Cargando…

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

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 thei...

Descripción completa

Detalles Bibliográficos
Autores principales: 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.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8238962/
https://www.ncbi.nlm.nih.gov/pubmed/34183682
http://dx.doi.org/10.1038/s41467-021-24312-4
_version_ 1783714985051947008
author 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.
author_facet 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.
author_sort Boschker, Henricus T. S.
collection PubMed
description 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.
format Online
Article
Text
id pubmed-8238962
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-82389622021-07-20 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. Nat Commun Article 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. Nature Publishing Group UK 2021-06-28 /pmc/articles/PMC8238962/ /pubmed/34183682 http://dx.doi.org/10.1038/s41467-021-24312-4 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
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
title Efficient long-range conduction in cable bacteria through nickel protein wires
title_full Efficient long-range conduction in cable bacteria through nickel protein wires
title_fullStr Efficient long-range conduction in cable bacteria through nickel protein wires
title_full_unstemmed Efficient long-range conduction in cable bacteria through nickel protein wires
title_short Efficient long-range conduction in cable bacteria through nickel protein wires
title_sort efficient long-range conduction in cable bacteria through nickel protein wires
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8238962/
https://www.ncbi.nlm.nih.gov/pubmed/34183682
http://dx.doi.org/10.1038/s41467-021-24312-4
work_keys_str_mv AT boschkerhenricusts efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT cookperranlm efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT polereckylubos efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT eachambadiraghavendranthiruvallur efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT lozanohelena efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT hidalgomartinezsilvia efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT khalenkowdmitry efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT spampinatovalentina efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT claesnathalie efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT kunduparomita efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT wangda efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT balssara efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT sandkarinak efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT cavezzafrancesca efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT hauffmantom efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT bjergjespertataru efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT skirtachandreg efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT kochankamila efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT mckeemerrilyn efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT woodbayden efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT bedolladiana efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT gianoncellialessandra efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT geerlingsnicolemj efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT vangervennani efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT remauthan efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT geelhoedjeanines efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT millansolsonaruben efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT fumagallilaura efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT nielsenlarspeter efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT franquetalexis efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT mancajeanv efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT gomilagabriel efficientlongrangeconductionincablebacteriathroughnickelproteinwires
AT meysmanfilipjr efficientlongrangeconductionincablebacteriathroughnickelproteinwires