Efficient long-range conduction in cable bacteria through nickel protein wires
Boschker, Henricus T.S.; Cook, Perran L.M.; Polerecky, Lubos; Eachambadi, Raghavendran Thiruvallur; Lozano, Helena; Hidalgo-Martinez, Silvia; Khalenkow, Dmitry; Spampinato, Valentina; Claes, Nathalie; Kundu, Paromita; Wang, Da; Bals, Sara; Sand, Karina K.; Cavezza, Francesca; Hauffman, Tom; Bjerg, Jesper Tataru; Skirtach, Andre G.; Kochan, Kamila; McKee, Merrilyn; Wood, Bayden; Bedolla, Diana; Gianoncelli, Alessandra; Geerlings, Nicole M.J.; Van Gerven, Nani; Remaut, Han; Geelhoed, Jeanine S.; Millan-Solsona, Ruben; Fumagalli, Laura; Nielsen, Lars Peter; Franquet, Alexis; Manca, Jean V.; Gomila, Gabriel; Meysman, Filip J.R.
(2021) Nature Communications, volume 12, issue 1, pp. 1 - 12
(Article)
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,
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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.
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Keywords: General Chemistry, General Biochemistry,Genetics and Molecular Biology, General Physics and Astronomy
ISSN: 2041-1723
Publisher: Nature Publishing Group
Note: Funding Information: The authors thank Marlies Neiemeisland for assistance with Raman microscopy, Michiel Kienhuis for assistance with NanoSIMS analysis, Peter Hildebrandt and Diego Millo for helping with the interpretation of the Raman spectra, IONTOF for the Orbitrap Hybrid-SIMS analysis, and Rene Fabregas for helping with finite-element numerical modeling for SDM. H.T.S.B. and F.J.R.M. were financially supported by the Netherlands Organization for Scientific Research (VICI grant 016.VICI.170.072). Research Foundation Flanders supported F.J.R.M., J.V.M., and R.T.E. through FWO grant G031416N, and F.J.R.M. and J.S.G. through FWO grant G038819N. N.M.J.G. is the recipient of a Ph.D. scholarship for teachers from NWO in the Netherlands (grant 023.005.049). The NanoSIMS facility at Utrecht University was financed through a large infrastructure grant by the Netherlands Organization for Scientific Research (NWO, grant no. 175.010.2009.011) and through a Research Infrastructure Fund by the Utrecht University Board. A.G.S. is supported by the Special Research Fund (BOF) of Ghent University (BOF14/IOP/003, BAS094-18, 01IO3618) and FWO (G043219). The ToF-SIMS was funded by FWO Hercules grant (ZW/13/07) to J.V.M. and A.F. H.L., R.M.S., and G.G. were funded by the European Union H2020 Framework Programme (MSCA-ITN-2016) under grant agreement n 721874.EU, the Spanish Agencia Estatal de Investigación and EU FEDER under grant agreements TEC2016-79156-P and TEC2015-72751-EXP, the Generalitat de Catalunya through 2017-SGR1079 grant and CERCA Program. G.G. was recipient of an ICREA Academia Award, and H.L. of a FPI fellowship (BES-2015-074799) from the Agencia Estatal de Investigación/Fondo Social Europeo. L.F. received funding from the European Research Council (grant agreement No. 819417) under the European Union’s Horizon 2020 research and innovation programme. Publisher Copyright: © 2021, The Author(s).
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