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

Henricus T.S. Boschker; Perran L.M. Cook; Lubos Polerecky; Raghavendran Thiruvallur Eachambadi; Helena Lozano; Silvia Hidalgo-Martinez; Dmitry Khalenkow; Valentina Spampinato; Nathalie Claes; Paromita Kundu; Da Wang; Sara Bals; Karina K. Sand; Francesca Cavezza; Tom Hauffman; Jesper Tataru Bjerg; Andre G. Skirtach; Kamila Kochan; Merrilyn McKee; Bayden Wood; Diana Bedolla; Alessandra Gianoncelli; Nicole M.J. Geerlings; Nani Van Gerven; Han Remaut; Jeanine S. Geelhoed; Ruben Millan-Solsona; Laura Fumagalli; Lars Peter Nielsen; Alexis Franquet; Jean V. Manca; Gabriel Gomila; Filip J.R. Meysman

doi:10.1038/s41467-021-24312-4

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

Henricus T.S. Boschker, Perran L.M. Cook, Lubos Polerecky, Raghavendran Thiruvallur Eachambadi, Helena Lozano, Silvia Hidalgo-Martinez, Dmitry Khalenkow, Valentina Spampinato, Nathalie Claes, Paromita Kundu, Da Wang, Sara Bals, Karina K. Sand, Francesca Cavezza, Tom Hauffman, Jesper Tataru Bjerg, Andre G. Skirtach, Kamila Kochan, Merrilyn McKee, Bayden WoodDiana Bedolla, Alessandra Gianoncelli, Nicole M.J. Geerlings, Nani Van Gerven, Han Remaut, Jeanine S. Geelhoed, Ruben Millan-Solsona, Laura Fumagalli, Lars Peter Nielsen, Alexis Franquet, Jean V. Manca, Gabriel Gomila, Filip J.R. Meysman

Functional Atomic Force Microscopy Group

Research output: Contribution to journal › Article › peer-review

50 Scopus citations

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.

Original language	English
Article number	3996
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-24312-4
State	Published - Dec 1 2021

Funding

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.

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Boschker, H. T. S., Cook, P. L. M., Polerecky, L., Eachambadi, R. T., Lozano, H., Hidalgo-Martinez, S., Khalenkow, D., Spampinato, V., Claes, N., Kundu, P., Wang, D., Bals, S., Sand, K. K., Cavezza, F., Hauffman, T., Bjerg, J. T., Skirtach, A. G., Kochan, K., McKee, M., ... Meysman, F. J. R. (2021). Efficient long-range conduction in cable bacteria through nickel protein wires. Nature Communications, 12(1), Article 3996. https://doi.org/10.1038/s41467-021-24312-4

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title = "Efficient long-range conduction in cable bacteria through nickel protein wires",

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.",

author = "Boschker, {Henricus T.S.} and Cook, {Perran L.M.} and Lubos Polerecky and Eachambadi, {Raghavendran Thiruvallur} and Helena Lozano and Silvia Hidalgo-Martinez and Dmitry Khalenkow and Valentina Spampinato and Nathalie Claes and Paromita Kundu and Da Wang and Sara Bals and Sand, {Karina K.} and Francesca Cavezza and Tom Hauffman and Bjerg, {Jesper Tataru} and Skirtach, {Andre G.} and Kamila Kochan and Merrilyn McKee and Bayden Wood and Diana Bedolla and Alessandra Gianoncelli and Geerlings, {Nicole M.J.} and {Van Gerven}, Nani and Han Remaut and Geelhoed, {Jeanine S.} and Ruben Millan-Solsona and Laura Fumagalli and Nielsen, {Lars Peter} and Alexis Franquet and Manca, {Jean V.} and Gabriel Gomila and Meysman, {Filip J.R.}",

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doi = "10.1038/s41467-021-24312-4",

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Boschker, HTS, Cook, PLM, Polerecky, L, Eachambadi, RT, Lozano, H, Hidalgo-Martinez, S, Khalenkow, D, Spampinato, V, Claes, N, Kundu, P, Wang, D, Bals, S, Sand, KK, Cavezza, F, Hauffman, T, Bjerg, JT, Skirtach, AG, Kochan, K, McKee, M, Wood, B, Bedolla, D, Gianoncelli, A, Geerlings, NMJ, Van Gerven, N, Remaut, H, Geelhoed, JS, Millan-Solsona, R, Fumagalli, L, Nielsen, LP, Franquet, A, Manca, JV, Gomila, G & Meysman, FJR 2021, 'Efficient long-range conduction in cable bacteria through nickel protein wires', Nature Communications, vol. 12, no. 1, 3996. https://doi.org/10.1038/s41467-021-24312-4

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T1 - Efficient long-range conduction in cable bacteria through nickel protein wires

AU - Boschker, Henricus T.S.

AU - Cook, Perran L.M.

AU - Polerecky, Lubos

AU - Eachambadi, Raghavendran Thiruvallur

AU - Lozano, Helena

AU - Hidalgo-Martinez, Silvia

AU - Khalenkow, Dmitry

AU - Spampinato, Valentina

AU - Claes, Nathalie

AU - Kundu, Paromita

AU - Wang, Da

AU - Bals, Sara

AU - Sand, Karina K.

AU - Cavezza, Francesca

AU - Hauffman, Tom

AU - Bjerg, Jesper Tataru

AU - Skirtach, Andre G.

AU - Kochan, Kamila

AU - McKee, Merrilyn

AU - Wood, Bayden

AU - Bedolla, Diana

AU - Gianoncelli, Alessandra

AU - Geerlings, Nicole M.J.

AU - Van Gerven, Nani

AU - Remaut, Han

AU - Geelhoed, Jeanine S.

AU - Millan-Solsona, Ruben

AU - Fumagalli, Laura

AU - Nielsen, Lars Peter

AU - Franquet, Alexis

AU - Manca, Jean V.

AU - Gomila, Gabriel

AU - Meysman, Filip J.R.

PY - 2021/12/1

Y1 - 2021/12/1

N2 - 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.

AB - 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.

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U2 - 10.1038/s41467-021-24312-4

DO - 10.1038/s41467-021-24312-4

M3 - Article

C2 - 34183682

AN - SCOPUS:85109790725

SN - 2041-1723

VL - 12

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 3996

ER -

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

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