCID,Kundu Paromita,Wang Da,Bals SaraORCID,Sand Karina K.ORCID,Cavezza Francesca,Hauffman TomORCID,Bjerg Jesper Tataru,Skirtach Andre G.ORCID,Kochan Kamila,McKee Merrilyn,Wood BaydenORCID,Bedolla DianaORCID,Gianoncelli AlessandraORCID,Geerlings Nicole M. J.,Van Gerven Nani,Remaut Han,Geelhoed Jeanine S.ORCID,Millan-Solsona RubenORCID,Fumagalli LauraORCID,Nielsen Lars PeterORCID,Franquet Alexis,Manca Jean V.ORCID,Gomila Gabriel,Meysman Filip J. R.ORCID

Abstract

AbstractFilamentous 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.

Funder

Nederlandse Organisatie voor Wetenschappelijk Onderzoek

Fonds Wetenschappelijk Onderzoek

EC | Horizon 2020 Framework Programme

Ministry of Economy and Competitiveness | Agencia Estatal de Investigación

Generalitat de Catalunya

Special Research Fund (BOF) of Ghent University

Publisher

Springer Science and Business Media LLC

Subject

General Physics and Astronomy,General Biochemistry, Genetics and Molecular Biology,General Chemistry

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