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 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 Jean Remi 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 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 Jean Remi Meysman

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

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.

Originalsprog	Engelsk
Artikelnummer	3996
Tidsskrift	Nature Communications
Vol/bind	12
Nummer	1
ISSN	2041-1723
DOI	https://doi.org/10.1038/s41467-021-24312-4
Status	Udgivet - 28 jun. 2021

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Boschker, H. T. S., Cook, P. L. M., Polerecky, L., Thiruvallur Eachambadi, R., Lozano, H., Hidalgo-Martinez, S., Khalenkow, D., Spampinato, V., Claes, N., Kundu, P., Wang, D., Bals, S., Sand, 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), Artikel 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 {Thiruvallur Eachambadi}, Raghavendran 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 Karina Sand 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 Jean Remi}",

year = "2021",

month = jun,

day = "28",

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

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Boschker, HTS, Cook, PLM, Polerecky, L, Thiruvallur Eachambadi, R, Lozano, H, Hidalgo-Martinez, S, Khalenkow, D, Spampinato, V, Claes, N, Kundu, P, Wang, D, Bals, S, Sand, K, 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, bind 12, nr. 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 - Thiruvallur Eachambadi, Raghavendran

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

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 Jean Remi

PY - 2021/6/28

Y1 - 2021/6/28

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 - Journal article

C2 - 34183682

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

Abstract

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