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
Pages (from-to)	1-1é
Number of pages	12
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-24312-4
Publication status	Published - 1 Dec 2021

Keywords

Bacterial Proteins/chemistry
Deltaproteobacteria/metabolism
Electric Conductivity
Electricity
Electron Transport/physiology
Nickel/chemistry

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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), 1-1é. [3996]. https://doi.org/10.1038/s41467-021-24312-4

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. / Efficient long-range conduction in cable bacteria through nickel protein wires. In: Nature Communications. 2021 ; Vol. 12, No. 1. pp. 1-1é.

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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.",

keywords = "Bacterial Proteins/chemistry, Deltaproteobacteria/metabolism, Electric Conductivity, Electricity, Electron Transport/physiology, Nickel/chemistry",

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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, pp. 1-1é. https://doi.org/10.1038/s41467-021-24312-4

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.

In: Nature Communications, Vol. 12, No. 1, 3996, 01.12.2021, p. 1-1é.

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

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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.

KW - Bacterial Proteins/chemistry

KW - Deltaproteobacteria/metabolism

KW - Electric Conductivity

KW - Electricity

KW - Electron Transport/physiology

KW - Nickel/chemistry

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U2 - 10.1038/s41467-021-24312-4

DO - 10.1038/s41467-021-24312-4

M3 - Article

C2 - 34183682

VL - 12

SP - 1-1é

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 3996

ER -

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

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