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A highly conductive fibre network enables centimetre-scale electron transport in multicellular cable bacteria.

ABSTRACT: Biological electron transport is classically thought to occur over nanometre distances, yet recent studies suggest that electrical currents can run along centimetre-long cable bacteria. The phenomenon remains elusive, however, as currents have not been directly measured, nor have the conductive structures been identified. Here we demonstrate that cable bacteria conduct electrons over centimetre distances via highly conductive fibres embedded in the cell envelope. Direct electrode measurements reveal nanoampere currents in intact filaments up to 10.1?mm long (>2000 adjacent cells). A network of parallel periplasmic fibres displays a high conductivity (up to 79?S?cm^-1), explaining currents measured through intact filaments. Conductance rapidly declines upon exposure to air, but remains stable under vacuum, demonstrating that charge transfer is electronic rather than ionic. Our finding of a biological structure that efficiently guides electrical currents over long distances greatly expands the paradigm of biological charge transport and could enable new bio-electronic applications.

SUBMITTER: Meysman FJR

PROVIDER: S-EPMC6739318 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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A highly conductive fibre network enables centimetre-scale electron transport in multicellular cable bacteria.

Meysman Filip J R FJR Cornelissen Rob R Trashin Stanislav S Bonné Robin R Martinez Silvia Hidalgo SH van der Veen Jasper J Blom Carsten J CJ Karman Cheryl C Hou Ji-Ling JL Eachambadi Raghavendran Thiruvallur RT Geelhoed Jeanine S JS Wael Karolien De K Beaumont Hubertus J E HJE Cleuren Bart B Valcke Roland R van der Zant Herre S J HSJ Boschker Henricus T S HTS Manca Jean V JV

Nature communications 20190911 1

Biological electron transport is classically thought to occur over nanometre distances, yet recent studies suggest that electrical currents can run along centimetre-long cable bacteria. The phenomenon remains elusive, however, as currents have not been directly measured, nor have the conductive structures been identified. Here we demonstrate that cable bacteria conduct electrons over centimetre distances via highly conductive fibres embedded in the cell envelope. Direct electrode measurements re ...[more]

PMID: 31511526

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Project description:Cable bacteria are multicellular sulfide oxidizing bacteria that display a unique metabolism based on long-distance electron transport. Cells in deeper sediment layers perform the sulfide oxidizing half-reaction whereas cells in the surface layers of the sediment perform the oxygen-reducing half-reaction. These half-reactions are coupled via electron transport through a conductive fiber network that runs along the shared cell envelope. Remarkably, only the sulfide oxidizing half-reaction is coupled to biosynthesis and growth whereas the oxygen reducing half-reaction serves to rapidly remove electrons from the conductive fiber network and is not coupled to energy generation and growth. Cells residing in the oxic zone are believed to (temporarily) rely on storage compounds of which polyphosphate (poly-P) is prominently present in cable bacteria. Here we investigate the role of poly-P in the metabolism of cable bacteria within the different redox environments. To this end, we combined nanoscale secondary ion mass spectrometry with dual-stable isotope probing (13C-DIC and 18O-H2O) to visualize the relationship between growth in the cytoplasm (13C-enrichment) and poly-P activity (18O-enrichment). We found that poly-P was synthesized in almost all cells, as indicated by 18O enrichment of poly-P granules. Hence, poly-P must have an important function in the metabolism of cable bacteria. Within the oxic zone of the sediment, where little growth is observed, 18O enrichment in poly-P granules was significantly lower than in the suboxic zone. Thus, both growth and poly-P metabolism appear to be correlated to the redox environment. However, the poly-P metabolism is not coupled to growth in cable bacteria, as many filaments from the suboxic zone showed poly-P activity but did not grow. We hypothesize that within the oxic zone, poly-P is used to protect the cells against oxidative stress and/or as a resource to support motility, while within the suboxic zone, poly-P is involved in the metabolic regulation before cells enter a non-growing stage.

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A highly conductive fibre network enables centimetre-scale electron transport in multicellular cable bacteria.

Publications

A highly conductive fibre network enables centimetre-scale electron transport in multicellular cable bacteria.

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