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

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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.

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
Externally published	Yes

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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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year = "2021",

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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

TY - JOUR

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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