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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.

SUBMITTER: Boschker HTS

PROVIDER: S-EPMC8238962 | biostudies-literature | 2021 Jun

REPOSITORIES: biostudies-literature

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

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

Nature communications 20210628 1

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 filame ...[more]

PMID: 34183682

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Project description:BackgroundCable bacteria are filamentous members of the Desulfobulbaceae family that are capable of performing centimetre‑scale electron transport in marine and freshwater sediments. This long‑distance electron transport is mediated by a network of parallel conductive fibres embedded in the cell envelope. This fibre network efficiently transports electrical currents along the entire length of the centimetre‑long filament. Recent analyses show that these fibres consist of metalloproteins that harbour a novel nickel‑containing cofactor, which indicates that cable bacteria have evolved a unique form of biological electron transport. This nickel‑dependent conduction mechanism suggests that cable bacteria are strongly dependent on nickel as a biosynthetic resource. Here, we performed a comprehensive comparative genomic analysis of the genes linked to nickel homeostasis. We compared the genome‑encoded adaptation to nickel of cable bacteria to related members of the Desulfobulbaceae family and other members of the Desulfobulbales order.ResultsPresently, four closed genomes are available for the monophyletic cable bacteria clade that consists of the genera Candidatus Electrothrix and Candidatus Electronema. To increase the phylogenomic coverage, we additionally generated two closed genomes of cable bacteria: Candidatus Electrothrix gigas strain HY10‑6 and Candidatus Electrothrix antwerpensis strain GW3‑4, which are the first closed genomes of their respective species. Nickel homeostasis genes were identified in a database of 38 cable bacteria genomes (including 6 closed genomes). Gene prevalence was compared to 19 genomes of related strains, residing within the Desulfobulbales order but outside of the cable bacteria clade, revealing several genome‑encoded adaptations to nickel homeostasis in cable bacteria. Phylogenetic analysis indicates that nickel importers, nickel‑binding enzymes and nickel chaperones of cable bacteria are affiliated to organisms outside the Desulfobulbaceae family, with several proteins showing affiliation to organisms outside of the Desulfobacterota phylum. Conspicuously, cable bacteria encode a unique periplasmic nickel export protein RcnA, which possesses a putative cytoplasmic histidine‑rich loop that has been largely expanded compared to RcnA homologs in other organisms.ConclusionCable bacteria genomes show a clear genetic adaptation for nickel utilization when compared to closely related genera. This fully aligns with the nickel‑dependent conduction mechanism that is uniquely found in cable bacteria.

Dataset Information

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

Publications

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

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